Vision Res. Vol. 26, No. 9, pp. 1401-1416.

1986
Printed in Great Britain. All rights reserved

HUMAN

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0042-6989186 $3.00 + 0.00

1986 Pergamon Journals L&d

VISUAL SUPPRESSION
FRANCES

C. VOLKMANN

Department of Psychology, Smith College, Northampton,

~~RODU~ON

The history of research on visual systems, as

abundantly illustrated in this Silver Jubilee
Issue, is a history of the rejection of the naive
realists view that we see the world as it is
(Holt, 1912). The selectivity of vision has
emerged as a primary outcome of the evolutionary process. Human visual perception as we
understand it is based upon mechanisms that
create for us an information-laden visual world,
a world that is not to be described by the
characteristics of the stimulus en~ronment
alone. Our visual systems filter input based
upon wavelength and spatial frequency in
highly selective ways. Different mechanisms
respond selectively to stimulus luminance and
to the movement of contours across the retina,
Enormous amounts of potential info~ation
are discarded in the adaptive interest of creating
a perceptual world of objects, identifiable by
their sizes, shapes, and hues, which may move
through the larger visual environment in relation to our own movements of body, head, and
eyes.
The phenomenon of visual suppression may
appropriately be regarded as one means by
which the visual system selects information.
Stimuli which are perceived under many normal
conditions are not perceived under certain
conditions related to the temporal sequence of
stimulation, the retinal areas stimulated, the
form and luminance* characteristics of the
stimuli, and the oculomotor behavior of the
perceiver.
Under this general definition we may include
principally the decrease of vision associated
with various oculomotor behaviors, some of
which has been discussed also in the previous
two articles. These include saccades, the brief,
ballistic movements made by the eyes as we
glance from one object to another in the visual
scene; the fast phase of nystagmus, in which the
eye follows a moving object by a series of
relatively slow tracking movements interspersed

MA 01063, U.S.A.

by fast saccade-like return flicks; eyeblinks of a

pre-programmed,
voluntary or reflex nature;
and vergence movements, the slow disjunctive
movements that align the two foveas to fixate
objects at various distances. Such a definition of
visual suppression may also include the decrease
of vision in the fixating eye that occurs when the
perception of a stimulus is masked by the
presentation of another stimulus. Finally, it may
include the phenomenon of rivalry, in which, in
its principal form, vision is decreased in one eye
when disparate images which cannot be fused
are presented to the two eyes.
A more restrictive definition of visual suppression that is often used or implied in the
literature limits the term to extraretinal neural
events which act to decrease vision during
saccades and other oculomotor behaviors (see
E. Matin, 1974, 1982; Volkmann, 1962; Zuber
and Stark, 1966). Such a definition excludes
masking and other phenomena of visual impairment which result solely from the configuration
and timing of stimulus events on the retina. The
present paper adopts this latter definition to a
limited degree. It reviews some of the major
research that permits us to delineate the respective roles that retinal and extraretinal events
play in the impairment of vision that accompanies a range of oculomotor behaviors. It,
therefore, does not include suppression due to
rivalry, and it includes only a specific subset of
the literature on visual masking. Further, partly
because of the enormous body of literature in
the field, the paper concentrates on psychophysical investigations of visual suppression
using human observers. Readers interested in
physiological investigations in other species may
wish to consult, as a first step, the useful recent
book, Visual Masking: An integrative Approach,
by Bruno Breitmeyer (1984).
SACCADIC

