Psychological Review Copyright 1984 by the

1984, Vol. 91, No. 2, 185-215 American Psychological Association, Inc.

Asymmetric Neural Control Systems in Human Self-Regulation

Don M. Tucker and Peter A. Williamson
University of North Dakota
The neural systems controlling motor readiness can be distinguished from those
determining the brain's phasic response to perceptual input. We review evidence
on the neurotransmitter substrates of these systems, showing that they produce
qualitative changes in the flow of information in the brain: Dopaminergic activation
increases informational redundancy, whereas noradrenergic arousal facilitates ori-
enting to novelty. Evidence that these neurotransmitter pathways are lateralized in
the human brain is consistent with the left hemisphere's specialization for complex
motor operations and the right hemisphere's integration of bilateral perceptual
input. Principles of attentional control are suggested by the operational characteristics
of neural control systems. The affective features of the activation and arousal
systems are integral to their adaptive roles and may suggest how specific emotional
processes dynamically regulate cognitive function.

Recognizing that the two cerebral hemi-
spheres have unique psychological character-
istics raises the question of how the brain
functions as an integrated organ of mind. This
question followed Sperry's (1966) conclusion
that each hemisphere is capable of independent
mental processes. Finding that the two hemi-
spheres take opposite approaches to problem
solving—the left hemisphere structures infor-
mation analytically and the right hemisphere
perceives holistically—Levy (1969) speculated
on the origins of hemispheric specialization:
Analytic and synthetic cognitive processes may
have evolved in specialized hemispheres be-
cause they are inherently incompatible, re-
quiring different forms of neural organization.
Bogen and Bogen (1969) suggested that the
challenge of integrating the two hemispheres'
specialized skills is central to human creativity.
These early reports from split-brain research
considered the general meaning of hemispheric
specialization for human psychology. A sub-
stantial body of research has been generated
on brain lateralization since the initial corn-
Helpful criticisms of this paper and its ideas were pro-
vided by Bill Beckwith, Floyd Bloom, George Erikson,
Pierre Hor-Henry, Doug Heck, Marcel Kinsbourne, James
Penland, Esther Strauss, Rod Swenson, four anonymous
reviewers, and the associate editor of the Psychological
Review, Murray Glanzer.
Requests for reprints should be sent to Don M. Tucker,
Department of Psychology, University of North Dakota,
Grand Forks, North Dakota 58202.
185
misurotomy studies. Rather than attempt to
address the general significance of brain asym-
metry, most of this research has dealt with the
more specific issue of what cognitive charac-
teristics reliably differ between the two cerebral
hemispheres. In early studies of effects of uni-
lateral lesions, it was found that an intact left
hemisphere was required to deal effectively
with most verbal stimuli, whereas the right
hemisphere appeared more important to han-
dling nonverbal input (Kimura, 1961). There
were exceptions to this verbal/nonverbal dis-
tinction, however, and it soon became apparent
that it was important to consider not only
properties of the stimulus but the nature of
the cognitive operations the subject performed
on the stimulus information as well. When an
analytic perceptual or conceptual structure is
required, the left hemisphere seems to be called
upon, even with nonverbal stimuli (Levy, 1969;
Russo & Vignolo, 1967; Tucker, 1976). In
contrast, the right hemisphere's contributions
appear most important when a global or ho-
listic organization of the stimulus information
is necessary (Nebes, 1978). Hemispheric spe-
cialization seems to entail not only different
forms of conceptual structure, but different
forms of cognitive process. The left hemisphere
excels at tasks that require the ordering of
cognitive operations sequentially, whereas the
right hemisphere appears more adept at par-
allel processing (Bradshaw & Nettleton, 1981).
Although there are many issues in the re-
search on hemispheric specialization for cog-
186 DON M. TUCKER AND PETER A. WILLIAMSON
nition that remain controversial (see the com-
mentary on Bradshaw & Nettleton, 1981, for
example), the research to date has provided
an important neuropsychological model of
human cognitive operations. This model is not
based on some arbitrary, "black box" as-
sumptions on the nature of cognition, but
rather characterizes the psychological func-
tions of specific neural systems.
The significance of brain lateralization for
the psychology of everyday life has been em-
phasized by recent indications that emotional
processes are asymmetrically represented in
the brain. The evidence is now substantial that
the right hemisphere is essential to normal
emotional communication. Right-hemisphere
lesions disrupt the patient's ability to under-
stand emotion conveyed by facial expression
or tone of voice (Heilman, Scholes, & Watson,
1975). Certain right-hemisphere lesions cause
speech to become monotonic, without mean-
ingful affective intonation (Ross & Mesulam,
1979). Indications of the right hemisphere's
role in normal emotional communication in-
clude a left-ear advantage for interpreting
emotion in tone of voice (Safer & Leventhal,
1977) and a greater intensity of emotional
expression on the left side of the face (Sackeim,
Gur, & Saucy, 1978).
These findings suggest that much of the
conceptual organization of emotional infor-
mation occurs in separate neural regions from
verbal, analytic cognition. The right hemi-
sphere's skill in dealing with the nonverbal,
analogical representation of information seems
requisite to emotional communication. Its ho-
listic concepts appear well suited to the inte-
gration of information from sensory and vis-
ceral channels in emotional experience (Safer
& Leventhal, 1977). The right hemisphere's
cognitive capacities contrast with those of the
left hemisphere, which has been described as
nonemotional (Schwartz, Davidson, & Maer,
1975). The left hemisphere's analytic skill and
its capacity for sequential control of linguis-
tically ordered ideation seem essential to ra-
tional cognition, traditionally assumed to be
separate from emotion. Some evidence sug-
gests that the left hemisphere may normally
control and inhibit emotionality (Buck &
Duffy, 1980; Tucker & Newman, 1981). The
traditional view of emotion in psychology
(James, 1884; Schachter & Singer, 1962) holds
that the visceral manifestations of emotional
arousal are diffuse and undifferentiated and
must be cognitively categorized with reference
to the environmental context to achieve the
status of an emotion. Learning of the unique
characteristics of each hemisphere's cognitive
process can suggest specific ways that emo-
tional experience is conceptualized.
Much of the evidence on emotional asym-
metries thus may be explained by considering
hemispheric differences in the cognitive pro-
cessing of emotional arousal. But for additional
evidence, the direction of the cognition/arousal
relationship is reversed: A change in hemi-
spheric arousal seems to result in a change in
the individual's emotional status and cognitive
functioning. The depressive-catastrophic re-
sponse often observed with left-hemisphere
brain lesions (Gainotti, 1972) may seem an
appropriate reaction to the loss of function.
Yet following right-hemisphere lesions, some
patients show an inappropriately positive
emotional response (Gainotti, 1972). Deciding
whether the damaged or the undamaged
hemisphere produces the emotional changes
has been difficult; unilateral lesions have been
variously interpreted as disinhibiting contra-
lateral (Sackeim et al., 1982) or ipsilateral
(Tucker, 1981) hemispheric functioning. Fur-
thermore, recent evidence indicates that the
nature of the emotional response depends on
the caudality as well as on the laterality of the
lesion (Kinsbourne & Bemporad, in press;
Robinson, Kubos, Starr, Rao, & Price, in press;
Tucker, in press). Although there are complex
issues in this research that remain to be un-
derstood, it seems clear that unilateral lesions
can produce an imbalance in hemispheric ac-
tivation that is accompanied by emotional im-
balance.
Asymmetric patterns of hemispheric acti-
vation are also found in emotionally disordered
persons and in strong emotional states in nor-
mal persons. Poor right-hemisphere perfor-
mance has been observed during depression
in psychiatric patients (Bruder & Yozawitz,
1979; Flor-Henry, 1976; Goldstein, Filskov,
Weaver, & Ives, 1977) and during a depressed
mood in normal students (Tucker, Stenslie,
Roth, & Shearer, 1981). The left hemisphere's
level of activation also may be influenced by
emotional variables. Many schizophrenics ev-
idence both an overactivation and a dysfunc-
 NEURAL CONTROL
tion of the left hemisphere (Flor-Henry, 1976;
Gur, 1978). Trait-anxious college students
show several signs of characteristically high
left-hemisphere activation (Tucker, Antes,
Stenslie, & Earnhardt, 1978; Tyler & Tucker,
1982).
There are a number of unresolved issues in
interpreting the asymmetries of brain function
found with emotional phenomena (for reviews,
see Davidson, in press; Flor-Henry, 1979;
Gruzelier, 1981; Sackeim et al., 1982; Strauss,
in press; Tucker, 1981; Wexler, 1980). But
throughout this research there seems to be an
inherent relation between certain emotional
processes and certain patterns of hemispheric
activation. Kahneman (1973) suggested that
the brain self-regulates its level of arousal as
a function of the demands for cognitive pro-
cessing. Neural systems differentially regulat-
ing hemispheric activation would achieve an
important specificity of cognitive control.
Important progress has been made in recent
years in delineating the neural circuitry re-
quiring brain activity. This circuitry can ap-
pear inordinately complicated, the hodge-
podge results of evolutionary opportunism re-
working primitive forms of anatomical and
biochemical structure to serve increasingly
more complex functions. But major brain ac-
tivation and arousal systems have been char-
acterized, and the regulatory effects of these
systems are beginning to be understood.
In this article, we consider the neural sys-
tems regulating hemispheric function. Draw-
ing from the Pribram and McGuinness (1975)
formulation of attentional control in the brain,
we differentiate between a system controlling
motor readiness and a system controlling per-
ceptual responsivity. We review evidence on
the neurotransmitter substrates of these sys-
tems that suggests that they not only determine
the degree of brain activity but alter infor-
mation-processing operations qualitatively.
From a consideration of the apparent asym-
metries of these control circuits in the human
brain, we suggest that their distinct cybernetic
effects may be integral to both emotional and
cognitive features of hemispheric specializa-
tion.
Activation and Arousal Systems
Psychology's closest link with physiology has
been through concepts of arousal. Within the
187
James-Lange view (James, 1884), visceral
arousal provides the impetus for emotional
experience. From the demonstration by Yerkes
and Dodson (1908) that optimal performance
is disrupted by high or low arousal came the
important realization that psychological pro-
cesses themselves are dependent on the ap-
propriate physiological tone of their neural
substrate. Cannon's (1929) classic experiments
confirmed that it is the activation of the brain
rather than viscera that is relevant to emotional
arousal: With visceral nerves severed, emo-
tional behavior remained; lesioning of cortical
regions showed primitive emotional responses
to stem fom the hypothalamus.
Although much of human psychophysio-
logical research has focused on autonomic re-
sponses, this appears due at least in part to
the ability to measure peripheral correlates of
arousal. The characterization of brainstem ac-
tivation systems in animal experiments pro-
vided a solid framework for neurophysiological
concepts of arousal, and pioneering attempts
were made to apply these concepts to human
emotional phenomena (Lindsley, 1960). The
increasing recognition of arousal as a central
rather than a peripheral phenomenon led to
the realization that the brain must regulate its
functional capacity through altering its own
arousal level (Kahneman, 1973). Equally im-
portant is the recent differentiation of the con-
cept of arousal to accomodate functionally
distinct neurophysiological systems.
Pribram and McGuinness (1975) describe
two separate neural pathways in the spinal
cord, each with a unique mode of response to
stimulation. In one pathway, neurons increase
their firing in response to continued stimu-
lation; neurons in the other pathway decre-
ment their firing with repetitive input. At
higher levels of the nervous system the circuitry
becomes more complex, but each higher level
seems to have elaborated on these two basic
neural response modes.
Major controls on neural activity are exerted
by brainstem reticular activating centers. With
the appearance of the limbic system and basal
ganglia in evolution came more complex con-
trols over primitive arousal mechanisms, ex-
erted largely through inhibitory influences.
The limbic system appears to modulate hy-
pothalamic arousal processes. The hippocam-
pus tonically inhibits the function of the nor-
188 DON M TUCKER AND PETER A. WILLIAMSON
adrenergic and serotonergic brainstem regu-
latory centers (Vinogradova, 1970). In the
human brain, cortical controls on arousal
mechanisms have become highly developed.
In addition to the substantial interconnections
between frontal cortex and the limbic system
(Nauta, 1971), recent clinical and experimen-
tal evidence has shown the importance of re-
ticular and limbic connections with parietal
cortex in regulating arousal and attention
(Mesulam, 1981). The control structure of the
brain is not easily deciphered, but there ap-
pears to be a continuity in the principles of
neural control, from the most primitive spinal
pathways to the most highly evolved frontal
systems. Pribram and McGuinness (1975)
characterize the functions of two major reg-
ulatory systems: an arousal system producing
a phasic response to input and an activation
system maintaining readiness for action.
