10 Am J Psychiatry 146:1, January 1989

Special Articles
A Biological Perspective on Em pathy
Leslie Brothers, M .D.
During the evolution of the primate CNS, organiza-
tion of neural activity has been shaped by the need for
rapid and accurate evaluation of the motivations of
others. Using a broad biological approach, the author
considers empathy from evolutionary, ontogenetic,
and neurophysiological viewpoints. Emotional com-
munication follows a developmental course in primate
evolution and in individuals: specialized neural activity
and CNS organization subserve the interpretation of
social signals. Neurophysiological studies now in prog-
ress may shed light on fundamental questions about
the nature of empathy.
(Am J Psychiatry 1989; 146:10-19)
T he integration of psychology and neuroscience is a
m ajor contem porary challenge. The earliest m od-
em attem pt to bridge high-level psychological theory
and neuroscience was Freuds Project for a Scientific
Psychology (1), an attem pt that failed for two rea-
sons. First, the contem porary paradigm s dom inating
physiology, borrowed from nonbiological sciences,
were ill-suited to the phenom ena Freud was trying to
explain (2). Second, com pared with current knowledge
at least, the data available about neurons were very
lim ited. By contrast, the prospects for successful inte-
Revised version of a paper presented at the University of Califor-
nia, Los Angeles, Departm ent of Psychiatry Research Dinner Con-
ference, April 23, 1987. Received Sept. 16, 1987; revision received
Feb. 22, 1988; accepted April 1, 1988. From the Departm ent of
Psychiatry, Sepulveda VA M edical Center, Sepulveda, Calif., and the
Division of Biology, California Institute of Technology, Pasadena.
Address reprint requests to Dr. Brothers, Division of Biology (216-
76), California Institute of Technology, Pasadena, CA 91125.
Supported in part by Physician Scientist Award M H-00629 from
NIMH.
The author thanks Drs. John Allm an, David M arkel, George Pig-
m an, and Jam es Sabry for helpful com m ents on the m anuscript and
Dr. Peter Tanguay for exchanges on infantile autism .
Copyright 1989 Am erican Psychiatric Association.
gration are increasingly prom ising at our current stage
of understanding because of advances in both psychol-
ogy and neuroscience.
Biologists have com e to insist on paradigm s that ad-
dress the characteristics of biological subject m atter,
which are in certain ways unique within the natural
sciences (3, pp. 51-59; 4). Organized com plexity is the
hallm ark of living form s (5). Adequate paradigm s
m ust take into account that organism s have a histori-
cal nature and that the patterned com plexity of living
system s is hierarchically organized, giving rise to the
em ergence of novelties. Furtherm ore, biological pro-
cesses obey physiochem ical laws, but biological con-
cepts cannot be reduced in any m eaningful way to the
language of physics or, for that m atter, to the language
of biological phenom ena at different levels of descrip-
tion. To cite an exam ple from genetics, the concept of
inclusive fitness cannot be reduced to the concepts of
base pairing or transcription and translation. Yet, a
knowledge of these m olecular and cellular m echanism s
is necessary for an understanding of the physical pro-
cesses from which inclusive fitness arises. This exam ple
from transm ission and m olecular genetics is illustrative
of the relations we m ay expect to find between psy-
chological events and neural events. It also dem on-
strates the im portance of paradigm s that are adequate
to deal with organized com plexity.
Not only do biologists have better conceptual tools
now than at the turn of the century, the sheer am ount
of data about neural operations that has been accum u-
lated is im pressive. Because of this, optim ism is run-
fling high and, at least in som e circles (6), eventual
reduction of psychological concepts to neural ones is
anticipated, especially in the areas of learning, where
the work of Kandel is frequently cited, and m em ory,
where advances m ade by Squire, M ishkin, and
Thom pson com e to m ind. Nevertheless, im portant ad-
vances rem ain to be m ade in the area of the relations of
parts of the brain, since it is from these relations that
functioning arises. Sheer num bers of facts about ion
channels do not add up to clinical phenom ena. The
LESLIE BROTHERS
Am J Psychiatry 146:1, January 1989 11
issue of reduction in biology has been cogently ad-
dressed by M ayr (3, pp. 59-63) and will not be further
taken up here.
Because of the staggering com plexity of even
sim ple invertebrate brains, the explanatory power
of the neurosciences rem ains quite lim ited; it is even
m ore lim ited as the relatively huge prim ate brain is
approached. Such fundam ental questions as How is a
m otor m ovem ent initiated? How is a visual pattern
perceived? and How does function return after neural
dam age? rem ain unanswered. W hen a discipline is im -
m ature it benefits from interaction with and refinem ent
by neighboring disciplines at higher and lower levels
(6, 7). At the present tim e, therefore, there is a definite
role for psychological concepts as organizers of the
neuroscientific quest. However, two caveats m ust be
kept in m ind. First, the psychological concept m ust be
sufficiently strong and valid-qualities that m ay not be
predictable in advance-to be heuristically useful in
illum inating previously obscure issues at neural levels.
Second, one-to-one reduction across levels should not
be anticipated.
A high-level concept that appears to have great po-
tential utility in bringing together neural and psycho-
logical data is that of em pathy. I will show that the
concept of em pathy links data from the disciplines of
ethology, child developm ent, psychoanalysis, and neu-
rophysiology. I will also offer som e speculation regard-
ing future developm ents in defining the neural sub-
strate of em pathy.
Before proceeding to definitions of em pathy, I will
address potential points of confusion. The term em -
pathy is subject to the sam e difficulties as
em otion-a notoriously difficult concept dem anding
a com prehensive theory spanning the som atic, sub jec-
tive, and interpersonal fram es of reference. Scott (8)
has pointed out that a system s theory approach to
em otion is essential. Like em otion, em pathy encom -
passes all three fram es of reference and can be m ost
effectively studied by considering all three levels m di-
visibly. In this essay, the word em pathy will be used
in discussion of interpersonal phenom ena. In describ-
ing studies of anim al behavior, however, em pathy
would seem anthropom orphic, and so the phrase
em otional com m unication will be used in that con-
text. In discussion of neural activity, phrases such as
processing of social-em otional signals will be used.
In this way, language that would seem to im pute em -
pathic properties to neurons will be avoided. The vary-
ing types of language are chosen to conform with our
usual way of talking about the subject m atter, be it
ethological, neuronal, or intrapsychic; nevertheless,
the unity of the phenom ena under discussion should be
kept in m ind.
An additional prelim inary note: historically, facial
expression has received much m ore attention in the
ethological literature relating to em otion (9, 10) than
have other form s of em otional expression-vocal
expression, for exam ple. For the purposes of this dis-
cussion, which draws on data obtained in several
fields, consideration of the em pathic process will be
lim ited m ostly to visual pathways of inform ation. This
is sim ply because m ost of the neural data available at
present refer to this channel. It is not, however, to deny
recognition to a growing body of research aim ed at
vocal em otional com m unication in a variety of species
(11-15).