Observations

SUPPRE~ION

and theories prior to 1960

Almost a century ago, Erdmann and Dodge

1402

FRANCESC.VOLKMANN

(1898) reported that in a reading task, letters

which reached an observers eye only during the
brief saccadic jumps made by the eye as it
moved along a line of print were not seen, and
that all visual information from the printed line
was acquired during the fixational pauses
between saccades. There followed a series of
experiments and observations by several investigators which showed that, typically, the eye is
functionally blind during saccades, although
given adequate liminance, stimuli presented
only during saccades might be seen (Dodge,
1900, 1905; Holt, 1903, 1906; Woodworth, 1906;
see E. Matin, 1974 and Volkmann, 1976 for
reviews). Except under unusual circumstances
(i.e. when the eye moves at the same speed as a
bright stimulus exposed by a stroboscope), the
stimulus, if seen, appears dim and blurred.
While the loss of vision during a saccadic eye
movement was accepted by all of these early
investigators, they disagreed as to the mechanism(s) responsible for it. Variations on the
models which they proposed to account for
suppression have in large measure set the framework for research in the field ever since.
Holt (1903, 1906) believed that vision was
blanked out centrally in the brain during
saccades by an anesthesia which originated
in the neural impulses from the extraocular
muscles. He believed the anesthesia to be
essentially complete, and held that when an
observer reports having seen a stimulus that
appeared only during a saccade he is actually
seeing an afterimage of the stimulus, which
persists after the saccade has ended.
Dodge (1900, 1905) contended that both
a central inhibitory process and peripheral,
retinaily originating processes contribute to
visual suppression during saccades. He viewed
the central effect in terms of apperceptive
predisposition and attention (Dodge, 1900, p.
464) which causes the observer to ignore the dim
blurred image on the retina during saccades. In
addition, he postulated an equally important
peripheral factor, which consists in the inhibitive action of the new stimulation at each new
point of regard (Dodge, 1905, p. 197). As
E. Matin (1974) has emphasized, this notion
anticipates more recent att~butions of saccadic
suppression to phenomena of visual masking
(see below).
Woodworth (1906, 1938) added his own
experiments, criticized those of Holt and
Dodge, and offered the most parsimonious
model, which attributes saccadic suppression

entirely to differences in retinal stimulation of

the saccading and the fixating eye. Vision with
the rapidly moving eye, he wrote, does not
differ essentially from vision with the resting
eye, or with the eye which is making a pursuit
movement-given
only the same retinal stimulation in the three cases (Woodworth, 1906,
p. 69).
And there the matter stood for approximately
half a century. The basic questions were framed,
but the answers had to await the advances in
quantitative methods and instrumentation that
occurred many years later, primarily in the
physical sciences and engineering.
To compare the perceptual effects of stimuli
presented to the fixating and the saccading eye
under conditions of equivalent retinal stimulation (i.e. comparable degrees of smear) required
the development of accurate techniques for
recording saccades in human observers, such as
the techniques of cornea1 reflection, the electrooculogram, and limbus, pupil, and eyelid tracking (Young and Sheena, 1975). It required the
development of techniques of stimulus presentation, timing, measurement and control, so that
stimuli reaching the saceading and the fixating
eye could be equated, the precise time of arrival
of a stimulus in relation to a saccade measured,
and an appropriate independent variable such
as stimulus luminance specified and varied. It
required, finally, the development of appropriate psychophysical techniques for determining
and evaluating the observers perceptual response (Green and Swets, 1966). In general, the
recent work that has contributed most to the
field is that which has moved the analysis toward the precise and systematic.
The last 25 years

The first quantitative comparison of visual

thresholds during saccades and during fixation
(Volkmann, 1962) and the first measurement
of the time-course of visual suppression during
saccades (Latour, 1962) were both reported in
the same year, the latter in the second volume
of Vision Research. My work, conducted in
Lorrin Riggs active laboratory at Brown University, showed that under conditions of equivalent stimulation, a stimulus to the saccading
eye had to have about three times the luminance
of a stimulus to the fixating eye to produce a
threshold response, a difference of about 0.5 log
unit. But three times the luminance didnt seem
very impressive in light of the enormous range
of luminances encountered in the visual world.

Human visual suppression

Latours paper showed that suppression began

prior to the onset of a saccade and lasted
beyond its conclusion. It looked as if we
had and extraretinally originating inhibition of
vision, but that it must play a relatively minor
role in the overall elevation of threshold that
occurs during saccades in normal viewing.
Ahead lay the principal work of investigating
the magnitude and the time-course of saccadic
suppression using a variety of dependent
variables and a host of independent variables
related to the characteristics of stimuli and
viewing fields, of eye movements, and of
observer behavior. Ahead also lay the task of
attempting to sort out and identify the retinal
and extraretinal sources of suppression, based
upon the findings of these investigations.
Principal dependent variables. In the human
observer, the magnitude and time-course of
saccadic suppression have been measured primarily using psychophysical threshold techniques.
Many experiments have asked observers to indicate whether or not a briefly presented stimulus
was seen when it was presented during saccades
or during fixation., Others have employed a
more sophisticated forced choice technique
in which observers must judge which of two
saccades or two periods of steady fixation was
accompanied by the presentation of a stimulus.
A number of experiments have used variants of
these techniques to measure other dependent
variables such as suppression of suprathreshold
stimuli and several have investigated saccadic
suppression of image displacement.
Objective techniques (Riggs, 1976), including
measurement of the visual evoked response and
the pupillary light reflex have also provided
measures of suppression.
Principal independent variables. Four major
classes of independent variables have received
attention: (1) characteristics of the background
field of view, including field luminance and the
degree of homogeneity or pattern in the field; (2)
characteristics of the stimuli to be discriminated, including luminance increments or decrements, the structure or pattern of the stimulus,
spatial frequency, wavelength, retinal location,
and displacment or smear of the image on the
retina; (3) characteristics of the eye movements
executed by the observer, including their velocity, amplitude and their voluntary/involuntary
or active/passive nature; and (4) characteristics
of the observers attentional state or response
criteria.
Magnitude of suppression. The luminance level