The arousal system emerges from elemen-
tary habituation phenomena in spinal and
brainstem pathways (Groves & Thompson,
1970). In higher animals, Pribram & Mc-
Guinness (1975) suggest that projections from
frontal cortex modulate the function of the
amygdala, which in turn feeds back to influ-
ence the hypothalamic control of arousal.
Given the recent clinical evidence on deficits
in arousal and attention (Heilman & Van Den
Able, 1980; Mesulam, 1981), it seems likely
that parietal cortex plays a major role in
arousal as well. Through the arousal system
the brain orients to novel input. Neural activity
is closely linked to information characteristics
of the environment. As with the classic ori-
enting response, arousal is augmented with
increasing novelty or complexity of the stim-
ulus, whereas repetitive input quickly produces
habituation. In a recent article, McGuinness
and Pribram (1980) specify the neurotrans-
mitter substrate of arousal: Reciprocal nor-
epinephrine (NE) and serotonin (5-HT) path-
ways proceed from brainstem nuclei, inner-
vating widespread brain areas to support alert
wakefulness and the brain's responsivity to
perceptual input.
A second system, activation, augments
neural activity for a different purpose: to
maintain a tonic readiness for action. Acti-
vation is regulated primarily by the basal gan-
glia of the extrapyramidal motor system (Pri-
bram & McGuinness, 1975). Activation is thus
integral to motor operations, supporting pos-
tural readiness and motivationally directed
action. In contrast to arousal, for which brain
activity is entrained to the stimulus infor-
mation, the attention directed by the activation
system is more internally controlled, more
characteristic of vigilance than of orienting.
Just as NE functions in a reciprocally bal-
ancing relation to 5-HT in arousal, dopamine
(DA) pathways from the brainstem substantia
nigra combine with cholinergic influences on
the basal ganglia to regulate activation
(McGuinness & Pribram, 1980).
In an intact organism, some coordination
between arousal and activation appears nec-
essary for integrated attention. Pribram and
McGuinness (1975) suggested that an effort
system centered on the hippocampus is re-
sponsible for an active, effortful regulation of
the balance between arousal and activation.
They suggest that the operation of the effort
system often corresponds closely to muscular
action and metabolism. The hippocampus has
important interactions with brainstem retic-
ular systems, and Pribram and McGuinness
(1975) argue convincingly that it mediates be-
tween behavioral activation and perceptual
arousal. But in our development of the Pri-
bram and McGuinness model, we do not in-
clude the effort construct, because it has at-
tributes of active, voluntary control of atten-
tion that seem to overlap with higher order
features of activation. The changes in motor
activity and muscle metabolism that Pribram
and McGuinness (1975) ascribed to effort
seem more easily attributed to the brain system
handling motor control than to the hippo-
campus.
Although in our usage the concepts of ac-
tivation and arousal are thus somewhat mod-
ified, we retain the major emphasis of the Pri-
bram and McGuinness formulation: The
neural circuits controlling motor readiness are
distinct from those regulating the brain's re-
sponse to perceptual input. Understanding the
operating characteristics of these control sys-
tems may lead to more specific concepts of
attention. Important clues to the qualitative
differences between motoric activation and
perceptual arousal are provided by research
on their neurochemical substrates.
 NEURAL CONTROL
Catecholamine Controls
Pribram and McGuinness (1975) discussed
a range of evidence that supports the differ-
entiation between activation and arousal.
These constructs refer to complex functions
of the limbic system and cortex as well as to
the more basic regulation of neural activity
by brainstem centers. Yet the brainstem con-
trol of neural activity, traditionally attributed
to the reticular activating system (Lindsley,
1960), is the most fundamental of the brain's
self-regulatory processes. The reticular acti-
vating system was initially considered as a sin-
gle entity operating in a unidimensional fash-
ion. However, a substantial body of literature
now shows neural activity to be regulated by
several distinct, neurotransmitter-specinc
pathways (Koella, 1982).
The most important pathways augmenting
brain activity are mediated by the catechol-
amine neurotransmitters, NE and DA. Al-
though the complex interdependence between
a number of neural regulators suggests caution
in interpreting the function of one pathway in
isolation, there are characteristic effects of al-
tering NE or DA neurotransmission. These
effects show how the systems changing the level
of neural activity can no longer be thought of
as diffuse and unidimensional but must be
recognized as producing qualitative changes
in the brain's information processing.
Noradrenergic Arousal
Norepinephrine is ubiquitous in the brain,
with noradrenergic fibers innervating the lim-
bic system, thalamic nuclei, and the entire
neocortex. The primary noradrenergic path-
way, the dorsal tegmental bundle, originates
in the pontine locus coeruleus and projects
rostrally to the median forebrain bundle and
limbic system, including the amygdala, hip-
pocampus, anterior olfactory cortex, and sep-
tum, as well as to the thalamus and neocortex
(Kostowski, 1980). This widespread inner-
vation of brain areas is remarkable, originating
from a relatively small number of NE cell bod-
ies in the locus coeruleus (e.g., 1,500 in the
rat brain). A large area of influence from a
central point of origin is suitable for a general
regulatory system (Clark, 1979). The NE fibers
enter the cortex at the frontal pole, ascend to
the superficial layers, and pass caudally in a
189
laminar, horizontal layer parallel to the outer
surface of the cortex (Emson & Lindvall,
1979). Although especially dense in frontal
cortex and the cingulate gyrus (Descarries &
Lapierre, 1973), NE fibers extend throughout
the cortex, with projections found in senso-
rimotor, auditory, and visual cortex (Emson
& Lindvall, 1979).
The role of noradrenergic neurotransmis-
sion in regulating the organism's general level
of arousal is shown by variations in the activity
of NE pathways with variations in the animal's
sleep/wake cycle. Some of the most infor-
mative studies have been with single-unit re-
cordings in the locus coeruleus of unanesthe-
tized squirrel monkeys (Aston-Jones & Bloom,
1981). These studies indicate that in many
cases the activity of the locus coeruleus an-
ticipates behavioral awakening and then co-
varies directly with the animal's level of alert-
ness in the waking state.
Noradrenergic function also appears im-
portant to short-term fluctuations in arousal,
particularly those caused by environmental
stimuli (Aston-Jones & Bloom, 1981). Con-
sistent with the Pribram & McGuinness (1975)
notion of arousal, the NE system appears re-
sponsive only to novel environmental stimuli,
and its activity declines with stimulus repe-
tition (Aston-Jones & Bloom, 1981).
A paradox in research on the functional
role of NE pathways has been that whereas
NE augments brain activity at a behavioral
level, it inhibits neuronal activity. Studies of
the effects of stimulation of NE pathways and
research with direct application of NE to brain
tissue have shown that, for all brain regions
studied, NE inhibits neuronal discharge
(Foote, Bloom, & Aston-Jones, in press). The
resolution of this paradox has provided further
insight into the specificity of the NE effect on
neuronal activity. Examining the response of
cells in monkey auditory cortex, Foote, Freed-
man, and Oliver (1975) found that NE inhib-
ited the spontaneous, background activity of
the cells, but augmented the cells' evoked re-
sponse to sensory stimulation. A similar in-
hibition of spontaneous activity, together with
facilitation of evoked responses, characterizes
the effect of NE on cerebellar cells (Freedman,
Hoffer, Woodward, & Puro, 1977). These
findings have led to interpretations of how such
cellular effects of NE could figure in its be-
190 DON M. TUCKER AND PETER A. WILLIAMSON
havioral role. Bloom (1979) suggested that the
NE influence may enable the target neurons
by making them more responsive to sensory
input.
The conventional notion of an activating
system, producing a direct and nonspecific in-
crease in neural activity, is thus inappropriate
to describe the effects of noradrenergic control.
Because NE modulation does not increase
neural activity directly, but enables respon-
sivity to environmental stimulation, this form
of neural control is inherently linked to ex-
ternal input. The augmenting of the brain's
responsivity to external stimulation has been
apparent in studies of locus coeruleus activity
in behaving animals (Aston-Jones & Bloom,
1981; Robbins & Everett, 1982).
These behavioral observations indicate that
it is specifically novel external input that elicits
locus coeruleus activity. An important issue
in neuropsychological research on the orient-
ing response has been how the brain deter-
mines that a change in the environment has
occurred (Pribram & McGuinness, 1975). So-
kolov (1960) proposed that the brain builds a
neuronal model of repetitive input and can
then respond with an orienting response when
new stimulation differs from the model. The
habituation to repetitive stimuli that occurs
within the NE pathways may help explain the
mechanism of orienting to novelty. Because
locus coeruleus neurons respond specifically
to novel stimuli, some sort of habituation
mechanism must influence either the afferents
to the locus coeruleus or the responsivity of
the locus coeruleus itself. Foote et al. (in press)
describe an apparent decrement in the trans-
mission efficiency of noradrenergic axons with
repeated stimulation, another possible mech-
anism for habituation. Although the respon-
sivity of the NE system as a whole may thus
decline with repeated stimulation, a more spe-
cific locus for the habituation effect, at the
particular neural pathways stimulated by the
sensory input, is also possible. The inhibition
of spontaneous firing by NE modulation seems
to maintain the target neurons in a ready state
for sensory input. Once they have responded
to the sensory input, these neurons may be
less enabled by NE's inhibitory influence.
The ability to consider the particular op-
erational characteristics of the noradrenergic
control of neural networks may be important
to understanding the role of NE in behavior.
There have been a number of attempts to as-
sociate the NE system with behavioral func-
tions such as learning, memory, anxiety, or
reward (see Bloom, Shulman, & Koob, in
press, for review). Often the rationale for how
NE is involved in these functions is less than
explicit. Few researchers have considered how
the effects of NE on its target neurons could
be relevant to its behavioral effects.
Largely from experiments in which animals
controlled electrical self-stimulation to various
brain regions, the hypothesis was developed
that NE pathways mediate reward (Crow,
1968; Crow & Wendlandt, 1976; Herberg, Ste-
phens, & Franklin, 1976; Mason & Iversen,
1975). However, further work with animal self-
stimulation has questioned whether NE is es-
sential to reward; animals continue to self-
stimulate when NE pathways are disrupted
(Bloom et al., in press). In contrast, lesioning
of the nigrostriatal DA pathway severely im-
pairs self-stimulation (Fibiger, Carter, & Phil-
lips, 1976).
These findings have been interpreted to in-
dicate that DA, rather than NE, mediates re-
ward in the brain. However, electrical self-
stimulation of the brain has important limits
as an analog of natural self-regulation (see
Liebman, 1983). Many of the requirements
for achieving reward in an ecological context,
such as directing perception toward rewarding
events and ignoring nonrewarding ones, are
not required in an intracranial stimulation
paradigm; NE appears linked to just this at-
tention to external perceptual events. To re-
ceive brain stimulation, the animal's only re-
quirement is to emit a motor response, and
motor control is regulated by the DA pathways
(Iversen, 1977). Some researchers observing
the decrements in self-stimulation with DA
lesions have suggested that it is the initiation
and maintenance of motor function that are
impaired with DA lesions (Fibiger et al., 1976;
Herberg et al., 1976).