PSYCHOANALYTIC THEORIES AND DEFINITIONS
OF EM PATHY
The Germ an word Einfuhlung apparently was first
used to refer to interpersonal knowledge in the early
1900s by the psychologist Theodor Lipps (16), who
adopted it from the then-neighboring discipline of aes-
thetics (paper in preparation by Pigm an). The term
enjoyed wide circulation in European academ ic circles
in the early decades of the twentieth century and was
used by Freud in his writings with surprisingly little
com m ent. Perhaps Freud did not write about em pathy
because Lipps-whom Freud adm ired and whose writ-
ings apparently were well-known to Freud (17)-had
already written on the subject extensively. Our word
em pathy, according to Lee (18), is a neologism at-
tributed to E.B. Titchener, who coined the word from
Greek roots specifically for the translation of Em-
fuhlung. Em pathy as a concept of theoretical im por-
tance to psychoanalysis em erged with the contribu-
tions of Kohut (19-21). In the past two decades the
concept has begun to stim ulate interest coincident with
growing attention to Kohuts self psychological theory.
I now turn to theories of em pathy. Freuds discus-
sion (22) has been translated as follows: A path leads
from identification by way of im itation to em pathy,
that is, to the com prehension of the m echanism by
m eans of which we are enabled to take up any attitude
at all towards another m ental life (p. 110, note 2).
From this follows the classical psychoanalytic expla-
nation of em pathy as given by Fenichel (23): Em -
pathy consists of two acts: (a) an identification with
the other person, and (b) an awareness of ones own
feelings after the identification, and in this way an
awareness of the objects feelings (p. 511).
These definitions include both the outcom e (an
awareness of the other persons feelings) and the pro-
cess (identification, for exam ple) whereby the outcom e
is achieved. Hoffm an (24) defined the em pathic re-
sponse as a vicarious affective response; that is, the
observer responds as if he were experiencing the sam e
affect as the m odel (p. 228). Separately, Hoffm an
considered several m echanism s that m ight give rise to
the em pathic response, including classical conditioning
and m otor m im icry com bined with varying degrees of
reliance on cognitive appraisals (p. 233).
Basch has written extensively on em pathy as a psy-
choanalytic concept; his review of the subject (25) is
recom m ended. In particular, Basch (25) took up and
rejected the notion of identification as the basis for
em pathy, preferring som atic m im icry instead:
BIOLOGICAL PERSPECTIVE ON EM PATHY
12 Am J Psychiatry 146:1, January 1989
A given affective expression by a m em ber of a particular
species tends to recruit a sim ilar response in other m em -
bers of that species . . . . This is done through the prom o-
tion of an unconscious, autom atic, and in adults not nec-
essarily obvious, im itation of the senders bodily state and
facial expression by the receiver. This then generates in the
receiver the autonom ic response associated with that bod-
ily state and facial expression, which is to say the receiver
experiences an affect identical with that of the sender. (p.
108)
Som atic, or m otor, m im icry as an explanation of em -
pathy was also put forward by Lipps (16) but m ay
have derived from other, earlier sources (paper in prep-
aration by Pigm an).
Kohut (20) wrote, Em pathy is a m ode of cognition
which is specifically attuned to the perception of corn-
plex psychological configurations (p. 300). For the
purpose of interdisciplinary investigation, Kohuts is a
quite satisfactory definition of a m ysterious process
inasm uch as it avoids depending on any other high-
level concepts. It is no m ore abstract than the state-
m ent that vision is a m ode of cognition which is spe-
cifically attuned to the perception of light-reflecting
objects-which straightforwardly leads to the study
of the visual system using light-reflecting objects as
stim uli.
From a spare definition such as Kohuts, one can
construct hypotheses em bracing the som atic level of
description, such as Baschs cited earlier in this paper,
which are testable by using appropriate stim uli. Alter-
native hypotheses to Baschs would be, for exam ple,
that em otional expressions are perceived on a purely
sensory basis, without m otor accom panim ent, through
classical central pathways. The perceptions are then
associated with the observers past subjective experi-
ences, leading finally to lim bic activation and concur-
rent autonom ic and m otor patterns (e.g., an ultim ate
change in heart rate and facial expression in response).
This is the conditioning m odel. A third hypothesis
would postulate a slowly processing pathway with
m ultiple synapses in classical sensory and association
cortices, acting in parallel with a rapidly processing
oligosynaptic pathway that m ight be responsible for
fast adaptive m otor and autonom ic responses to easily
abstracted features such as loud, loom ing, or
teeth. In this third case, the subjective experience
would then arise from both the elaborate central eval-
uation of the social signal and the autonom ic activity it
has already set into play. Students of the history of
research on em otion will note the com bination of
Schachter and Singers theory of cognitive appraisal
(26) and the Jam es-Lange theory of som atic equiva-
lence (27) in this latter m odel. The procedures for test-
ing these m odels are discussed later in this paper.
A final glance at the status of em pathy in psycho-
analysis reveals that it is transcending its role as a tool
for the gathering of clinical data and becom ing a cen-
tral concept in theories of psychopathology. Briefly,
the m etapsychology of drives has been found increas-
ingly unsatisfactory. Although the idea of conflict is
being retained in contem porary theory, it is being
based on the historical vicissitudes of affects in the
interpersonal sphere rather than on drives. It has been
proposed (28) that system atically unem pathic re-
sponses on the part of a parent to critical affect states
in the child give rise to avoidance of the affects as
threats to the needed relationship with the parent.
Thus, intrapsychic conflict arises regarding the affect
state. W hat is innate, according to this m odel, is the
developm ental requirem ent for appropriate em pathic
responses from the environm ent. This outlook, which
focuses on the interpersonal fram e of reference, con-
siders psychoanalytic treatm ent the reworking of em o-
tional phenom ena at the interpersonal level-phenom -
ena that nevertheless also have intrapsychic and even
som atic aspects.
CLINICAL PATHOLOGICAL SYNDROM ES
INVOLVING EM PATHY
How em pathic processes are carried out by the CNS
is unknown. In this section and the section on labora-
tory studies, I present evidence for the involvem ent of
specific brain regions.