1403

of a homogeneous viewing field (Ganzfeld)

determines importantly
the magnitude
of
suppression (Brooks et al., 1980a; Brooks and
Fuchs, 1975; Riggs et al., 1982b): the higher the
luminance level, the larger the suppression. The
Riggs et al. paper, for example, found threshold
elevations during saccades of about 0.85 log
unit at a field luminance of 3Oft-L and 0.40 log
unit at 0.03 ft-L, using full-field decremental
stimuli. Using incremental flashes under somewhat similar conditions, Brooks and Fuchs
(1975) found threshold differences ranging from
about 1.3 log units at high field luminances to
about 0.1 log unit in darkness.
The question of whether saccadic suppression
occurs in darkness has received special attention
because of its importance in separating out
retinally originating from extraretinally originating components of suppression. Many experiments have measured suppression in relative
darkness (Brooks and Fuchs, 1975; Brooks et
al., 1980a; Krauskopf et al., 1966; Latour, 1962,
1966; E. Matin et al., 1972; Mitrani et al., 1971;
Pearce and Porter, 1970; Richards, 1969; Zuber
et al., 1964; Zuber and Stark, 1966). Under
these conditions several investigators have
found no significant threshold elevations during
saccades (Brooks and Fuchs, 1975; Brooks et
al., 1980a; Mitrani et al., 1971; Richards, 1969).
On the other hand, Riggs et al. (1974), using as
stimuli electrically produced visual phosphenes
in conditions of total darkness, found saccadic
thresholds to be elevated by the equivalent of
about 0.4 log unit of relative luminance.
The degree of homogeneity or contour in the
background field is an important determiner of
the magnitude of suppression. Further, there is
an interaction between the characteristics of the
background field and the characteristics of the
stimulus to be detected. Contour in the background field raises saccadic thresholds substantially to punctate stimuli, while having less effect
on thresholds to diffuse stimuli (Brooks and
Fuchs, 1975; Mitrani et al., 1975). For example,
Brooks and Fuchs (1975) found saccadic
thresholds for spot stimuli on contoured backgrounds to be raised by more than 2 log units,
as compared with about 0.4 log unit on a
noncontoured
background. Full field flashes
produced a smaller effect of contour: threshold
elevations were about 1.75 log units on contoured backgrounds and 1.4 log units on a nch
contoured one. These investigators concluded
that saccadic thresholds to diffuse stimuli are
more regulated by field luminance while those to

1404

FRANCESC. VOLKMANN

punctate stimuli are more affected by field contour, with variations occurring as a function of
stimulus size and the crispness of edges (see also
Brooks and Impelman, 1981; Mitrani et al.,
1971; Wolf et al., 1978; Zuber et al., 1966).
Some investigators have questioned whether,
if saccadic suppression is attributable primarily
to masking effects (see below), any suppression
exists in conditions of genuine homogeneity of
the background field. Even under carefully controlled Ganzfeld conditions (Volkmann et al..
1978a; Volkmann et al., 1978b), it is difficult to
achieve a truly uniform field, and an observer
may receive some small degree of stimulation
from the defocussed edges of the nose and
orbits. To address this issue, Riggs and
Manning (1982) employed translucent goggles
to achieve a condition of complete whiteout,
and compared suppression of diffuse light
decrements under these conditions with that
measured in a more conventional Ganzfeld.
They found comparable magnitudes of suppression in the two cases, with thresholds elevated
by 0.7 to 1.l log units during saccades.
Focussing on the characteristics of the stimuli
to be discriminated, the magnitude of suppression has been found to be influenced by a
number of features in addition to size, crispness
of edges, and relative diffuseness, as described
above. Using sinusoidal grating stimuli superposed upon a background of equal space average luminance, Volkmann et al. (1978b) compared contrast sensitivity during saccades and
during fixation using horizontal gratings which
varied in spatial frequency. They found that the
magnitude of suppression varied with the spatial
frequency of the grating, with maximum suppression at low spatial frequencies where the
least contour and the least effect of retinal image
smear occur. A number of investigators have
compared acuity thresholds for foveally flashed
targets during saccades and steady fixation
(Volkmann, 1962; Krauskopf et al., 1966) with
findings of relatively small threshold elevations
during saccades. Similar results have come from
experiments measuring recognition of words or
letters (Uttal and Smith, 1968; Volkmann,
1962).
Saccadic suppression of retinal image displacement has received considerable attention
(Beeler, 1967; Bridgeman et al., 1975; Bridgeman et al., 1979; Bridgeman and Stark, 1979;
Brooks et ul., 1980; Lennie and Sidwell, 1978;
Mack, 1970; Mack et al., 1978; MacKay, 1970~;
Stark et al., 1976; Wallach and Lewis, 1965).