Progress in understanding how the cate-
cholamine pathways are important to reward
thus requires moving from an unspecific as-
sociation of the neurotransmitter with the be-
havior toward a more definite notion of how
the change in neural activity mediated by the
transmitter may help carry out the information
processing and sensorimotor operations re-
quired for the behavior. A more specific ap-
proach may also be important to understand-
 NEURAL CONTROL 191

ing the role of NE in learning and memory. cleus and putamen, the neostriatum of the
The initial question has been whether NE me- basal ganglia (Iversen, 1977; see Bloom et al.,
diates learning. The more productive question in press, for a review of DA anatomy). A re-
may be how NE supports the attentional com- lated DA pathway is the mesocortical or me-
ponents of learning, such as by augmenting solimbic system, with cell bodies in the ventral
neural arousal to novel or rewarding events, tegmental nucleus and connections to limbic
or by habituating the brain's perceptual re- structures including the olfactory tubercle,
sponse to repetitious or unimportant stimuli. nucleus accumbens, central amygdaloid nu-
Studies of animals with lesions of NE path-cleus, and the lateral septal nuclei (Bunney &
ways suggest that they may be able to learn a Aghajanian, 1977). Dopamine receptors have
variety of tasks but are impaired in habitua- been observed in discrete areas of the frontal
tion. Mason & Iversen (1975), for example, cortex and in entorhinal cortex (Berger, 1977).
found that animals with neurochemical lesions Microiontophoretic studies have shown DA
of forebrain NE pathways still show the ca- receptors to be most abundant in deep cortical
pacity for simple learning but are slow to ex-layers (Bunney & Aghajanian, 1977), although
tinguish performance during nonreinforce- some penetration of the superficial layers also
ment. Similar observations are reported by seems to occur (Emson & Lindvall, 1979). The
Lorden, Rickert, Dawson, & Pelleymounter concentration of DA fibers in frontal cortex
(1980). Strains of rats with genetically high is substantial, with a marked decrease in den-
brainstem NE levels show increased explor- sity caudally (Saledate & Orrego, 1977). Some
atory activity and poor avoidance learning recent histochemical studies have indicated a
(Kempf, Greilsamer, Mack, & Mandel, 1974). lack of DA projections to posterior cortex
With NE depletion, rats continue to repeti- (Emson & Lindvall, 1979).
tively examine the same surroundings (Mason As with NE, studies of the effects of DA on
& Fibiger, 1979), as if the habituation process
target neurons have produced unexpected and
were inoperative. Reviewing evidence that NE- paradoxical results. Although an excitatory
depleted animals are more distractable by ir- influence on motor behavior accompanies an
relevant cues, impaired in discrimination increase in the activity of either the nigrostri-
learning, and resistant to extinction, Mason atal or the mesocortical systems, the primary
and Fibiger (1979) suggest that the locus coe-effect of DA on target neurons appears to be
ruleus NE system may be important to filteringinhibitory (Bloom et al., in press). It has be-
out irrelevant stimuli. They posit that the re-
come clear that any consideration of the effect
sistance to extinction shown by NE-depleted of DA on target cells in the striatum must
animals may stem from a greater reward value consider interactions with other neurotrans-
attached to irrelevant cues during acquisition.
mitters such as acetylcholine and GABA
A diverse array of attributes has thus been(Groves, 1983). Bloom et al. suggested that
associated with the NE system. It appears im- studies of DA effects at the cellular level have
portant to the animal's sleep/waking cycle, and
been less informative than those examining
shows the phasic responsivity to stimulus input
cellular NE effects, and that it may be nec-
that seems consistent with the Pribram and essary to work backward from the behavioral
McGuinness (1975) notion of arousal. Al- effects of DA to design experiments that may
though a confident interpretation of the nor- elucidate cellular mechanisms.
adrenergic influence on neural activity must Whereas NE is distributed throughout many
await further research, the evidence gathered brain regions, and thus may exert its regulatory
thus far suggests that this influence is not aeffects through widespread neuronal changes,
diffuse increase in activity, but a qualitative
the DA pathways appear to target more specific
form of neural control. A similar specificity structures. Dopaminergic controls on behavior
of regulatory effect is found for the second may be exerted specifically through altering
major catecholamine, dopamine. the function of these structures. Groves (1983)
Dopaminergic Activation considered ways in which the dopaminergic
influence on the neostriatum may alter the
The primary dopaminergic pathway in the extrapyramidal regulation of motor output.
brain originates from the substantia nigra in The efferents from the striatum regulate the
the brainstem and innervates the caudate nu- functioning of the globus pallidus, which in
192 DON M. TUCKER AND PETER A. WILLIAMSON
turn exerts an inhibitory control over thalamic
motor centers.
Although the nature of the basal ganglia
contribution to motor activity and the regu-
lation of this contribution by the several rel-
evant neurotransmitter systems remain to be
understood, the behavioral evidence on do-
paminergic function consistently indicates a
role in motor control. The facilitation of lo-
comotor activity by the mesocortical pathway
has been indicated by administration of DA
to the nucleus accumbens (Rossum, Broek-
kamp, & Pijenberg, 1977; Ungerstedt & Ljun-
berg, 1977). Whereas a reduction of muscle
tone is associated with increased NE (Cools
& Rossum, 1970), increased DA neurotrans-
mission augments motor activity. Spontaneous
locomotion appears dependent on an intact
DA network (Iversen, 1977). Correlational
studies have found spontaneous motor activity
to correlate closer with changes in DA than
in NE (Everett & Weigand, 1962).
Although DA systems thus target motor
functions, and do not appear to have the major
role in sensory processes shown by NE, they
do appear important to coordinating motor
output with perceptual information (Ljung-
berg & Ungerstedt, 1976), probably through
reciprocol innervation with thalamocortical
centers. The result seems to be an active, vig-
ilant attentional mode closely tied to motor
readiness. This form of attentional control
seems essential for adequate avoidance be-
havior. Both active and passive forms of avoid-
ance learning (Iversen, 1977) are impaired in
DA-depleted animals. When stress depletes NE
and dopaminergic behavioral stereotypy is ob-
served, animals exhibit increased motoric ac-
tivity, avoidance behavior, and fighting (An-
telman & Caggiula, 1977).
Because of its connections with the frontal
lobe and limbic system, the mesocortical DA
system is thought to be important to higher
order motivational processes (Bunney &
Aghajanian, 1977). Footshock stress does not
affect striatal DA but produces decreases in
mesolimbic DA and sharp DA reductions in
frontal cortex (Thierry et al., 1977). Iversen
(1977) proposes that, whereas all DA pathways
are important to supporting the organism's
general level of activity, the nigrostriatal system
handles sensorimotor integration and the me-
socortical system supports motivated inter-
actions with the environment.
As described above in the discussion of NE
in reward, the decrement in self-stimulation
with DA lesions appear to be due to a motor
dysfunction (Fibiger et al., 1976; Herberg et
al., 1976). Similarly, in research relating DA
impairment to learning and memory, the an-
imals' difficulty seems to involve response ini-
tiation specifically (Bloom et al., in press). Each
of the functions in which DA has been im-
plicated involves the common feature of motor
control, consistent with the Pribram &
McGuinness (1975) construct of activation as
motor readiness. Rather than simply increas-
ing motor activity diffusely or randomly, how-
ever, dopaminergic regulation seems to facil-
itate a tight control of behavior. It is the or-
dered, sequential organization of behavior that
is most impaired with DA depletion (Iversen,
1977). Iversen suggested that DA systems op-
erate to facilitate the selection of specific motor
acts and to determine the sequence in which
they are to be performed. The effects of ex-
cessive dopaminergic control on the animal's
behavior are remarkable and are instructive
in indicating the qualitatively specific nature
of dopaminergic activation. Iversen (1977) de-
scribed incremental levels of DA modulation
as first producing a restriction in the range of
the animal's behavior, then a further restriction
of responses to high-probability behavior that
is performed repetitively. With maximal DA
activation the animal continually repeats brief,
highly stereotyped motor sequences.
Self-Regulation Through
Activation and Arousal
Any complete account of the brain neu-
rochemistry relevant to behavior control must
deal with complex interactions among a num-
ber of systems. McGuinness & Pribram (1980)
emphasized the importance of the interaction
between dopamine and acetylcholine pathways
in the activation circuitry and between nor-
epinephrine and serotonin pathways in
arousal. Many other interactions are relevant
as well. Brain serotonin pathways originating
in brainstem raphe nuclei modulate not only
noradrenergic but dopaminergic function
(Quick & Sourkes, 1977). The monoamines
form only one class of brain substances with
major neuroregulator functions; amino acids
such as GABA influence the activity of large
 NEURAL CONTROL
neural networks, and important behavioral ef-
fects of brain peptides are now well docu-
mented (for a review see McGeer & McGeer,
1980).
Although the complexity of neurophysio-
logical processes is formidable, even a sim-
plistic model of neural control deduced from
the NE and DA literature may help clarify the
constructs of activation and arousal. Tradi-
tional unidimensional notions of arousal have
assumed that neural activity varies in a simple
quantitative fashion—greater arousal means
more neural activity of the same kind. But
this assumption is not consistent with the be-
havioral evidence on brain catecholamine sys-
tems. Neural control is inherently qualitative.
In this section we draw from the unique func-
tional effects of NE and DA modulation to
consider the adaptive cybernetics of activation
and arousal.
Control by Negative Feedback
The norepinephrine system supports per-
ceptual orienting, consistent with arousal, yet
this system achieves its major attentional con-
trol through increasing habituation. The sys-
tem responsible for augmenting neural activity
in response to perceptual input thus simul-
taneously decrements further response to in-
put. The dopaminergic activation system,
which increments brain activity to support
motor output, also produces a paradoxical ef-
fect, through simultaneously restricting the
organisms's behavior. With high levels of DA
modulation, the animal's behavior is reduced
to routinized stereotyped actions. Considering
these observations, we suggest that it is possible
to characterize the nature of qualitative neural
control: Arousal and activation regulate per-
ception and behavior through applying neg-
ative feedback.
Many if not all of the attentional effects of
noradrenergic arousal in the animal literature
are associated with a bias toward habituation
in response to repetitive input. This is seen
clearly in the impairment of habituation and
extinction in NE-depleted animals. A habit-
uation bias, although inherently a negative
control, has the important positive effect of
augmenting the brain's response to changes in
the input stream. This regulatory effect seems
integral to the orienting response and to the
exploration of novel environments. If it is as-
193
sumed that the habituation bias does not op-
erate indiscriminately, but may be subject to
motivational constraints, the function of the
NE system in differentially encoding relevant,
rewarding stimuli may be accomplished at least
in part through a general habituation bias that
produces inattention to nonrewarding stimuli.
Although a negative feedback effect can be
deduced solely from the behavioral evidence
on NE function, the importance of regulation
through negative feedback can be argued on
logical grounds as well. Consider the design of
an arousal system. The circuitry must increase
its functioning in response to perceptual input.
Yet in this response, by augmenting its func-
tional level, the system becomes increasingly
responsive to further input. With a constant
stimulus input to this simple arousal circuit,
a positive regenerative feedback loop ensues,
not unlike that when an amplifier's micro-
phone responds to its speaker, and the system
quickly escalates out of control. Because of
this inherent design problem, the neural con-
trol of arousal seems to have evolved within
pathways that decrement responses to repeated
stimulation, self-regulating through negative
feedback.
The control of output operations with ac-
tivation also entails negative feedback, but with
an opposite effect on the information flow. The
tonic level of neural activity maintained by
the dopaminergic system appears to be ac-
complished by increasing the redundancy of
the information in brain channels. This in-
creased redundancy is clearly apparent in the
behavior of an animal with overstimulated DA
pathways (Iversen, 1977): The animal's motor
output becomes dominated by progressively
fewer acts that are performed with increasing
frequency. The qualitative regulatory effect of
activation is thus opposite to that of arousal,
which decreases redundancy. Yet for motor
functions, a redundancy bias applies a negative
control not unlike the negative feedback on
perceptual responsivity provided by arousal.
Behavioral output requires constant change in
the motor channels. A redundancy bias re-
stricts change.
The need for negative feedback in the con-
trol of output operations can be appreciated
by considering an organism with a nonspecific
behavioral activation system. Given the pres-
ence of an arousal system incrementing neural
response to novel input, a nonspecific behav-
194 DON M. TUCKER AND PETER A. WILLIAMSON
ioral activation system with no regulatory bias
would simply increase the quantity of behavior
that is then controlled only by perceptual re-
sponsivity. Arousal would continually select
for novel action, disrupting the continuity of
motor sequences, and eventually causing the
organism's behavior to degenerate into a frenzy
of novel self-stimulation. Activation provides
a bias against change in the output channels,
thereby affording continuity and stability in
motor control.
Stability achieved through negative feedback
is a well-known principle in cybernetics, con-
trol theory applied to electronic systems (Wie-
ner, 1961). The instructive paradox of neural
control is that for bpth perceptual responsivity
and motor readiness there is at the same time
an increase in the neural activity of the system
and a negative feedback on the system's func-
tional operation.
Change Control
From the general principle that activation
and arousal systems modulate redundancy in
opposite ways, there are several corollaries with
implications for attentional control. Increasing
the redundancy in an information channel de-
creases the rate of information change. Perhaps
the most fundamental distinction between ac-
tivation and arousal made by Pribram &
McGuinness (1975) is that activation operates
in a tonic fashion, whereas arousal produces
a phasic increment in neural activity. These
operational characteristics follow from the dif-
ferential regulation of information change.
With a high redundancy bias the activation
system maintains not only the current infor-
mation content of the motor channels but also
the brain's functional readiness. Operating
under a habituation bias, arousal quickly dec-
rements brain activity under constant envi-
ronmental conditions.
The animal with an augmented redundancy
bias shows high activity in the motor system
but also a strong restriction on change in motor
output. The result is behavioral stereotypy. The
animal with high noradrenergic tone orients
specifically to novel input. This differential
emphasis on routinization versus novelty in Representational Scope
information processing may be intrinsic to dif-
ferences in the attentional requirements of
motor versus perceptual systems. In most per- resent information, these two neural control
ception, redundancy has little utility; given
some modicum of memory, data input need
not be repetitious. In motor control, however,
redundancy facilitates behavioral organization.