There are several syndrom es of known or presum ed
neurological basis that have as their hallm arks a defect
of interpersonal em otional com m unication. Heilm an
et al. (29) described auditory affective agnosia in pa-
tients with right tem poroparietal lesions; these patients
m anifest an inability to understand em otion in voice
quality. The inability to express em otions through
prosody or spontaneous gesture (aprosodic-agestural
syndrom e) in patients with right-hem isphere lesions
has been described by Ross and M esulam (30). Their
subjects disclosed that they felt em otions subjectively
but could not convey them . The loss of spontaneous
gesture was differentiated not only from ideom otor
apraxia but also from an inability to pantom im e,
which m ay be seen in left-sided lesions as a result of
dam age to substrates of sym bolic com m unication.
Ross and M esulam (30) have com m ented that the
dam aged brain regions in question are connected with
lim bic structures. Ross (31) postulated a right-hem i-
sphere specialization for producing and com prehend-
ing the affective com ponents of language, analogous to
the specialization of the left hem isphere for proposi-
tional com ponents. Preferential involvem ent of the
right hem isphere in the analysis of em otional signals
has also been supported by studies of norm al subjects
responses to neutral and em otional faces presented in
left and right visual fields and by studies com paring
subjects with left- and right-hem isphere lesions for
ability to understand em otional faces and situations
(32-34).
A clinical syndrom e that m ay provide excellent op-
portunities for the study of neural m echanism s of em -
pathy is infantile autism . Kanner (3S) wrote,
LESLIE BROTHERS
Am J Psychiatry 146:1, January 1989 13
W e m ust assum e, then, that these children have com e
into the world with innate inability to form the usual,
biologically provided affective contact with people, just as
other children com e into the world with innate physical or
intellectual handicaps. (p. 250)
As understanding of the syndrom e of infantile autism
has progressed, it has becom e increasingly clear that its
central and prim ary pathology is a defect of em pathy
(unpublished 1987 paper of P. Tanguay). This defect
m ay exist with or without the presence of m ental re-
tardation but is always present. Reflecting this view,
DSM -III-R uses a defect of em pathy as a prim ary cri-
tenon for diagnosis of autistic disorder.
Of unclear etiology is the inability of patients de-
scribed as alexithym ic (36) to perceive the em otions of
others. In these patients the defect of em pathy is ex-
plained as arising secondarily from a prim ary inability
to be aware of subjective em otions. The origin of this
deficit is obscure (37-39).
W ith the exception of alexithym ia, the disorders de-
scribed here, although they provide little inform ation
to support a narrow localization of em pathic function-
ing, clearly dem onstrate that em pathic processes are
beginning to be describable in neurological term s. The
occurrence of infantile autism , in particular, suggests
there m ay be a specific neural or neurotransm itter
subsystem for em pathy.
THE ONTOGENY OF EM PATHY
M uch m ore needs to be learned about the develop-
m ent of the capacity for em pathy in people. Basch (25)
has hypothesized several stages, beginning with invol-
untary autonom ic responses present from birth, pro-
ceeding to conscious awareness of an affective event,
then the experience of feelings in relationship to the
self and its goals, and finally to em pathic understand-
ing. Em de (5) noted that at 9 months, affect provides
a signal to the inside . . . not just to the outside . . . ; in
other words, social signals becom e psychological sig-
nals as well (p. 101; authors italics). Few em pirical
studies of em pathy in children have been carried out.
Lenrow (40) studied helping responses to com m unica-
tion of distress in preschoolers, acknowledging, how-
ever, som e difficulties in interpretation of the results.
Other studies were discussed by Ekm an and Oster
(41). Although not studying em pathy per se, Stern (42)
has studied in detail the establishm ent of intersubjec-
tive com m unication between child and parent, which
begins at around 9 m onths of age.
W e know there is preferential gaze fixation by neo-
nates on the face (43) as well as specific responses to
facial expression. In now classic studies, M eltzoff and
M oore (44) established the ability of infants younger
than 3 days of age to im itate adults opening and clos-
ing their m ouths and sticking out their tongues. Field
et a!. (45) showed that neonates at around 36 hours
were able to im itate facial expressions. (For an alter-
native explanation of these findings see [46].) Oster
(47) has described cycles of gazing at the caretakers
face and sm iling, together with com plex facial m ove-
m ents accom panying the sm ile, in infants 3 to 4 weeks
old.
It is striking that com plex facial m otor patterns are
present from an early age in hum an beings and can be
elicited in a specific m anner in social settings. It has
also been shown that newborn infants cry on hearing
the crying of other infants (48). These early facial re-
sponses and crying responses should be considered
analogous to other prim itive reflexes, such as the step-
ping reflex, in the sense that the eventual learning to
walk depends on an innate neurological capability to-
gether with the appropriate environm ental conditions
present at the right tim e and the m aturation of other
system s. The reflex analogy should not be taken to
suggest, however, that these social responses are purely
m otoric and do not also contain affects (for discussion
of this point see [47]).
It is reasonable to assum e that the capacity for em -
pathy is present in som e precursor form at birth in the
norm al brain and is elaborated by cognitive m atura-
tion and by subsequent experiences in the social m i-
lieu. (A schem e for the relation of cognitive m aturation
and em otional experience has been proposed by Lane
and Schwartz [49]. For Piagetian views of em otional
m aturation see [SO, 51].) As is the case in every other
com plex hum an behavior, varying individual capaci-
ties for em pathy m ust be the result either of different
genetic endowm ents or of different experiences-al-
though in practice these m ust always interact. The in-
teraction of innate capacity for differential response to
faces in rhesus m onkeys with social experience has
been shown by Sackett (52) and is discussed in the
section entitled Laboratory Studies.
THE PHYLOGENY OF EM PATHY
In 1873, Darwin (9) wrote,
The com m unity of certain expressions in distinct though
allied species, as in the m ovem ents of the sam e facial m us-
des during laughter by m an and by various m onkeys, is
rendered som ewhat m ore intelligible, if we believe in their
descent from a com m on progenitor. He who adm its on
general grounds that the structure and habits of all anim als
have been gradually evolved, will look at the whole subject
of Expression in a new and interesting light . . . . W hen we
witness any deep em otion, our sym pathy is so strongly
excited, that close observation is forgotten or rendered
alm ost im possible; of which fact I have had m any curious
proofs. (p. 12)
Although he did not further address it, Darwin here
alludes to the com m unication of an em otional state.
The evolution of form s of social com m unication in
the prim ate order has been studied prim arily by com -
parative m ethods. Of special interest for such studies
are the prosim ians, a heterogeneous group of prim ates
BIOLOGICAL PERSPECTIVE ON EM PATHY
14 Am J Psychiatry 146:1, January 1989
found m ainly but not exclusively on the island of M ad-
agascar. It is believed that M adagascar was separated
from the African continent in the early Eocene (53), at
a tim e when prosim ians were the dom inant prim ate
form throughout the world. Subsequently, New W orld
and Old W orld prim ates em erged and were quite effec-
tive com petitors with their prosim ian relatives. Those
prosim ians which rem ained in relative isolation from
both predators and their sim ian com petitors-as oc-
curred in M adagascar-today provide an opportunity
to study ancestral characteristics of the prim ate order.
According to com parative data, it appears that noc-
turnal prim ates were the earliest form s (54). These an-
im als lived in rather sim ple social groups and com m u-
nicated prim arily by olfaction (spraying of scent from
special-purpose glands) rather than by vision-as
would be expected, given their nocturnal life styles.
The switch to diurnal activity patterns was probably
accom panied by two developm ents: a greater reliance
on visual social com m unication and m ore com plex so-
cia! structures. That these two developm ents should go
together is not surprising, given that vision perm its a
high degree of tem poral sequencing and brevity of sig-
nals com pared with olfaction (54). Lem urs are a par-
ticularly interesting group in regard to the transition
from olfaction to vision because they use both m odal-
ities. They are able to use facial expression to a lim ited
degree but are restricted by the anatom ical fact that
their upper lips are attached to their gum s in the m id-
dle (as are the upper lips of dogs, to use a fam iliar
exam ple). Prim ates that use their visual system s exten-
sively for social com m unication, such as ourselves,
have nonattached, m obile upper lips. This perm its the
m outh region to be used for a very rich variety of facial
expressions. Indeed, those m uscles innervated by the
seventh cranial nerve, which include the m uscles
around the eyes, are som etim es referred to as the m us-
des of expression.
It is necessary to assum e that, concom itant with the
developm ent of an ever m ore com plex signaling appa-
ratus-one that appears to be intim ately tied to signal-
ing of em otional states-an apparatus for correct per-
ception and response evolved as well. Cheney et al.
(55) have written,
As inform ation on prim ate social behavior continues to
accum ulate, the com plex and m ultifaceted social relation-
ships of nonhuman primates become increasingly appa-
rent . . . . They em ploy a variety of m echanism s for sus-
tam ing relationships that com bine com petitive and
affiliative elements, and they seem to be able to adjust their
behavior to particular individuals and circum stances.
These features of primate behavior raise intriguing ques-
tions about the cognitive capacities that underlie social
interactions. (p. 1363)
Hum phrey (56) has em phasized that being able to
read the m otivational states of other individuals de-
pends on having had conscious awareness of ones
own feelings:
I assum e that any anim al which lives in a com plex social
group needs above all else the ability to do what I have
called natural psychology, the ability to model the be-
havior of other members of its group . . . . The true value
of consciousness is that it gives the natural psychologist
direct access to those psychological concepts-the concept
of feeling pain, feeling fear, feeling contentment, etc.-
without which it would find the task of modelling the
behavior of another animal impossibly difficult. Unless, for
exam ple, an anim al has itself been consciously aware of
the feeling of pain, resulting from its own injury, it could
hardly begin to understand the behavior of another injured
animal. (p. 44)
Hum phrey noted further (p. 22) that when individ-
uals of a species com pete with each other for success in
outwitting each other, which is one outcom e of the
ability to read social signals, the evolutionary situ-
ation is quite different from one in which all com pete
for success against an external environm ental pressure.
In the form er case, evolutionary pressure favoring the
development of social skill is continually intensified by
the presence of ever-increasing skill in other m em bers
of the group. Thus, in prim ate society the stage has
been set for the developm ent of ever-increasing sub-
tlety and sensitivity in detecting social signals. Further-
m ore, the m ost highly developed ability to m anipulate,
to deceive, and to be am biguous-and to detect those
activities in others-would carry a survival premium.
At the sam e tim e, social bonds m ust be m aintained for
the sake of group survival; probably for this reason,
there appears to be a positive m otivation for m aintain-
ing social intercourse (57).
To sum m arize briefly to this point: the social corn-
plexity of the prim ate environm ent has increased over
the course of evolution. In response, prim ate neural
m achinery has been dedicated to analysis of social sig-
nals. This contention is supported by the fact that, in
people, certain types of brain damage compromise the
ability to detect emotions in others. It is also supported
by the presence of innate social responses in infants. In
the next section of this paper, data from two addi-
tional vantage points are presented: the existence of
animal models of empathy makes it possible to study
underlying neural processes, and studies of neural
firing characteristics reveal responsiveness to social
stimuli.
LABORATORY STUDIES OF EM OTIONAL
COM M UNICATION
Animal M odels
Observations in field settings make it abundantly
clear that nonhum an prim ates are well endowed with
the capacity for effective em otional com m unication;
however, in order to study neural processes underlying
this ability, it becom es necessary to first dem onstrate
that such abilities occur and are displayed in the m ore
artificial laboratory setting.
LESLIE BROTHERS
Am J Psychiatry 146:1, January 1989 15
In a study of the ontogeny of response to facial
expression in m onkeys, Sackett (52) showed that in-
fant rhesus m onkeys deprived of norm al visually m e-
diated social experiences from birth distinguished be-
tween categories of facial expression of conspecifics as
shown in slides. Evidence for the distinctions persisted
until about 4 m onths of age, but differential responses
faded with the persisting absence of other social input.
These findings support the presence of an inborn ca-
pacity to distinguish facial expressions and also the
role of subsequent social experience in m aintaining the
ability to respond appropriately.
In a series of studies, M iller et al. and M irsky et al.
(58-60) trained rhesus m onkeys to associate an audi-
tory signal with an electrical shock that followed a few
seconds later and to avoid the shock by pressing a lever
whenever the signal was heard. Trained m onkeys were
then paired in a cooperative avoidance paradigm : the
warning tone was presented to one m em ber of the pair
(the stim ulus m onkey) that did not have access to a
lever. The partner or observer m onkey could not
hear the warning signal, but it had access through
closed-circuit television to pictures of the face of the
stim ulus m onkey and access to a lever. Lever presses
by the observer m onkeys in response to the distressed
faces of the stim ulus m onkeys occurred well above
chance levels from the tim e the paired experim ent was
begun. This anim al m odel of em pathy provides proof
that nonhum an prim ates are highly suitable subjects
for study of the brain processes subserving em pathy.
Single Neuron Studies
Observations of cell firing in the brains of anim al
prim ates in response to faces and hands were m ade
incidentally in the course of other investigations by
several groups of neurophysiologists. The efficacy of
these stim uli gave rise to subsequent efforts to further
characterize the neural responses. System atic investi-
gation of cell firing in the prim ate brain in response to
visual social stimuli has been undertaken by Gross and
colleagues at Princeton, Rolls and colleagues at Ox-
ford, and Perrett and colleagues at St. Andrews. Their
findings to date are sum m arized here. Briefly, these
experim ents are carried out in alert m onkeys that are
trained to sit quietly while attending to a variety of
stim uli. Fine-tipped electrodes record the activity of
single neurons; firing data are correlated with different
features of the presented stim uli in order to character-
ize neuronal responses.