Not only is constancy in information channels
required to execute complex motor operations,
routinization and repetition are often neces-
sary for successful motor integration.
Quality of Change
Controlling the rate of change in a cognitive
system has an important effect on the nature
of the changes that occur. A change in be-
havioral or perceptual operations can be pro-
duced by a number of interacting motivational
and environmental determinants. Assuming
a limited capacity for change determination,
restricting the rate of change causes the changes
that do occur to be more thoroughly deter-
mined. In contrast, a habituation bias spreads
the system's determinant capacity over a larger
number of changes, and as a result, the average
change is less cognitively and motivationally
meaningful.
Control of the rate of information change
thus dynamically allocates the organism's
limited processing capacity. When a dopa-
minergic bias restricts the rate of change, in-
formation processing proceeds under a tight
form of regulation, where the cognitive and
motivational impetus toward change must be
substantial to overcome the negative feedback
of redundancy modulation. This tight regu-
lation may be necessary for the sequential
control of serial motor operations, which de-
pend specifically on intact dopamine pathways
(Iversen, 1977). Sequential control requires
that each behavioral transition is highly de-
termined in order to maintain the continuity
of the overall motor sequence.
In perceptual operations, however, the loose
regulation of a noradrenergic habituation bias
is appropriate to maximizing the informa-
tiveness of the input data. Rather than being
restricted to a given semantic or motivational
content, the animal's processing capacity is
allocated to the most novel—usually the most
informative—feature of the stimulus array.
Given limits to the brain's capacity to rep-
 NEURAL CONTROL
modes use storage resources differently. The
result is a difference in perceptual breadth, the
scope of the internal representation of the ex-
ternal surround. With habituation and min-
imal redundancy in the input stream, the
brain's working memory is soon filled with a
diverse array of unique data. This expansive
representational format seems appropriate for
many perceptual operations, where the sensory
apparatus allows the registration of a broad
range of information. With the bias against
change that occurs with redundancy modu-
lation, a constricted representational scope is
produced, with less unique information in
current short-term stories.
Although the tuning of representational
scope by the balance of activation and arousal
is essentially an attentional phenomenon, it
has fundamental implications for memory. In
communications, the best insurance against
information loss is redundancy. Operating with
finite memory resources, a redundancy bias
constricts the unique informational content of
current stores, producing redundant encoding
that facilitates the retention of that limited
content. A habituation bias saturates memory
with unique data, yielding a broad represen-
tational scope at the expense of data retention.
Internal and External Control
An intrinsic regulatory effect of altering the
balance between differential modes of redun-
dancy handling is a shift between internal and
external sources of information control. This
effect figures importantly in the nature of the
organism's relation to the environment.
Largely from his work with cortical lesions in
primates, Pribram (1981) concluded that re-
dundancy in the brain's processing of infor-
mation is influenced in an opposite fashion
by anterior and posterior cortical systems. The
frontal cortex facilitates redundancy, and this
assists the animal's internal control of behavior
in the face of a distracting environmental con-
text. With greater constancy in the information
channels, the animal can maintain a consis-
tent, ongoing internal determination of be-
havior.
Although in discussing redundancy Pribram
(1981) and Pribram & McGuinness (1975)
described cortical functions rather than pro-
cesses of activation and arousal, the different
195
controls on redundancy they describe at the
cortical level have much in common with the
functional effects of the neurotransmitter sys-
tems supporting activation and arousal. The
dorsolateral frontal cortex that is important
to maintaining redundancy and internal con-
trol has substantial anatomical connections
with the neostriatum and may have evolved
at least in part to extend and elaborate striatal
functions (Simon, Scatton, & Le Moal, 1980).
Simon et al. have shown that lesions to the
substantia nigra, disrupting the dopamine
pathway to the striatum, produce deficits in
delayed alternation in rats. It was delayed al-
ternation deficits in monkeys following dor-
solateral frontal lesions that suggested to Pri-
bram the importance of the frontal cortex to
increased redundancy in information pro-
cessing and internal control over behavior
(Pribram, 1981).
Pribram described the predominance of
frontal cortical influence as an episodic atten-
tional mode and contrasted it with the more
participatory mode of the posterior brain.
Through minimizing processing redundancy,
the posterior cortex maximizes the brain's
participation in the unique information of the
immediate environmental context (Pribram,
1981). The external control mode that Pribram
attributed to parietal association cortex is
consistent with the minimizing of redundancy
by arousal, and with the external attentional
orientation supported by the norepinephrine
pathways.
Because the increment in the activity of its
target neurons does not occur without simul-
taneous sensory stimulation (Bloom, 1979),
noradrenergic arousal is inherently controlled
by external input. Observation of activity in
the locus coeruleus shows it to coincide with
the animal's attention to external events (As-
ton-Jones & Bloom, 1981). When the animal
turns its attention from the environment to-
ward a more internal focus, such as in groom-
ing or consummatory behavior, locus coeru-
leus activity shows a marked decline (Aston-
Jones & Bloom, 1981). It is interesting in this
regard that endogenous opiate pathways from
the hypothalamus target the locus coeruleus
and appear to inhibit its activity (Henderson,
1983). The close link between the NE system
and external input is shown by the decrease
in locus coeruleus activity during rapid eye
196 DON M. TUCKER AND PETER A. WILLIAMSON
movement sleep (Foote et al., in press), when
the brain shows substantial electrophysiologic
activity but is minimally responsive to envi-
ronmental events.
The evidence on the behavioral effects of
NE and DA pathways suggests that the reg-
ulation of internal versus external control may
be intrinsic to the most elementary brainstem
controls supporting activation and arousal.
The increased redundancy with dopaminergic
modulation facilitates the internal control of
motor operations. A redundancy bias causes
the control of the information flow to be de-
termined by the brain's current information
stores: The current content of the information
channel serves as a reference for further pro-
cessing. The habituation bias that accompanies
arousal in the perceptual systems shifts control
of the data flow to external sources. With a
habituation bias, the current information con-
tents serve as a negative reference: Novelty is
selected for input.
The effects on short-term-memory alloca-
tion may be integral to internal versus external
control. A habituation bias loads storage ca-
pacity with new data, such that prior cognitive
representations can have less influence on the
current process. The locus of information
control shifts from a determination by pre-
vious, internal representations to determina-
tion by novel features of the external percep-
tual array. The shift between greater or lesser
redundancy thus differentially allocates the
brain's representational capacity between the
continuity of internal control versus maximal
participation in the embedding context.
Ecological Control
Although we have emphasized the infor-
mation-processing implications of opposing
redundancy biases, there are important prac-
tical implications for the animal's self-regu-
lation in an adaptive context. McGuinness and
Pribram (1980) suggested that activation is
important to motivation, and arousal is im-
portant to emotion. This alignment seems
congruent with the differential involvement of
these systems in efferent versus afferent pro-
cesses. It also emphasizes the close link be-
tween the attentional and the affective char-
acteristics of brain systems. Evolution has se-
lected efficient, multifaceted methods of neural
control. Attention is directed with reference
to the animal's motivational state; affective re-
sponses do not occur in isolation but directly
regulate coping strategies. A consideration of
the adaptive functions of NE and DA regu-
lation may further clarify the motivational and
emotional properties of activation and arousal.
The most elementary need for motor readi-
ness occurs in the fight-flight response. Faced
with a sudden threat, the animal must rapidly
engage the motor system. In this situation a
control problem arises that may have figured
in the evolution of the cybernetics of activation.
With a sudden and strong impetus for motor
activity, the animal's capacity to organize mo-
tor operations is likely to be overwhelmed.
Greater activity than order produces entropy,
and the animal responding to threat with sub-
stantial randomness in its actions is likely to
be eaten. By applying an inherent redundancy
bias to motor operations, the activation system
imposes order on the fight-flight response.
Representational scope is restricted; attention
is focused on a few high-probability actions.
Change control becomes tight, and actions are
highly determined. The animal engages in
practiced motor operations, such as routinized
escape paths or fight sequences that have been
rehearsed in play or in previous encounters.
As more complex ways of coping with threat
have evolved, they seem to have elaborated on
the regulatory features of activation. Avoidance
behavior is particularly impaired by lesions of
dopamine pathways (Antelman & Caggiula,
1977; Iversen, 1977). A redundancy bias
maintains a vigilant, tonic attention that seems
essential for avoidance. The constriction of
representational scope with increased redun-
dancy allows the animal to focus attention on
a narrow class of adaptively important stimuli.
In the laboratory, the internal control from a
redundancy bias allows the animal to avoid
distractions in delayed alternation tasks (Pri-
bram, 1981). In the wild, this same regulatory
effect may decrease the external control of at-
tention by novel, extraneous events and sup-
port the maintenance of a vigilant posture.
The regulatory effects of activation may be
important to approach behavior as well as to
avoidance behavior. In the control of eating,
for example, the lateral hypothalamic lesions
that impair feeding (Teitelbaum, 1971) are
now known to achieve their effects at least in
 NEURAL CONTROL
part through damaging the dopamine path-
ways that course through this region of the
hypothalamus. Specific lesioning of the do-
pamine nigrostriatal pathway produces
aphagia similar to that from lateral hypotha-
lamic lesions (Ungerstedt, 1971).
There are several control processes neces-
sary to organize approach or avoidance be-
havior. The cholinergic pathways seem im-
portant not just to motor readiness but to
memory (Coyle, Price, & DeLong, 1983). The
role of the hippocampus in balancing acti-
vation and arousal (Pribram & McGuinness,
1975) seems important for connecting an ef-
fective response to a relevant stimulus. Yet the
specific regulatory effect of a redundancy bias
may be an essential component in organizing
effective behavior patterns. When the animal
is motivated, high levels of activation produce
not only motor initiative but a tendency toward
redundancy in motor output. This decreases
novel, stimulus-elicited attention and behavior,
and increases the likelihood of behavior per-
formed repeatedly in the past. Given some
selection mechanism for relating behavior to
relevant cues, the redundancy bias of activation
may provide a regulatory substrate for the op-
eration of this mechanism, facilitating habit
formation in a motivated state.
At times of decreased motivational urgency,
when internal control is less important, it is
appropriate for the animal to allow its per-
ceptual capacity to be directed externally, by
the informational characteristics of the envi-
ronment. Because each novel event engenders
arousal, perception is directed by a simple
control process that does not require invoking
mechanisms of reward or punishment for its
explanation. By allocating attention to novel
environmental features, arousal allows the
perceptual system to maintain a continuously
revised and maximally comprehensive map of
the external context. This simple control loop
of arousal to novelty may be the primitive
anlage of unmotivated information processing,
such as the curiosity drive in primate attention
(Harlow, Harlow, & Meyer, 1950), and the in-
terest stimulating the human infant's cognitive
development (Izard, 1977).
There are also processes that link arousal
to reward mechanisms. In describing cortical
systems in attentional control, Mesulam (1981)
suggested that the cingulate cortex supple-
197
ments the parietal coordination of perceptual
data by providing information on the moti-
vational significance of objects in the external
surround. Given the particularly dense nor-
adrenergic innervation of the cingulate cortex
(Descarries & Lapierre, 1973), cingulate-pa-
rietal interactions may be important in higher
order direction of arousal.
The notion that NE pathways mediate re-
ward (Crow, 1968; Crow & Wendlandt, 1976)
clearly needs refinement (Bloom et al., in
press). The decrement in locus coeruleus ac-
tivity during consummatory behavior (Bloom
et al., in press) indicates that other systems
must direct important components of reward.
The contribution of arousal seems to be a more
specific and limited role: facilitating the ani-
mal's perceptual orienting to relevant events
and habituating the perceptual response to ir-
relevant events (Herberg et al., 1976; Mason
& Fibiger, 1979). Given some mechanism for
modulating arousal as a function of the adap-
tive significance of environmental stimuli, a
habituation bias would maximize the brain's
representation of, and external control by,
these stimuli.
Because noradrenergic enabling actually
primes the responsiveness of perceptual net-
works (Bloom, 1979), the response to ecolog-
ically relevant stimuli is not determined by a
secondary evaluation of what is perceived, but
entails a direct enhancement of the perception
of meaningful stimuli (see Gibson, 1979). As
suggsted by the essential role of NE pathways
in sexual responsiveness (Robbins & Everitt,
1982), arousal may prime the brain to respond
to events that are not only informationally
unique but are affectively interesting.