The m ajority of observations have been m ade in the
superior tem poral sulcus of the tem poral lobes and in
the am ygdala. Data collected by Baylis et al. (61)
showed that cells responding to pictures of faces had
preferences for the identity of the face, responding
weakly to som e and strongly to others. Leonard et al.
(62) dem onstrated that the latency of firing in response
to these stim uli was longer in the am ygdala than in the
superior tem poral sulcus, consistent with a processing
sequence occurring first in the tem poral cortex and
subsequently in the amygdala. The distribution of cells
responsive to faces in the tem poral cortex appeared to
be restricted to discrete regions of the fundus of the
m iddle third of the superior tem poral sulcus (63). At-
tem pts were m ade to discover whether face-selective
cells were in fact responding only to features of face
pictures, such as the hairline or eyes. Cells that re-
sponded to pictures of these features responded even
m ore strongly to pictures of the whole face (63), re-
sulting in the interpretation that features were effective
only insofar as they suggested a face gestalt. However,
neurons varied in their selectivity for different parts:
som e were driven m ore effectively by the eyes, others
by the m outh, and still others by the hair. Attem pts to
find alternative explanations for the cell responses
(that the effective aspect of the stim ulus was its size,
contrast, or spatial frequency characteristics) also con-
firmed the interpretation that the effective feature was
faceness (64, 65), not any of these incidental at-
tributes. In addition, single-unit studies have explored
the lateralization of face recognition in m onkeys (66).
M ore recent investigations of face-selective neurons
using richer stim uli suggested that som e of these neu-
rons m ay be coding for a higher-level feature than the
face, nam ely, facial expression. Tem poral lobe neurons
were discovered to be selective for the orientation of
the head and direction of gaze of the eyes in a stim ulus
picture (67, 68). Furtherm ore, a cell that responded to
a specific facial expression (the yawn, which has ago-
nistic significance) was found: it showed a robust firing
response to pictures of yawns whether displayed fron-
tally or in profile, but not to other expressions. The
sam e investigation (69) described a cell specifically re-
sponsive to crouching body posture, which is a socially
m eaningful feature. Even m ore recently, in the first
system atic study using facial expressions as stim uli,
Hasselmo et al. (70) showed that a substantial fraction
of face-selective neurons in the anterior superior tern-
poral sulcus showed significant responses to expression.
I now turn from data on single neurons to conjecture
regarding the flow of neural information among brain
regions during processing of social em otional signals.
THE ROLE OF THE AM YGDALA IN SOCIAL
EM OTIONAL COM M UNICATION
The am ygdala is a highly interconnected cluster of
neurons lying deep in the m edial tem poral lobes. It is
one com ponent of the brains lim bic system , described
by Nauta and Feirtag (71) as a determ inant of the
organism s attitude toward its environm ent (p. 125).
The arnygdala receives inputs prim arily from the high-
level sensory cortex, that is, inform ation which is sev-
eral stages m ore processed than prim ary sensory input
(72, 73). The one exception to this pattern is olfactory
input, which im pinges directly on the am ygdala from
the prim ary olfactory cortex. In the case of auditory
and visual m odalities, regions with the m ost elabo-
rated processing of sensory input have the heaviest
BIOLOGICAL PERSPECTIVE ON EM PATHY
16 Am J Psychiatry 146:1, January 1989
projections to the am ygdala (73). These afferents from
the so-called association cortex represent the m ajor
input to the am ygdala. Inform ation arrives m ainly
through relays in the tem poral cortex, including the su-
perior tem poral sulcus m entioned earlier in this paper.
Am ygdala outputs can be conceptualized under two
m ajor headings. The first is the reciprocal of the sen-
sory input just described: the am ygdala has wide-
spread outputs to the sensory association cortex, per-
haps im parting an em otional tone to analysis of
sensory data (71). A recent anatomical study (72) im-
plied that the am ygdala processes data received from
the sensory cortex before sending signals back to that
area. In addition, this study provided evidence for
am ygdala projections to areas that handle visual in-
form ation in relatively early stages of the processing
sequence.
The second category of am ygdala efferents is output
to specific brainstem centers that control heart rate and
respiratory rate (74-76) and to the hypothalam us (77),
which has been called the head ganglion of the auto-
nom ic nervous system and which also is critical in or-
chestrating endocrine activity. This arrangem ent of af-
ferent and efferent connections im plies that the
am ygdala is strategically located for generating rapid
and specific autonom ic and endocrine patterns in re-
sponse to com plex social signals. The survival value of
such a system is obvious: the perception of another
individuals approach should give rise to a specific pat-
tern of cardiac output and respiration-and very
quickly-tailored to whether the intent is to bite, to
have a quiet groom ing session, or to copulate. Indeed,
exposure of anim als in laboratory settings to particular
types of social interactions with other anim als gives
rise to highly specific endocrine and autonom ic
changes (78).
Not only does the pattern of the am ygdalas connec-
tions suggest that it is strategically located for respond-
ing to social signals, there is evidence that it indeed
perform s such a role. One line of evidence com es from
the studies of single unit activity already cited and
from studies of m ulti-unit activity occurring during so-
cial interactions in squirrel m onkeys (1 1). Another bit
of evidence com es from lesion experim ents perform ed
in the wild. In one study (79), free-ranging m onkeys
were observed in their social groups, captured, sub-
jected to bilateral lesions of the am ygdala, and then
returned to their group. These anim als did not have
difficulty with ordinary tasks such as feeding them-
selves or clim bing trees, but they had severe difficulties
responding appropriately to other anim als. They ran
away from every approach, including friendly ones,
and eventually isolated them selves com pletely from
their troop.
As we begin to study the brain processes underlying
em pathy, the role of neural activity within the am yg-
dala will be of great interest. Its interaction with the
sensory cortex on the one hand and with brainstem
structures on the other will almost certainly prove to
be key inform ation for our understanding of em pathic
processes.
UNDERSTANDING THE NEURAL SUBSTRATE OF
EM PATHY
There are several m odes in which em pathic com m u-
nication m ay take place. Schafer (80) wrote that em -
pathy requires attention . . . to cues . . . in m otility,
verbalization, affective expression and tem po. Hoff-
m an (24, pp. 235, 236) contrasted em pathic under-
standing of the m eaning of language with em pathic
understanding of stim uli whose relevant properties are
restricted to physical features, such as cries or facial
expression. The relation between language and em pa-
thy was highlighted by Alpert et al. (8 1 ) in a study of
residents ability to detect references to the them e of
separation in verbal m aterial excerpted from a psycho-
therapy session. Alpert et al. im plied that words or
phrases with high im agery content are potent vehicles
for em pathic com m unication. However, the neural ba-
sis for language com prehension-still m ore for the
grasp of m etaphors and parapraxes-is obscure. It is
difficult at present, therefore, to fram e hypotheses re-
garding neural m echanism s of em pathy at the sem antic
level.
By contrast, because the prim ate visual system is
well described (even though its workings as a whole
are still incom pletely understood), neural responses to
visual affective stim uli in anim als are within the reach
of experim ental study. It is possible with a neurophys-
iological apparatus to m easure the sequence of events
with m illisecond resolution. In other words, from the
tim e a stim ulus is presented, the latency of onset of
neural firing in different regions together with the la-
tency of autonom ic changes (such as in pupil size and
heart rate) suggests the sequence of processing that
occurs in the brain. Using such firing data from dif-
ferent brain regions, it becom es possible to discover
whether in fact m otor or autonom ic system s partici-
pate from the outset in em otional perception, as so-
m atic-m im icry theories of em pathy postulate. It also
becom es possible, if an appropriate array of social test
stim uli are used, to analyze which regions of the brain
are activated by expressions of em otion in conspe-
cifics-and how this inform ation is extracted from
physical features of the stim ulus by neurons earlier in
processing.
It is now well established that visual inform ation is
processed in the inferior tem poral cortex at the end of
several stages of processing from the retina through the
lateral geniculate body, striate cortex, and secondary
and tertiary visual areas. It is presum ed, but not
known for certain, that analysis of com plex features
such as social signals m ust be carried out in the highest
visual areas. The am ygdala lies at the end of this path-
way, the final effectors being endocrine-releasing fac-
tors (from the hypothalam us) and autonom ic changes
arising in the hypothalam us and brainstem . However,
LESLIE BROTHERS
Am J Psychiatry 146:1, January 1989 17
autonom ic responses have yet to be recorded sim ulta-
neously with the presentation of social stim uli and re-
cording of central neuronal activity.
Other features of the neuronal response to social
em otional signals rem ain to be studied as well. For
exam ple, the role of central m otor neurons-either in
m otor association areas or in the basal ganglia-in
influencing or form ing part of the perception of social
signals (such as facial expression, for e cam ple) has not
been studied. Likewise, activity in shorter and faster
sensory pathways from the retina to the am ygdala
through the superior colliculus, which may transduce
som e aspects of a stim ulus into im m ediate autonom ic
activity, has not been investigated. (Evidence for the
role of these extrastriate visual pathways in generating
perceptions outside conscious awareness exists in phe-
nom ena such as blindsight [82].) Finally, the possi-
ble convergence of inform ation from several sensory
m odalities onto single lim bic neurons has not been
studied. M y colleagues and I are now carrying out
som e of these studies using an array of visual and au-
ditory social signals as stim uli.
SUM M ARY
Em pathy is a concept whose recent origin is in psy-
choanalysis and in ideas that influenced Freud from the
intellectual milieu of turn-of-the-century Germany. It
appears to have been m uch discussed in the psycho-
logical literature of the early decades of this century
and is now reem erging as a subject of discussion and
debate in the clinical literature.
Evidence from com parative prim atological studies
suggests that sophisticated social com m unication is a
hallm ark of prim ate evolution. W hen taken to sub-
sum e som atic-including neural-events, em pathic
processes are found to be analyzable in term s of brain
activity.
Studies of human and nonhuman primate infants
reveal the presence of innate and early responses to
facial expression. In the absence of organic disease or
social deprivation, prim itive response system s becom e
elaborated into m ature social com m unication, by pro-
cesses as yet incom pletely understood.
Recent neurophysiological investigations reveal the
presence of neurons in the prim ate tem poral lobe that
fire in response to aspects of the appearance of other
m onkeys-in response to a specific facial expression in
som e cases. Application of neurophysiological tech-
niques to analysis of social-em otional com m unication
will m ake it possible to prove or disprove the idea of
som atic m im icry as the basis of em pathy.
Because of this confluence of data from a variety of
disciplines, em pathy (a subjective experience between
people), social-em otional com m unication (in anim als)
and social signal processing (by neurons) can be un-
derstood as aspects of a single phenom enon. The phe-
nom enon in m an appears to be a product of both spe-
cies evolution and individual history. Em pathy, then, is
a biological concept par excellence whose full analysis
depends on understanding historically interdependent
social, som atic, and intrapsychic events.
REFERENCES
1. Freud S: Project for a scientific psychology (19S0[1895]), in
Com plete Psychological W orks, standard ed, vol 1 . London,
Hogarth Press, 1966
2. Em de RN: Toward a psychoanalytic theory of affect, I: the
organizational model and its propositions, in The Course of
Life: Psychoanalytic Contributions Toward Understanding Per-
sonality Developm ent, vol I: Infancy and Early Childhood. Ed-
ited by Greenspan SI, Pollock GH. Adelphi, M d, National In-
stitute of M ental Health, 1980
3. M ayr E: The Growth of Biological Thought: Diversity, Evolu-
non, and Inheritance. Cam bridge, Harvard University Press,
1982
4. Lewontin RC, Rose S, Kam in U: Not in Our Genes: Biology,
Ideology, and Hum an Nature. New York, Pantheon Books,
1984, pp 3-iS
S. Em de RN: Toward a psychoanalytic theory of affect, II: em erg-
ing m odels of em otional developm ent in infancy, in The Course
of Life: Psychoanalytic Contributions Toward Understanding
Personality Developm ent, vol I: Infancy and Early Childhood.
Edited by Greenspan Sl, Pollock GH. Adelphi, M d, National
Institute of M ental Health, 1980
6. Churchland P: Neurophilosophy: Toward a Unified Science of
the M ind/Brain. Cam bridge, M ass, M IT Press, 1986
7. Sereno M : A program for the neurobiology of m ind. Inquiry
1986; 29:217-240
8. Scott JP: The function of em otions in behavioral system s: a
system s theory analysis, in Em otion: Theory, Research and
Experience, vol 1. Edited by Plutchik R, Kellerm an H. New
York, Academ ic Press, 1980, pp 35-56
9. Darwin C: The Expression of the Em otions in M an and Ani-
m als. New York, D Appleton, 1873
10. Tom kins SS: Affect, lm agery, Consciousness. New York,
Springer, 1962
1 1. Kling A, Lloyd RL, Perrym an K: Slow wave changes in am yg-
dala to visual auditory and social stim uli following lesions of the
inferior tem poral cortex in squirrel m onkey (Saim iri sciureus).