Asymmetric Cognitive Controls
The elementary regulatory controls of the
neurotransmitter pathways must be elaborated
by the functioning of higher level neural sys-
tems. The effects of the dopamine pathways
on motor control are mediated through the
operations of the basal ganglia. Given the sub-
stantial anatomical and functional intercon-
nections between frontal cortex and the basal
ganglia (Groves, 1983) and given that dopa-
minergic projections to the cortex appear re-
stricted to frontal regions (Emson & Lindvall,
1979), iit seems likely that the more complex
198 DON M. TUCKER AND PETER A. WILLIAMSON
attentional features of the activation system
depend on frontal structures. This link between
activation and frontal regions is consistent with
the redundancy attributed by Pribram (1981)
to frontal association cortex.
Frontal cortical systems are important to
arousal as well (Pribram & McGuinness,
1975), but the habituation bias of arousal sug-
gests a functional link with the perceptual rep-
resentation systems of the posterior brain: Pri-
bram (1981) suggested that the posterior as-
sociation cortex minimizes redundancy.
Mesulam (1981) reviewed recent evidence that
regions of parietal as well as frontal cortex are
interconnected with the brainstem centers that
regulate neural activity. These brainstem in-
terconnections with parietal cortex are specific,
including the locus coeruleus and raphe nuclei
of the noradrenergic and serotonergic pathways
(Mesulam, 1981), the primary neurotrans-
mitter substrates of arousal.
The operational characteristics of the ac-
tivation and arousal systems thus may be im-
portant to the differing attentional controls on
anterior motor versus posterior perceptual
functions. In addition to this front/back di-
mension, we suggest that activation and arousal
are important to a related dimension of brain
organization, the left/right axis of hemispheric
specialization. At the turn of the century,
Hughlings Jackson (Taylor, 1958) recognized
that the two hemispheres are not identical in
their handling of input and output operations.
Largely from his clinical observations of the
effects of cortical lesions, Hughlings Jackson
concluded that the left hemisphere is special-
ized for expressive functions, whereas the right
hemisphere is specialized for receptive func-
tions. The primary role of the left hemisphere
in higher order motor control is indicated by
a substantial body of clinical literature. In ad-
dition, many of the functions for which the
right hemisphere is specialized include major
perceptual components.
We propose that along with their differential
specialization for motor and perceptual func-
tions, the two cerebral hemispheres have be-
come specialized for the attentional controls
underlying those functions, the left hemisphere
utilizing the regulatory properties of activation,
and the right hemisphere relying on arousal.
Support for this proposal comes from recent
evidence that the relevant neurotransmitter
pathways are asymmetric in their distribution
and function.
Neurochemical Asymmetries
Pharmacologic stimulation of dopamine
pathways in rats often produces an asymmetric
increase in motor function, and the animals
turn in circles (Glick, Jerussi, & Zimmerberg,
1977). Mittleman and Valenstein (1982) ob-
served that a rat's eating behavior is regulated
by the nigrostriatal pathway innervating its
dominant hemisphere (i.e., the hemisphere
contralateral to the direction of rotation fol-
lowing amphetamine treatment). Although
Glick and associates observed that the direc-
tion of rotation depends on the individual an-
imal, Denenberg (1981) reanalyzed the Glick
et al. data and found a tendency toward higher
right turning in the group data, which sug-
gested a left-lateralization of the dopamine
pathways. In other research with rats, Glick,
Meibach, Cox, and Maayani (1979) found
higher levels of metabolic activity in left than
in right frontal cortex.
Glick and Ross (1981) proposed that the
asymmetry of dopamine pathways observed
in animal brains may be relevant to human
brain function. Glick, Ross, and Hough (1982)
reanalyzed data collected by Rossor, Garret,
and Iversen (1980) on human neurotrans-
mitter levels in various brain regions at au-
topsy. They found levels of dopamine and of
choline acetyltransferase, an index of acetyl-
choline activity, to be higher in the left than
in the right globus pallidus. Very recently, pos-
itron emission tomography has been used to
image the dopamine receptors of a living hu-
man subject (Wagner et al., 1983). Inspection
of the scan of this subject (Figure 2 of Wagner
et al.) shows the concentration of dopamine
terminals to be higher in the left than in the
right basal ganglia.
Indications of a left-lateralization of dopa-
minergic processes have also appeared in re-
search on schizophrenics. Because clinical im-
provement in this disorder occurs with ad-
ministration of neuroleptics, which are DA
antagonists, and because DA agonists such as
amphetamine can produce symptoms of
paranoid schizophrenia (Ellinwood, 1967), the
prevailing hypothesis in psychiatry is that
schizophrenia entials chronically high dopa-
minergic function (Meltzer, 1979). In light of
 NEURAL CONTROL
this hypothesis, it is relevant that schizophren-
ics have exhibited signs of high left-hemisphere
activation in behavioral (Gur, 1978) and elec-
troencephalographic (EEG; Flor-Henry, 1976;
Serafetinides, 1973) studies. More direct evi-
dence of DA lateralization was provided when
Serafetinides (1973) gave neuroleptics to a
sample of schizophrenics and observed a nor-
malization of the high left-hemisphere acti-
vation. Mintz, Tomer, and Myslobodsky (1982)
observed that in unmedicated schizophrenics,
the visual evoked potential was higher over
the left than over the right hemisphere. Mintz
et al. suggested this high left-hemisphere ac-
tivation may be associated with fragmented
attention. Medication with neuroleptics re-
versed the evoked potential asymmetry, dec-
rementing left-hemisphere activation and en-
hancing the visual evoked potential over the
right hemisphere (Mintz et al., 1982). Recently,
Laurian, Gaillard, Le, and Schopf (in press)
administered neuroleptics to normal subjects
and observed a decrease in EEG activation
that was most evident for left-hemisphere lo-
cations.
In data from a mixed sample of psychiatric
patients, Gottfries, Ferris, and Roos (1974)
found that the level of homovanilic acid, a DA
metabolite, in the cerebrospinal fluid was cor-
related with cortical evoked potentials from
the left but not from the right hemisphere.
The dyskinesias that occur following neuro-
leptic treatment have been observed to be more
frequent on the right side of the body (Waziri,
1980). Patients treated with certain neuroleptic
drugs that are particularly prone to producing
dyskinesias were found by Tomer, Mintz, and
Myslobodsky (1982) to show a high incidence
of right lateral eye movements during ques-
tioning—further indication that dopaminergic
motor control is left-lateralized in humans.
Although we have focused on dopamine
pathways supporting activation, McGuinness
and Pribram (1980) pointed to the interaction
of acetylcholine with dopamine pathways in
the motor readiness system. A recent study of
samples of left and right temporal cortex taken
from human brains at autopsy (Sorbi et al.,
1980) showed levels of choline acetyltransfer-
ase to be several times higher in the left than
in the right hemisphere. A similar cholinergic
asymmetry favoring the left cortex finding has
been reported by Kononeko (1980). Because
199
the inhibitory effect of GABA neurotrans-
mission may be important to modulating DA
function (McGeer & McGeer, 1980), the re-
cently observed asymmetry of GABA in the
substantia nigra (Rossor, Garret, & Iversen,
1980) is also relevant. Frumkin and Grim
(1981) suggested that the asymmetrical dis-
tribution of GABA may be associated with an
asymmetric effect of barbiturates on cortical
function.
These indications that the neurotransmitter
substrates of the motor readiness system are
left-lateralized are consistent with the left
hemisphere's direction of complex motor op-
erations. That the right hand is superior in
manual skill in most of the population attests
to a lateral asymmetry in motor control. In
right handers, the left hemisphere's importance
to coordinating bilateral motor functions has
been shown repeatedly in clinical investiga-
tions. Liepmann at the turn of the century
observed that apraxias often follow damage to
the corpus callosum. He suggested that the left
hemisphere uses its superior motor skill to aid
the right hemisphere's control of the left hand
(Geschwind, 1975). Even when complex motor
tasks are clearly nonverbal, left-hemisphere
damage often impairs performance more than
right-hemisphere damage (Kolb & Milner,
1981).
Kimura (1977) found that it is particularly
the appropriate sequencing of manual actions
that suffers from left-hemisphere damage. She
suggested that this sequential motor control
may be especially important to the left hemi-
sphere's articulation of speech. A similar view
was offered by Semmes (1968), who pointed
to the impairment in motor articulatory ability
that often accompanies aphasia. Rejecting the
traditional interpretation that the left hemi-
sphere's verbal monitoring ability explains its
importance to complex motor functions,
Semmes suggested that it is left-hemisphere
specialization for motor control that is the
more primary aspect of brain lateralization,
and that this may have led to its specialization
for language.
Semmes (1968) proposed that the right
hemisphere has developed a complementary
specialization for higher perceptual functions.
She cited evidence of the right hemisphere's
skill in topographic orientation, integrating
perceptual data to form a holistic map of ex-
200 DON M. TUCKER AND PETER A. WILLIAMSON
ternal space. The right hemisphere is superior
in a number of functions that require inte-
gration of bilateral perceptual information,
such as depth perception (Carmon & Bechtolt,
1969). To support this global integration of
perceptual input, the right hemisphere may
draw on the attentional control of the arousal
system. Studies of asymmetries in neurotrans-
mitter pathways and asymmetries in the effects
of psychoactive drugs suggest a right-lateral-
ization of the biochemical substrate of arousal.
Right-hemisphere lesions in rats are partic-
ularly influential on emotional behavior and
brain neurochemistry, with right-frontal le-
sions impairing NE pathways bilaterally. Rob-
inson (1979) found that ligation of the right-
but not the left-middle cerebral artery pro-
duced behavioral hyperactivity and decreased
ipsilateral levels of both NE and DA. Denen-
berg (1981) observed that, for rats given the
early sensory stimulation of handling, right-
hemisphere lesions were more effective than
left-hemisphere lesions in impairing taste
aversion and in decreasing mouse killing.
Because the NE pathways enter the cortex
at the frontal pole (Emson & Lindvall, 1979),
asymmetric effects of frontal-pole lesions ob-
served by Pearlson and Robinson (1981) are
particularly informative. Right-frontal lesions
produced behavioral hyperactivity and de-
creased levels of NE in the cortex bilaterally.
These lesions also decreased NE levels in the
locus coeruleus, the site of the primary nor-
adrenergic nuclei of the brainstem. Lesions of
the left-frontal cortex produced none of these
effects. Higher right- than left-hemisphere lev-
els of NE in rats have also been demonstrated
in assays of the thalamus (Oke, Lewis, &
Adams, 1980).
Assessment of post mortem samples of the
human thalamus (Oke, Keller, Mefford, &
Adams, 1978) shows NE to be higher in the
right than in the left hemisphere in several
areas, particularly in somatosensory nuclei. A
functional connection between NE and the
right hemisphere in humans is suggested by
the neuropsychological effects of variations
mood level. The catecholamine hypothesis of
the affective disorders (Schildkraut et al, 1978)
proposed that depression is associated with
low, and mania with high, levels of activity in
brain NE pathways. It appears to be right-
hemisphere arousal and function that is most
impaired in psychiatric (Flor-Henry, 1976;
Goldstein et al., 1977) and in normal (Tucker
et al., 1981) depression. When psychiatric de-
pressives show clinical improvement, the right
hemisphere's performance also improves
(Kronfol, Hamsher, Digre & Waziri, 1978).
Children treated for depression with tricyclics
show a specific improvemnt in right-hemi-
sphere cognitive functions (Brumback, Staton,
& Wilson, 1980).
The importance of the arousal system in
regulating the right hemisphere's functional
capacity is further indicated by asymmetries
in brain serotonin pathways, described by
McGuinness and Pribram (1980) as interact-
ing with NE in the control of arousal. In mice,
Mandell and Knapp (1979) found that sero-
tonin levels are usually asymmetric between
homologous left- and right-hemisphere re-
gions. Significantly, this asymmetry is de-
creased by the administration of lithium.
Lithium is often an effective treatment for
mania and is thought to stabilize serotonergic
neurotransmission (Treiser et al., 1981). In a
patient showing EEC asymmetry during a
manic state, treatment with lithium produced
a normalization of mood and symmetry of
the EEG (Harding, Lolas-Stepke, & Jenner,
1976). That the right hemisphere in humans
is more sensitive than the left hemisphere to
serotonergic controls is suggested by the ob-
servation of Gottfries et al. (1974) that right-
but not left-hemisphere cortical-evoked po-
tentials were correlated with cerebrospinal
fluid levels of 5-hydroxyindole acetic acid, a
serotonin metabolite. Furthermore, when Flor-
Henry & Koles (1981) administered lithium
to normal subjects, the EEG changes were
most pronounced over the right hemisphere.