Behav Neural Biol 1987; 47:54-72
12. Ploog D: Neurobiology of prim ate audio-vocal behavior. Brain
Res Rev 1981; 3:35-61
13. Buchwald J, Shipley C, Altafullah I, et al: The feline isolation
call, in The Physiological Control of M am m alian Vocalizations.
Edited by Newm an J. New York, Plenum (in press)
14. M acLean PD: Brain evolution relating to fam ily, play and the
separation call. Arch Gen Psychiatry 1985; 42:405-417
15. W inter P, Ploog D, Latta J: Vocal repertoire of the squirrel
m onkey (Saim iri sciureus), its analysis and significance. Exp
Brain Res 1966; 1:359-384
i6. Lipps T: Leitfaden der Psychologie. Leipzig, W ilhelm Engel-
m ann, 1903, pp 187-200
17. M asson JM (ed): The Com plete Letters of Sigm und Freud to
W ilhelm Fliess, 1887-1904. Cam bridge, Belknap (Harvard
University Press), 1985, pp 324-325
18. Lee V: The Beautiful: An Introduction to Psychological Aesthet-
ics. Cambridge, Cambridge University Press, 1913, p 66
19. Kohut H: Introspection, em pathy and psychoanalysis. J Am
Psychoanal Assoc 1959; 7:459-483
20. Kohut H: The Analysis of the Self: A Systematic Approach to
the Psychoanalytic Treatm ent of Narcissistic Personality Disor-
ders. New York, International Universities Press, 1971
21. Kohut H: The Restoration of the Self. New York, International
Universities Press, 1977
22. Freud S: Group psychology and the analysis of the ego (1921),
in Com plete Psychological W orks, standard ed, vol 18. London,
Hogarth Press, 1955
23. Fenichel 0: The Psychoanalytic Theory of Neurosis. New York,
BIOLOGICAL PERSPECTIVE ON EM PATHY
18 Am J Psychiatry 146:1, January 1989
W W Norton, 1945
24. Hoffm an M L: Toward a theory of em pathic arousal and devel-
opm ent, in The Developm ent of Affect. Edited by Lewis M ,
Rosenblum L. New York, Plenum , 1978
25. Basch M F: Em pathic understanding: a review of the concept
and som e theoretical considerations. J Am Psychoanal Assoc
1983; 31:101-126
26. Schachter S, Singer JE: Cognitive, social and physiological de-
term inants of em otional state. Psychol Rev 1962; 69:379-399
27. Lange CG, Jam es W : The Em otions (1922). New York, Hafner,
1967
28. Stolorow R, Brandchaft B: Developm ental failure and psychic
conflict. Psychoanal Psychol 1987; 4:241-2S3
29. Heilm an KM , Scholes R, W atson RT: Auditory affective agno-
sia: disturbed com prehension of affective speech. J Neurol Neu-
rosurg Psychiatry 1975; 38:69-72
30. Ross ED, M esulam M -M : Dom inant language functions of the
right hem isphere? Arch Neurol 1979; 36:144-148
31. Ross ED: The aprosodias: functional-anatom ic organization of
the affective com ponents of language in the right hem isphere.
Arch Neurol 1981; 38:561-569
32. Suberi M , M cKeever W F: Differential right hemispheric mem-
ory storage of em otional and non-em otional faces. Neuropsy-
chol 1977; 15:757-768
33. Ley RG, Bryden M P: Hem ispheric differences in processing
em otions and faces. Brain Lang 1979; 7:127-138
34. Cicone M , W apner W , Gardner H: Sensitivity to em otional
expressions and situations in organic patients. Cortex 1980; 16:
145-158
35. Kanner L: Autistic disturbances of affective contact. Nervous
Child 1943; 2:217-250
36. Krystal H: Alexithym ia and psychotherapy. Am J Psychother
1979; 33:17-31
37. Nemiah JC: Alexithymia: theoretical considerations. Psycho-
ther Psychosom 1977; 28:199-206
38. Taylor GJ: Alexithym ia: concept, m easurem ent, and im plica-
tions for treatment. Am J Psychiatry 1984; 141:725-732
39. TenHouten W D, Hoppe KD, Bogen JE, et al: Alexithym ia: an
experim ental study of cerebral com m issurotom y patients and
norm al control subjects. Am J Psychiatry 1986; 143:312-316
40. Lenrow PB: Studies of sym pathy, in Affect, Cognition and Per-
sonaliry. Edited by Tom kins SS, Izard CE. New York, Springer,
1965
41. Ekm an P, Oster H: Facial expression of em otion. Annu Rev
Psychol 1979; 30:527-554
42. Stern DN: The Interpersonal W orld of the Infant: A View From
Psychoanalysis and Developm ental Psychology. New York, Ba-
sic Books, 1985
43. Stern D: The First Relationship: Infant and M other. Cam -
bridge, Harvard University Press, 1977, pp 34-37
44. M eltzoff AN, M oore M K: Im itation of facial and m anual ges-
tures by hum an neonates. Science 1977; 198:75-78
45. Field TM , W oodson R, Greenberg R, et al: Discrim ination and
im itation of facial expressions by neonates. Science 1982; 218:
179-181
46. Eibl-Eibesfeldt I: Strategies of social interaction, in Em otion:
Theory, Research and Experience, vol 1. Edited by Plutchik R,
Kellerm an H. New York, Academ ic Press, 1980, p 65
47. Oster H: Facial expression and affect development, in The Dc-
velopm ent of Affect. Edited by Lewis M , Rosenblum L. New
York, Plenum , 1978
48. Sagi A, Hoffm an M L: Em pathic distress in the newborn. Dc-
velopm ental Psychol 1976; 12: 175-1 76
49. Lane RD, Schwartz GE: Levels of em otional awareness: a cog-
nitive-developm ental theory and its application to psychopa-
thology. Am J Psychiatry 1987; 144:133-143
SO. Decarie TG: Affect developm ent and cognition in a Piagetian
context, in The Developm ent of Affect. Edited by Lewis M ,
Rosenblum L. New York, Plenum , 1978
S 1 . Cicchetti D, Hesse P: Affect and intellect: Piagets contributions
to the study of infant em otional developm ent, in Em otion: The-
ory, Research, and Experience, vol 2. Edited by Plutchik R,
Kellerm an H. New York, Academ ic Press, 1983
52. Sackett GP: M onkeys reared in isolation with pictures as visual
input: evidence for an innate releasing mechanism. Science
1966; 154:1468-1473
53. Charles-Dom inique P, M artin R: Behavior and Ecology of Noc-
turnal Prosimians: Advances in Ethology 9. Berlin, Paul Parey,
1972
54. Allm an J: Reconstructing the evolution of the brain in prim ates
through the use of com parative neurophysiological and neuro-
anatom ical data, in Prim ate Brain Evolution: M ethods and
Concepts. Edited by Arm strong E, Falk D. New York, Plenum ,
1982
55. Cheney D, Seyfarth R, Smuts B: Social relationships and social
cognition in nonhuman primates. Science 1986; 234:1361-
1366
56. Hum phrey N: Consciousness Regained. Oxford, Oxford Uni-
versity Press, 1983
57. Ham burg DA: Em otions in the perspective of hum an evolution,
in Expression of the Em otions in M an. Edited by Knapp PH.