These indications of asymmetries in brain
neurotransmitter pathways seem directly rel-
evant to the findings of altered hemispheric
function in psychopathology. Yet the question
becomes why are these pathways asymmetric
in normal persons. The functional aspect of
hemispheric specialization most relevant to
neurotransmitter asymmetries may be differ-
ential hemispheric involvement in perceptual
versus motor operations. Consistent with
Hughlings Jackson's (Taylor, 1958) initial ob-
servations, in its control of motor operations
the left hemisphere may have evolved to draw
on the active attentional control supported by
 NEURAL CONTROL
the dopaminergic and cholinergic pathways of
the motor readiness system. In its specializa-
tion for the holistic integration of perceptual
data, the right hemisphere may have come to
rely on the more receptive attention supported
by the noradrenergic and serotonergic sub-
strate of arousal.
Asymmetries of Active and
Receptive Attention
Investigators in recent studies of attention
have questioned how the differing cognitive
resources of the two hemispheres are allocated
to the task at hand. Friedman and Poison
(1981) suggested that each hemisphere may
represent a separate pool of processing re-
sources. A similar view of independent hemi-
spheric resources is held by Hellige and Wong
(1983). Although some degree of separate
hemispheric processing is suggested by these
studies, Sperry and Ellenberg (1980) showed
that an intact corpus callosum in normal sub-
jects integrates attention and precludes the
parallel, simultaneous task performance shown
by the two hemispheres of commissurotomy
patients.
In addition to the extensive transcallosal co-
ordination of the hemispheres in an intact
brain, the notion of separate hemispheric pools
of processing resources does not take into ac-
count what appear to be hemispheric differ-
ences in attentional priority. From observa-
tions of commissurotomy patients, Kins-
bourne (1974) described the priority given to
left-hemisphere operations when task demands
are high. When the two hemispheres of one
patient were given difficult tasks to perform
in parallel, the right hand (left hemisphere)
responded to the appropriate stimuli, but the
left hand (right hemisphere) responded reflex-
ively and inappropriately to each stimulus.
While tapping with both hands, a woman
commissurotomy patient was asked a difficult
question. As she reflected on her answer, her
right hand stopped tapping but her left hand
continued, apparently uninterrupted by the
attentional requirements of the question. In
recent research with normal subjects, Hayne,
Antes, & Tucker (1981) observed additional
evidence of left-hemisphere priority for active
attention. In a concurrent task paradigm, a
secondary task requiring left-hand response
did not interfere with the primary task, but a
201
secondary task requiring a right-hand response
appeared to compete for the attentional re-
sources required by the primary task.
These findings seem consistent with the tra-
ditional notion of left-hemisphere dominance,
which grew not only from the prominence of
the right hand in motor operations but from
the importance of language in directing human
behavior. The integral role of the left hemi-
sphere's verbal cognition in the development
of attention is shown by the self-verbalizations
that children use to maintain order and con-
tinuity in behavior (Luria, 1982).
That the left hemisphere is linked specifi-
cally to an active, vigilant attentional mode is
suggested by recent research by Dimond &
Beaumont (1971, 1973). Using an apparatus
that allowed signal lights to be lateralized to
the left and the right visual fields, Dimond &
Beaumont (1971) conducted a vigilance ex-
periment that required the subject to maintain
attention to respond to an unwarned stimulus.
Subjects showed an initial right visual field
superiority for this task, which declined after
several minutes apparently because of fatigue,
Dimond and Beaumont interpreted this find-
ing as evidence of the left hemisphere's control
of basic attention.
Yet other attentional tasks, which do not
require the vigilance of the motor readiness
system, may be performed better by the right
hemisphere. Heilman and Van Den Abell
(1980) also examined reaction time when sig-
nal lights were presented to the left and to the
right visual half fields (VHFs). In this study,
warning stimuli were presented prior to the
target signals, and it was these warning stimuli
that were lateralized. A significant asymmetry
was observed in the facilitation of reaction
time by the warning stimulus, with a superior
performance following left-field warning stim-
uli. In further experiments it was found that
left-VHP warning stimuli facilitated perfor-
mance with either right or left hands more
than did right-field stimuli. In addition to these
observations, Heilman & Van Den Abell
(1980) pointed to the impairment of behav-
ioral and electrodermal arousal with right-
hemisphere lesions, and the frequency of uni-
lateral neglect following damage to the right
hemisphere. They suggested that the right
hemisphere is specialized for controlling gen-
eral organismic arousal and attention.
202 DON M. TUCKER AND PETER A. WILLIAMSON
These differing conclusions on hemispheric
control of attention can be resolved only when
the construct of attention is differentiated from
the assumption of an inner homunculus look-
ing out on the world to describe specific con-
trols on the organism's information processing
(Posner, 1978). The attention required to
maintain vigilance in the absence of external
stimulation may be fundamentally different
than the orienting response to a warning stim-
ulus or to other external events. Pribram &
McGuinness (1975) suggested the former in-
volves the activation system, whereas the latter
involves perceptual arousal. Hemispheric spe-
cialization for attention may be explained by
the more fundamental hemispheric special-
ization for motor control versus perceptual in-
tegration. To complement the left hemisphere's
active direction of cognitive operations, the
right hemisphere may play an equally impor-
tant role in attention, supporting responsivity
to environmental events.
As Heilman and associates have docu-
mented (Heilman, 1979), the attentional ne-
glect following brain damage is asymmetric,
and is more severe with right-hemisphere le-
sions. Rather than indicating that the right
hemisphere handles all attention, however, this
finding implicates the receptive attentional
mode required to respond to environmental
surroundings. It is especially right-parietal
damage that produces unilateral neglect, and
the right hemisphere's role in spatially ori-
enting to the environment (Semmes, 1968)
may help to explain its importance to neglect
phenomena. In addition, given the connections
of the inferior parietal cortex with noradren-
ergic and serotonergic pathways (Mesulam,
1981), the asymmetry of unilateral neglect in
humans may be further evidence of the right-
lateralization of the receptive attentional con-
trols of arousal.
Another perspective on lateralized neural
systems in active and receptive attention is
provided by evidence on heart rate changes
with attentional demands. Lacey's (1967)
demonstration that specific cognitive tasks al-
ter heart rate in different ways has been an
important challenge to the traditional notion
that physiologic arousal is unitary (Duffy,
1962). Lacey's findings showed what he termed
directional fractionation: Heart rate acceler-
ated when subjects were requested to concen-
trate on internal cognitive operations, such as
mental arithmetic, and ignore or reject po-
tentially distracting environmental events.
When a receptive attention to the environment
was required, as in simple perceptual intake
tasks, heart rate deceleration was more likely.
Controversy over Lacey's interpretations has
focused on the possible confounding of atten-
tional variables with task demands for motor
readiness. Obrist, Webb, Sutterer, and Howard
(1970) pointed to evidence that heart rate ac-
celeration not only accompanies the metabolic
demands of motor activity but can occur in
anticipation of a motor response. If it is ac-
cepted that cognitive operations may utilize
the attentional controls of the motor readiness
system, it would seem reasonable that they
would engage the associated metabolic sys-
tems, even if minimal motor output is re-
quired.
In the environmental "rejection" tasks, the
subject withdraws attention from external in-
put and focuses on actively directing internal
cognitive processes. This would seem to be
facilitated by the internal control of activation.
The demands on short-term memory and the
need to monitor serial, sequential cognitive
operations in these tasks would also draw on
the redundancy bias of activation.
As Obrist et al. (1970) suggested, it is adap-
tive when preparing for action to prime the
cardiovascular system to handle the antici-
pated metabolic load. The evidence that ad-
renal activity is regulated by central dopa-
minergic pathways (Quick & Sourkes, 1977)
may suggest how engaging the active atten-
tional control of the motor readiness system
augments heart rate.
When the intake of environmental infor-
mation is required, a qualitatively different at-
tentional mode predominates. The organism
opens up sensory channels for receptive input.
As Pribram (1981) suggested, minimizing re-
dundancy serves to maximize the brain's par-
ticipation in the information of its immediate
environment. A noradrenergic habituation
bias not only broadens attentional scope, it
shifts control of the current information flow
to the outside. In this attentional mode the
motor system should be quiet; central NE ac-
tivity is associated with a reduction in muscle
tone (Cools & Rossum, 1970). The cardiac
deceleration during perceptual intake is not
 NEURAL CONTROL
unlike the more phasic heart rate slowing dur-
ing the orienting response to novel stimuli
(Graham & Clifton, 1966), and both may re-
flect noradrenergic arousal. Recent animal
studies have shown heart rate deceleration and
a decrease in blood pressure to accompany
release of NE in brain pathways (Tackett,
Webb, &Privitera, 1981).
The different forms of cognitive activity in
Lacey's research thus may have produced dif-
ferent effects on cardiovascular function be-
cause they engaged specific attentional control
systems that have evolved in concert with the
demands for the autonomic support of motor
operations. It may be that hemispheric spe-
cialization for these two attentional modes also
leads to specificity in the cognitive processes
indexed by cardiac function. Some of the cog-
nitive tasks thought to involve rejection of the
environment in the directional fractionation
research, such as mental arithmetic, would
seem to draw on the left hemisphere's cognitive
skills specifically. The frequency observed
heart rate acceleration prior to verbalization
(Campos & Johnson, 1967) may further in-
dicate the effects of activation with left hemi-
sphere cognition. Direct evidence of lateral-
izalion in the relation of cortical activity to
cardiac function has been provided by Walker
and Sandman (1979), who were initially in-
terested in whether cardiac activity influences
the brain through brainstem baroreceptors.
Examining evoked potential measures of cor-
tical arousal, they found an unexpected asym-
metry in their data, with higher responses from
right- than from left-cortical regions during
periods of low blood pressure and heart rate
deceleration.
Neural Cybernetics
At the most elementary level, the activation
and arousal systems determine the level of ac-
tivity in the brain. Even at this basic level, the
regulatory effects of activation and arousal are
specific and alter the information-processing
characteristics of neural networks. A cyber-
netic analysis, specifying the controls on the
brain's information handling, may show how
the regulatory effects of activation and arousal
cut across the boundaries of traditional sub-
divisions of psychology: arousal, attention,
memory, and concept formation. The same
203
control systems that are called upon as the
brain self-regulates its level of activity may be
called upon to self-regulate qualitative features
of cognition.
An important bridge between theories of
attention and questions of neural control is
Kahneman's (1973) proposal that the brain
self-regulates its arousal dynamically to meet
ongoing information-processing demands.
Kahneman, however, considers only quanti-
tative features of neural activity. A conven-
tional distinction in attention research is be-
tween the intensive and the selective aspects
of attention (Silverman, 1970). Kahneman
suggests that the brain's self-regulation of
arousal involves only the intensive aspects. The
recent evidence on the regulatory effects of
neurotransmitter systems shows that impor-
tant selective aspects of attention are altered
inherently by the systems controlling the
quantity of neural activity.
Increased activation and arousal produce
increased motor and perceptual activity, but
this activity is not diffuse. It is accompanied
by an inherent negative feedback on the func-
tioning of the motor and perceptual systems.
As we have described above, qualitative control
effects may be important to elementary motor
and perceptual operations. At more complex
levels of brain function, the cybernetic
uniqueness of the activation and arousal sys-
tems, their differing biases on informational
redundancy, may be integral to the cognitive
operations of the cerebral hemispheres.
In its specialization for coordinating per-
ceptual input, the right hemisphere shows
cognitive skills congruent with the habituation
bias of arousal. By decrementing the response
of perceptual networks to repetitive input, a
habituation bias enhances the brain's response
to novelty. In an ongoing stream of perceptual
processing, this effect decreases the attention
allocated to a given event and maximizes the
number of unique events that receive attention.
In contrast to a redundancy bias, which causes
a few events to be repetitively encoded in short-
term memory, a habituation bias saturates
memory stores with a broad range of unique
events.
The extensive coverage of the perceptual ar-
ray thus produced by arousal may be intrinsic
to a receptive mode of attention and many
support holistic perception. In describing the
204 DON M. TUCKER AND PETER A. WILLIAMSON
early stages of perception, Neisser (1967) sug-
gests that information processing is initially
global, organizing general patterns of stimulus
data into percepts of identifiable objects. This
preattentive processing is fast and automatic,
often insufficiently encoded in memory to be
subject to conscious examination. The neural
substrate of preattentive processing may be
arousal. In a novel context it operates to min-
imize redundancy in the input stream, max-
imizing the breadth of attentional coverage to
allow holistic perception.
The research on cognitive lateralization has
provided consistent evidence that the right
hemisphere is skilled in forming holistic per-
cepts (Bradshaw & Nettleton, 1981; Levy,
1969; Nebes, 1978). The right hemisphere's
neural architecture may be specialized to sup-
port global, cross-modal representations
(Goldberg & Costa, 1981; Gur et al., 1980;
Semmes, 1968; Tucker, Roth, & Bair, 1983).
As it became specialized in the course of evo-
lution for integrating perceptual processing,
the right hemisphere would have been directed
by the main regulatory mode of the perceptual
systems, arousal. Because minimizing redun-
dancy and maximizing information unique-
ness is inherent to neural networks controlled
by arousal, the right hemisphere developed the
cognitive capacity to maintain a global rep-
resentation of the present surroundings.
Other features of right hemisphere cognition
may also be consistent with the cybernetics of
arousal. Whereas the left hemisphere processes
information in a linear, sequential fashion, the
right hemisphere is better able to maintain
parallel processes simultaneously (Bradshaw
& Nettleton, 1981; Cohen, 1973). The broad
attentional coverage resulting from a habitu-
ation bias may allow cognitive resources to be
allocated across parallel operations. Instead of
focusing resources on a linear process, arousal
provides a low threshold for orienting to the
novel events that arise in the execution of par-
allel operations.
The risk of this control mode is straining
memory capacity such that the parallel op-
erations cannot be maintained and terminate
unproductively. Because memory resources
are spread thinly across multiple operations,
these operations when productive may not have
traceable semantic origins and may appear in-
tuitive.
In their theoretical review of the cognitive
lateralization literature, Goldberg and Costa
(1981) propose that the right hemisphere is
particularly important in handling novel sit-
uations. In the early stages of problem solving,
the individual must cope with a large amount
of new information with few existing cognitive
structures to help organize the information.
The right hemisphere's abilities in globally
representing an array of information and in
apprehending inherent patterns are undoubt-
edly relevant, but its contributions to handling
novelty may reflect even more directly the
control properties of arousal. The selection for
novel input is inherent to a habituation bias.
With its phasic and ephemeral attentional
response, the right hemisphere contributes to
novelty in problem solving by generating mul-
tiple ways of representing the available infor-
mation. Fixation on a single mode of approach
is perhaps the most frequent cause of failure
in human problem solving (Posner, 1973). The
flexibility, variety, and uniqueness of the right
hemisphere's representations of a problem
may result from the orienting to novelty that
occurs with control by arousal. Although there
are important disadvantages of this cognitive
mode, under optimal conditions the cyber-
netics of arousal may support the creative flex-
ibility of the right hemisphere in human imag-
ination (Bogen & Bogen, 1969).
From the activation system, on the other
hand, comes a bias toward increased redun-
dancy in information processing. By restricting
the range of events that are processed and in-
creasing the degree of processing for each
event, this redundancy bias produces a focal
attentional mode that may be integral to the
left hemisphere's analytic cognition.
The clearest evidence of increased redun-
dancy with activation is the highly routinized
motor output of animals with pharmacolog-
ically overstimulated dopamine pathways
(Iversen, 1977). In the interconnections of the
basal ganglia with frontal cortex, the motor
readiness system may support a higher form
of attention as well: the tonic, vigilant attention
of activation (Pribram & McGuinness, 1975).
Semmes (1968) suggests that the left hemi-
sphere's specialization for cognition is consis-
tent with its more basic specialization for mo-
tor control. Not only frontal, but posterior
association cortex in the left hemisphere con-
 - NEURAL CONTROL
tributes to directing motor output (Kolb &
Milner, 1981). We suggest that in addition to
allowing finely articulated motor operations,
left hemisphere specialization has occurred to
capitalize on the cybernetics of activation.
In considering the attentional mechanisms
underlying cognitive lateralization, Kins-
bourne (1974) proposed that the left hemi-
sphere controls focal attention. Recent exper-
imental findings are consistent with his hy-
pothesis. Alwitt (1981) varied hand of response
and global versus local processing require-
ments with normal subjects and found that
the left hemisphere is more adept than the
right in focusing attention for detailed pro-
cessing. Martin (1979) presented stimuli with
both local and global features to the two visual
fields and found that the left hemisphere was
superior in attending to local features.
The ability to focus attention allows a stim-
ulus to be analyzed into components. The left
hemisphere has been shown to adopt an an-
alytic cognitive approach with a variety of
stimuli (Bradshaw & Nettleton, 1981; Levy,
1969; Russo & Vignolo, 1967; Tucker, 1976).
Although the immediate effect of a redundancy
bias is to maintain constancy in attention, over
a period of time a succession of attentional
foci produce a differentiation of the stimulus
array into specific elements. This differentia-
tion of percepts or concepts may reflect a
higher order capacity of the left hemisphere
that depends on the more elementary control
of a redundancy bias.
The capacity for effective, adaptive differ-
entiations requires substantial semantic de-
termination. In analyzing a simple percept,
the visual informativeness of specific features
may be sufficient to determine the attentional
foci and thus the scheme of differentiation.
But with more complex instances of analytic
perception and cognition, the individual's se-
mantic networks, conditioned by previous ex-
posure to similar situations, must direct the
analytic process. Without this higher order de-
termination, the effect of a strong redundancy
bias may not be to differentiate experience,
but to fragment it. The fragmented perception
and cognition of the schizophrenic (Arieti,
1962; Mintz et al., 1982) may reflect a level
of dopaminergic redundancy beyond what can
be ,adaptively directed by the individual's se-
mantic capacities.
205
The effect of a redundancy bias on ongoing
operations is to routinize the sequence of those
operations. Although at extreme levels this may
produce pathological stereotypy, a moderate
degree of routinization may be essential for
developing cognitive skills. Goldberg & Costa
(1981) reviewed the nature of the tasks per-
formed well by the left hemisphere in exper-
imental studies. They concluded that the left
hemisphere is particularly adept in developing
practiced skills. After the right hemisphere ap-
prehends the initial patterning of novel infor-
mation, the left hemisphere organizes the pro-
cessing of this information in efficient, re-
peatable strategies.
Rourke (1982) suggested that these hemi-
spheric differences in handling novelty versus
routinization are integral to the child's cog-
nitive development. With its early maturation
(Whitaker, 1978) the right hemisphere facili-
tates building an experiential base by rapidly
comprehending a variety of novel situations.
But the capacity for complex cognition re-
quires well-routinized skills, such as the read-
ing, writing, and arithmetic of an elementary
education. Goldberg & Costa (1981) proposed
that the ability to routinize cognition is fun-
damental to the left hemisphere's competence
in linguistic and analytic problem solving.
It may not only be the child's development
of rudimentary cognitive skills but the expert's
development of sophisticated intelligence that
depends on adequate routinization. Descrip-
tive studies of the cognitive abilities that sep-
arate expert problem solvers, such as physicists
or chess masters, from novices show that the
experts have developed efficient routines for
conceptualizing elementary features of the
problem, and can then allocate working mem-
ory and processing resources to more general,
or more subtle, features of the problem (Newell
& Simon, 1972). Experimental studies of skill
in visual-search problems have shown that
initially the required cognitive operations must
be heavily controlled (Schneider & Shiffrin,
1977; Shiffrin & Schneider, 1977). Controlled
operations require substantial attention, place
heavy demands on short-term memory, and
must be processed serially. With repetition,
however, the operations become efficient and
seemingly automatic.
The redundancy bias of activation may be
the attentional substrate that allows the left
206 DON M. TUCKER AND PETER A. WILLIAMSON
hemisphere to build a repertoire of efficient
processing routines. Goldberg & Costa (1981)
suggested that the left hemisphere becomes
capable of descriptive systems, regularized
ways of representing information. Natural
language is the prototype descriptive system,
and the grammatical rules for processing the
verbal units allow complex and yet verifiable
semantic constructions.
Considering the cybernetics of primitive
biological systems, Bertalanffy (1968) de-
scribed the processes as being in dynamic in-
teraction; because the processes themselves are
dynamic and ephemeral, the effect of one pro-
cess on another is unique and transitory. This
dynamic and labile developmental stage con-
trasts with the more structured systems func-
tion that occurs in later stages of development,
when the operations become more regular and
routinized. Because they are repeatable, the
effect of one process on another at later stages
of development is not transitory, but can be
fixed as one aspect of a complex cybernetic
network. Although Bertalanffy discusses con-
trol processes in the development of organisms,
his systems-theory notions may illuminate
neural cybernetics as well. With the dynamic
interaction among its multiple processes, the
right hemisphere offers fast and global config-
uring of novel and unfamiliar information.
But developing structured and dependable se-
mantic interactions among cognitive opera-
tions may require the left hemisphere's ca-
pacity to establish and maintain a well-rou-
tinized descriptive system such as language or
mathematics.
The ability to package information in dis-
crete units, such as words or numbers, is nec-
essary for a regularized descriptive system. But
the fact that it operates in a verbal, digital
mode explains only part of the left hemi-
sphere's capacities. Its verbal representations
must be suitably processed, and several fea-
tures of left-hemisphere processing reflect the
redundancy bias of the motor readiness sys-
tem. By focusing attention, a redundancy bias
allocates available capacity to a serial mode,
handling one cognitive operation at a time.
With this dense, redundant encoding, the serial
operations are assured sufficient memory to
be available for thorough processing. They are
then not only repeatable, and communicable,
but reversible, such that the conclusion of a
given operation can be validated by tracing its
origins. Because a redundancy bias restricts
the rate of change, each change that occurs
can be highly determined. These several reg-
ulatory features emergent from a redundancy
bias may afford the capacity for logical thought.
At the level of logic or imagination, cog-
nition is more complex than can be described
by simple control principles, or even by single-
hemisphere models of cognition. The seman-
tics of the cognitive operations themselves exert
substantial control over elementary attentional
processes. Yet we suggest that there is a con-
tinuity that runs from the self-regulation of
neural networks to the self-regulation of con-
ceptual functioning. By studying the brain's
control of its arousal, we may learn much of
cognitive control.
Adaptive Human Self-Regulation
In animal research, activation and arousal
have clear adaptive roles. In humans as well,
the self-regulation of neural activity occurs in
an ecological context. Activation and arousal
must be closely linked to this context if they
are to be effective control systems. Several lines
of evidence on human self-regulation are con-
gruent with the suggestion that activation di-
rects motivation and arousal supports emotion
(Pribram & McGuinness, 1975). Evidence on
human drug abuse shows the powerful effects
of short-circuiting neurotransmitter pathways.
Evidence from studies of psychopathology
suggests how the abnormal brain chemistry of
schizophrenia and the affective disorders may
be relevant to the characteristic hemispheric
asymmetries shown by many of these patients.
Although the implications for normal emotion
are still controversial, there are indications that
a better understanding of the asymmetric
function of neural control systems may help
explain the differential contributions of the
two hemispheres to personality and cognitive
style.
External Control
The emotional importance of arousal in
humans is suggested by the increase in NE
activity associated with the use of mood-ele-
vating drugs, particularly in the initial, eu-
phoriant phase of their use. In normal subjects,
 NEURAL CONTROL
ingestion of alcohol increases NE turnover in
the brain (Borg, Kvande, & Sedvall, 1981).
Although the functional implication of this
increased metabolic turnover is uncertain, it
is interesting that alcoholics show an even
greater increase in NE turnover following al-
cohol ingestion (Borg et al., 1981). In rats,
brain levels of NE are also higher immediately
following alcohol intake, although a later effect
may be to deplete brain NE (Holman, 1983).
The possibility that alcohol effects are right-
lateralized in humans is suggested by greater
decrements in right- than in left-hemisphere
visual-evoked potentials following alcohol in-
take (Rhodes, Obitz, & Creel, 1975).
Although it is not related specifically to NE
effects, a connection between drug-induced
euphoria and the right hemisphere has been
suggested by Stillman et al. (1977). Considering
the parallels between cognitive effects of mar-
ijuana and the cognitive processes of the right
hemisphere, Stillman et al. gave subjects mod-
erate doses of marijuana and observed the ef-
fects on performance of verbal and pictoral
tasks presented tachistoscopically to the left
and to the right VHFs. Performance was
slowed generally. For pictoral stimuli this
slowing was greater for left- than for right-
hemisphere performance, consistent with the
hypothesis of greater right- than left-hemi-
sphere functioning in the drugged state. Gold-
stein and Stoltzfus (1973) examined the EEC
during euphoria produced by marijuana use
and found greater electrophysiological acti-
vation for the right than for the left hemi-
sphere.
The euphoria experienced soon after am-
phetamine use also appears to increase relative
right-hemisphere activity, and may be paral-
leled by increases in noradrenergic neuro-
transmission. Although the effects of am-
phetamine on brain chemistry are complex,
a major short-term effect seems to be a facil-
itation of brain NE pathways (Kokkinidis &
Anisman, 1980). The "high" of an acute am-
phetamine dose is paralleled by increased NE
metabolites in the urine, whereas the later
"crash" or depressive phase is accompanied
by markedly lower NE metabolites (Jones,
Maas, Dekirmenjian, & Fawcett, 1973). When
Goldstein and Stoltzfus (1973) gave amphet-
amine to humans, the short-term effect was a
small increase in right-hemisphere EEG ac-
207
tivation and a substantial decrease in left-
hemisphere activation.