New York, International Universities Press, 1963, p 305
58. M iller RE, Banks JH, Ogawa N: Role of facial expression in
cooperative-avoidance conditioning in m onkeys. J Abnorm
Soc Psychol 1963; 67:24-30
59. M iller RE, M urphy JV, M irsky IA: Relevance of facial expres-
sion and posture as cues in com m unication of affect between
monkeys. Arch Gen Psychiatry 1959; 1:480-488
60. M irsky IA, M iller RE, M urphy JV: The communication of affect
in rhesus m onkeys, I: an experim ental m ethod. J Am Psychoanal
Assoc 1958; 6:433-441
61. Baylis GC, Rolls ET, Leonard CM : Selectivity between faces in
the responses of a population of neurons in the cortex in the
superior temporal sulcus of the monkey. Brain Res 1985; 342:
91-102
62. Leonard CM , Rolls ET, W ilson FAW , et al: Neurons in the
am ygdala of the m onkey with responses selective for faces. Be-
hay Brain Res 1985; 15:159-176
63. Perrett DI, Rolls ET, Caan W : Visual neurons responsive to
faces in the monkey temporal cortex. Exp Brain Res 1982; 47:
329-342
64. Rolls ET, Baylis GC: Size and contrast have only sm all effects on
the responses to faces of neurons in the cortex of the superior
tem poral sulcus of the m onkey. Exp Brain Res 1986; 65:38-48
65. Rolls ET, Baylis GC, Leonard CM : Role oflow and high spatial
frequencies in the face-selective responses of neurons in the cor-
tex in the superior tem poral sulcus. Vision Res 1985; 25:
1021-1035
66. Perrett DI, M istlin AJ, Chitty AJ, et al: Specialized face proc-
essing and hemispheric asymmetry in man and monkey: cvi-
dence from single unit and reaction tim e studies. Behav Brain
Res 1988; 29:245-258
67. Perrett DI, Sm ith PAJ, M istlin AJ, et al: Visual analysis of body
m ovem ents by neurones in the tem poral cortex of the m acaque
m onkey: a prelim inary report. Behav Brain Res 1985; 16:
153-170
68. Perrett DI, Sm ith PAJ, Potter DD, et al: Visual cells in the tern-
poral cortex sensitive to face view and gaze direction. Proc R
Soc Lond (Biol) 1985; 223:293-317
69. Perrert DI, Sm ith PAJ, Potter DD, et al: Neurones responsive to
faces in the temporal cortex: studies of functional organization,
sensitivity to identity and relation to perception. Hum Neuro-
biol 1984; 3:197-208
70. Hasselm o M E, Rolls ET, Baylis GC: Selectivity between facial
expressions in the responses of a population of neurons in the
superior temporal sulcus of the monkey. Neurosci Lett 1986;
26:S571
71. Nauta W JH, Feirtag M : Fundam ental Neuroanatom y. New
York, W H Freem an, 1986
72. lwai E, Yukie M : Am ygdalofugal and am ygdalopetal connec-
tions with modality specific visual cortical areas in macaques (M
fuscata, M m ulatta, M fascicularis). J Com p Neurol 1987; 261:
362-387
73. Turner BH, M ishkin M , Knapp M : Organization of the am yg-
dalopetal m odality-specific cortical association areas in the
m onkey. J Com p Neurol 1980; 191:515-543
Deceased M embers of the American Psychiatric Association
The deaths of these members were reported to APA between Aug. 3 and Oct. 5, 1988.
Edward Karl Allis, Jr.
Craig Carroll Beesley
Courtenay L. Bennett
Barbara Jean Betz
W illiam Bleier
Ann Carlson Brown
Francis H. Butler
H. Jam es Crecraft
Ezra E. Dorison
Ella Duff-Good
Thom as 0. English, Jr.
Brucha D. Frank
Robert L. Frazier
Kersi Jal Gazdar
M elvin Goodm an
Charles W . Harding
Joseph M . Hughes
Gary R. Kirshbaum
Paul Kramer
Harry H. Lipcon
Louis V. Lopez
Gustav M achol
J ohn J. M arren
Frederick T. M elges
Barbara C. M ueller
Sol Nichtern
Francis A. ODonnell
Clarence W . Olsen
Charan S. Sandhu
M ax A. Sherm an
W illiam R. Sorum
Jack M ichael Stein
Eva Rose Towns
Cornelus J. Trim bos
J am es W . W atson
Benjam in I. W eininger
M artin Howard W endkos
Donald B. W illiams
Joseph Yavit
LESLIE BROTHERS
Am J Psychiatry 146: 1, January 1989 19
74. Harper RM , Frysinger RC, Trelease RB, et al: State-dependent
alteration of respiratory cycle tim ing by stim ulation of the cen-
tral nucleus of the am ygdala. Brain Res 1984; 306: 1-8
75. Kapp BS, Gallagher M , Frysinger RC, et al: The amygdala,
em otion, and cardiovascular conditioning, in The Am ygdaloid
Com plex. Edited by Ben-An Y. New York, Elsevier/North Hol-
land, 1981
76. Price JL, Russchen Fr, Am aral DG: The am ygdaloid com plex,
in Handbook of Chem ical Neuroanatom y, vol 5: Integrated
System s, part I. Edited by Swanson LW , Bjorklund A, Hokfelt
T. New York, Elsevier, 1988
77. Nauta W JH: Fiber degeneration following lesions of the am yg-
daloid com plex in the m onkey. J Anat 1961; 95:515-531
78. W einer H: Psychobiology and Hum an Disease. New York, El-
sevier, 1977, pp 140-143
79. Kling A: Effects of am ygdalectom y on social-affective behavior
in nonhum an prim ates, in The Neurobiology of the Am ygdala.
Edited by Eleftheriou BE. New York, Plenum , 1972
80. Schafer R: Generative em pathy in the treatm ent situation. Psy-
choanal Q 1959; 28:342-373
81. Alpert M , Cohen NL, M artz M , et al: Electroencephalographic
analysis: a m ethodology for evaluating psychotherapeutic pro-
cess. Psychiatr Res 1980; 2:323-329
82. W eiskrantz L: Blindsight: A Case Study and Im plications: Ox-
ford Psychology Series 12. New York, Clarendon Press, 1986