Another popular euphoriant, cocaine, ap-
pears to potentiate NE neurotransmission
through decreasing its presynaptic reuptake
(Cooper, Bloom, & Roth, 1974). Administra-
tion of cocaine to mice increased the hemi-
spheric asymmetry of serotonin (Mandell &
Knapp, 1979). Given the initial suggestion that
serotonin pathways may be right-lateralized in
humans (Gottfries et al., 1974), these findings
with cocaine may suggest another connection
between mood elevation, the neurotransmit-
ters of arousal, and the right hemisphere.
The endogenous increase in mood level in
mania may also be accompanied by increased
noradrenergic arousal and augmented right-
hemisphere function. A direct relationship is
thought to exist between brain NE activity
and mood level (Maas, Dekirmenjian, & Faw-
cett, 1974; Schildkraut et al., 1978). The at-
tentional controls of a habituation bias may
be observable at high mood levels. The manic
habituates rapidly to repetitive input and then
seeks novel stimulation. With the heightened
functioning of the right hemisphere that may
occur in mania (see Dagani, 1981), cognition
becomes global (Kushnir, Gordon, & Heifetz,
1980) and expansive. With the loose regulatory
mode of arousal, the tnanic's cognitive asso-
ciations become loose (i.e., minimally deter-
mined).
The effect of arousal in orienting the brain
to external events may have affective as well
as attentional implications. For the manic, as
in euphoriant use, the emotional value of en-
vironmental events is heightened; ordinary
experiences may be described as thrilling. In
depression, concomitant with the decrement
in right-hemisphere function (Goldstein et al.,
1977; Tucker et al., 1981) the person's atten-
tional scope becomes restricted, and normally
gratifying events lose hedonic value.
Thus there may be a confluence of atten-
tional and affective characteristics in the op-
eration of the arousal system. Self-regulation
with arousal may not be limited to extremes
of mood level. It may be an integral aspect of
normal personality functioning, modulating
both the cybernetic and the phenomenological
aspects of the individual's responsiveness to
external events. Personality theorists since Jung
(1921/1971) have emphasized that extraver-
208 DON M. TUCKER AND PETER A. WILLIAMSON
sion describes not just a trait of sociability,
but the extent of an individual's psychological
reliance on external sources of control. Levy
(1982) theorized that the extravert's charac-
teristic optimism reflects a preponderance of
right-hemisphere influences in personality.
University students scoring high in extraver-
sion showed not only a right-hemisphere cog-
nitive style but a positive bias in self-descrip-
tion (Swenson & Tucker, 1983).
A substantial body of research by H. J.
Eysenck (1967) and his associates showed
marked differences in attentional capacity be-
tween introverts and extraverts; many of these
findings seem consistent with the extravert's
self-control with arousal. Extraverts are less
distracted by competing stimuli (M. W.
Eysenck, 1981), possibly due to a greater fa-
cility for parallel rather than sequential pro-
cessing. Extraverts habituate rapidly to un-
changing input (Stelmack, Bourgeois, Chain,
& Pickard, 1979). Perhaps because of their
rapid habituation, extraverts show poor vigi-
lance, and often seek out stimulating envi-
ronments (Wilson, 1981).
The adaptive deficiencies of an excessive re-
liance on arousal in self-control—what could
be described as pathological extraversion—
may be seen not only in the affective disorders
but in hysteric and impulsive personalities.
Studies of normal subjects who show hysteric
personality traits suggest that they favor a right-
hemisphere cognitive style (Dunivin & Zen-
hausern, 1981; Smokier &Shevrin, 1979). The
hysteric personality shows not only exaggerated
emotional responsiveness and expressivity,
which suggests an unmoderated right hemi-
sphere, but also a global and impressionistic
cognitive style (Shapiro, 1965). The deficiency
in deliberate, analytic reasoning skills in these
persons suggests inadequate left-hemisphere
contributions to thought processes.
The external control produced by a dispro-
portionate influence of arousal is reflected in
the hysteric's tendency to become caught up
in novel situations, impulsively forming in-
tense relationships and making radical changes
in living circumstances. Arousal is sufficient
to produce, but not maintain, the hysteric's
infatuation with novel persons or situations,
leading to short-lived, superficial relationships
and repeated adaptive failures (Shapiro, 1965).
Although it seems unlikely that the charac-
teristics of one neurotransmitter system can
be explanatory for a personality prototype,
there are interesting parallels between the ex-
ternal control facilitated by the enabling effect
of NE pathways (Bloom, 1979) and the ex-
ternal control required by the self-regulatory
style of the extravert or hysteric. Lacking the
internal control of activation, the person op-
erates with an incomplete set of adaptive cy-
bernetics and can only self-regulate through
being aroused by the emotional stimulation
of the current environmental context.
Internal Control
The active attention supported by activation
seems to arise from the system responsible for
rapid engagement of the motor apparatus in
the fight-flight response. Although the motor
readiness system and its redundancy bias are
important to a variety of motivational issues,
a primary function of activation seems to be
maintaining vigilance. As higher level strategies
for coping with danger have evolved from the
fight-flight response, they have continued to
be linked to the motor priming mechanism,
drawing on its unique cybernetics. The vigilant
attention supporting avoidance behavior in
animals is closely dependent on intact dopa-
mine pathways (Antelman & Caggiula, 1977).
Hypervigilance may also occur in humans with
excessive activation.
Although the short-term, euphoric effects
of amphetamine use are noradrenergic,
chronic use eventually overstimulates DA
pathways (Kokkinidis & Anisman, 1980). In
human amphetamine abusers, both attentional
and affective symptoms suggest a high degree
of activation. The behavioral stereotypies
shown by these persons (Ellinwood, 1967)
parallel those in animals with augmented DA
neurotransmission (Iversen, 1977). Matthysse
(1977) points out that dopamine blockers were
first shown to be clinically effective not with
schizophrenia, but with the motor stereotypies
of severely obsessive-compulsive patients. The
overly focused attention of the amphetamine
addict (Matthysse, 1977) may reflect a higher
order effect of activation, the constriction of
representational scope with a strong redun-
dancy bias. Amphetamine abuse eventually
results in compulsively analytic cognitive and
perceptual processing (Ellinwood, 1967), con-
 NEURAL CONTROL
sistent with a link between left-hemisphere
function and activation in humans. The
thought disorder characteristic of amphet-
amine abuse may stem from the affective as
well as the attentional features of activation.
The addict becomes hypervigilant and inap-
propriately avoidant, eventually manifesting
behavior and disordered cognition that is dif-
ficult to distinguish from paranoid schizo-
phrenia (Ellinwood, 1967).
The primary subjective experience of ac-
tivation may be anxiety. As it operates to prime
the motor system, activation engages an active
attentional mode with experiential as well as
cybernetic features. In anxiety, a tonic alertness
is maintained in anticipation of negative
events. One of the most common treatments
for anxiety is relaxation training, targeting the
muscle tension of chronic motor readiness. In
our research with normal university students,
we have found high trait anxiety to be asso-
ciated with high left-hemisphere activation
(Tucker et al., 1978) and an overly analytical
approach to visual perception (Tyler & Tucker,
1982). Students who were extremely anxious
showed a right-VHP performance decrement
(Tucker et al., 1978), which suggests an over-
activation of the left hemisphere not unlike
that observed in schizophrenics (Gur, 1978).
With increased anxiety, the individual be-
comes less directed by arousal in response to
emotionally stimulating events, and more in-
ternally directed. The increased internality
produced by the redundancy bias of activation
may be observed in the social withdrawal in
animals with pharmacologically stimulated
dopamine pathways (Kokkinidis & Anisman,
1980) and in the autism associated with the
apparent dopamine excess of schizophrenia.
In the self-regulation of normal personality,
introversion may result from a surfeit of ac-
tivation in the individual's control repertoire.
Although H. J. Eysenck (1967) interprets
the attentional differences between introverts
and extraverts in terms of unidimensional no-
tions of brain arousal, the attentional style of
introverts suggests activation specifically. Un-
like extraverts, introverts respond to a signal
stimulus with heart rate acceleration (Gange,
Green, & Harkin, 1979), which suggests a ten-
dency to engage the motor readiness system.
A related observation is that external locus of
control subjects respond with heart rate de-
209
celeration to bright colors, whereas internal
locus of control subjects do not (McCanne &
Lotsof, 1980). With a focused attention and
serial mode of information processing, intro-
verts are easily disrupted by distracting stimuli
(M. W. Eysenck, 1981). With the constancy
provided by a redundancy bias, introverts excel
in tasks requiring sustained vigilance (Krupski,
Raskin, & Bakan, 1971).
When personality operations are exclusively
centered on activation, the result may be the
tight self-regulatory style of the paranoid or
obsessive-compulsive personality (Shapiro,
1965). The increment in left- rather than right-
hemisphere processing with high activation is
seen in the prominence of analytic and intel-
lectual ideation in these personality styles. In
the paranoid personality, the analytic cognition
is closely linked to hypervigilance; in the ob-
sessive-compulsive it is a pervasive cognitive
mode and is used at the expense of noverbal,
imaginal ideation even when it appears forced
and intellectualized. In the extreme left-hemi-
sphere activation shown by many schizo-
phrenics (Flor-Henry, 1976; Gur, 1978), the
concomitant suppression of right-hemisphere
processing may produce blunted affect (Alpert
& Martz, 1977). In the obsessive-compulsive,
the right hemisphere's contributions to emo-
tional expressiveness in tone of voice or facial
display may be restricted, with an adverse effect
on interpersonal relations. Because the right
hemisphere's psychological processes are not
well integrated into the individual's conscious
functioning, when imaginal intrusions do oc-
cur they may be both primitive and threat-
ening.
A strong emphasis on activation as a self-
regulatory mode influences not only emotion
and attention but memory and problem solv-
ing. A redundancy bias operates in both spatial
and temporal domains. Spatially, increased
redundancy constricts representational scope.
This causes the obsessive-compulsive, when
not in an extreme or pathological state, to
succeed in tasks that require attention to detail.
In jobs that require global thinking, such as
in management positions demanding a view
of the "big picture," this personality style leads
to failure.
Applied to cognitive operations occurring
over time, a redundancy bias restricts change.
Under optimal circumstances, this form of
210 DON M. TUCKER AND PETER A. WILLIAMSON
control facilitates sequential, highly deter-
mined cognitive processing, leading to deci-
sions that are logical and deliberate rather than
impulsive or intuitive. But under an excessive
redundancy bias even a high degree of se-
mantic determination is insufficient to pro-
duce change. The obsessive-compulsive be-
comes ambivalent and indecisive, preoccupied
with many possible considerations but unable
to act.
The routinization produced by the redun-
dancy of activation can have important adap-
tive effects, allowing the person who uses this
self-regulatory mode to achieve order and ef-
ficiency in a job or in a lifestyle. But in less
optimal circumstances, as anxiety and its con-
trol effects become chronic, routinization be-
comes intense. The obsessive-compulsive
manifests cognitive and motor stereotypies, the
mental ruminations and behavioral rituals that
are symptomatic of this disorder.
Attention and Survival
In this article we have crossed several levels
of analysis, ignoring important complexities
in both neural and psychological systems, to
emphasize what seems to be a fundamental
continuity running through the control struc-
ture of the brain. In the course of evolution,
certain neural control algorithms appeared
that were effective in regulating sensory and
motor operations. Each new level of brain or-
ganization could not replace these fundamen-
tal processes, but elaborated on their regula-
tory characteristics. By understanding the
principles of sensory and motor control in
simple animals we may better understand the
biological foundations of our own cognition.
From an evolutionary perspective, the con-
tinuity in the brain's organization seems nec-
essary. In the process of evolution, each suc-
cessive version of neural cybernetics was re-
quired to be adaptively functional. There was
no hiatus in survival demands to allow time
out for major design changes.
In humans, neural control principles must
now function in new arenas, not just in in-
dividual brains, nor in the family and hunting
groups in which human behavior evolved, but
in the self-regulation of nations. It remains to
be seen whether the emotional and attentional
controls appropriate to earlier stages of evo-
lution will continue to serve us adequately in
handling the technology of a nuclear age. In
the time frame of evolution, the context for
self-control has suddenly changed. But the re-
quirement to remain continuously adaptive is
still in effect for us as it was for our evolu-
tionary predecessors: Extinction is still the
price of inadequate self-regulation.
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