Bridgeman et al. (1979), using stimuli of sufficient luminance to be visible during a saccade,
showed that under optimal timing conditions,
target displacements are not detected if the
saccade exceeds about three times the extent of
the target displacement, and the displa~ments
of up to 4 deg arc are suppressed if they occur
during a large enough saccade. Likewise, a
number of investigators have shown that a brief
target stimulus presented just before or during
a saccade cannot be localized accurately in
space (Mateeff, 1978; L. Matin, 1972, 1982;
L. Matin et al., 1969; L. Matin et al., 1970;
L. Matin and Pearce, 1965; Sperling and
Speelman, 1966). This finding has important
implications for theories regarding the determinants of suppression, to be discussed below
(see also Hallett and Lightstone, 1976a, 1976b).
Saccadic suppression has been demonstrated
with fovea1 stimuli (Beeler, 1967; Lederberg,
1970; Mitrani et al., 1970b; Richards, 1968;
Uttal and Smith, 1968; Volkmann,
1962;
Volkmann et al., 1978b) and with peripheral
stimuli (Brooks and Impelman, 1981; Brooks
and Fuchs, 1975; Latour, 1962, 1966; Pearce
and Porter, 1970; Zuber and Stark, 1966).
Returning to the interaction between stimulus
and background field characteristics, Brooks
and Impelman (1981) have found that a
patterned background field significantly elevates
thresholds during saccades for fovea1 stimuli but
produces inconsequential elevations for stimuli
presented at a retinal location 5 deg arc eccentric to the fovea (see also Mitrani et al., 1975).
Most of the experiments discussed above have
been conducted under conditions designed to
eliminate or minimize smear of the retinal image
of the stimulus. This is important, of course, in
order to equate stimulation of the saccading
and the fixating eye (see E. Matin, 1974, pp.
904905), and is most often achieved by using
very brief (microsec duration) stimulus flashes
or stimulus configurations in which saccades
cannot produce significant image smear (see
Volkmann, 1976). It is possible, however, to
evaluate independently the loss of vision attributable to image smear and that attributable
to other sources (Mitrani et al., 1970a, 1971;
Volkmann et al., 1978a). It is obvious that
image smear plays an important role in suppression of stimuli that arrive during saccades in
normal photopic vision in a structured environment. As well, it is clear that saccadic suppression is not eliminated under conditions in
which image smear does not occur.

Human visual suppression

The characteristics of the saccades during

which suppression is measured are, as might be
expected, important determiners of the magnitude of suppression. Suppression increases as
a function of amplitude for voluntary saccades
(Bridgeman et al., 1975; Brooks et al., 1980a;
Latour, 1966; Mitrani et al., 1970; Stevenson et
al., 1986; Volkmann et al., 1981). In the latter
experiment, suppression ranged from about
0.7 log unit for 2 deg arc saccades to about
1.05 log unit for 32 deg arc saccades under the
same viewing conditions. There has been some
disagreement about whether suppression also
accompanies the small involuntary flicks of
the eye that occur during normal fixation (see
Steinman et al., 1973). Krauskopf et al. (1966)
report no suppression, while Beeler (1967),
Ditchburn (1955) Ebbers (1965) and Zuber
and Stark (1966) report evidence of suppression.
Quantitatively, Beelers results indicate a magnitude of suppression of approx. 0.5 log unit of
relative luminance during flicks of an amplitude
of about 30 arc or smaller. Finally, suppression
has been shown to accompany the fast phase
of optokinetic
nystagmus (Latour,
1966),
vestibular nystagmus (Zuber and Stark, 1966),
and voluntary nystagmus (Nagle et al., 1980).
Voluntary nystagmus has been shown to be
essentially saccadic in nature (Shults et al.,
1977), and it seems reasonable to believe that
the other types of nystagmus are saccadic also
in the fast phase (see Bahill et al., 1975).
Quantitatively, Nagle et al. (1980) found average threshold elevations of 0.53 log unit of
relative luminance for stimuli presented during
the fast phase of voluntary nystagmus.
Several investigators
have measured the
magnitude of suppression as affected by the
observers direction of attention or by his or
her criteria of responding. Lederberg (1970), for
example, addressed the question of whether the
elevation of saccadic over fixating eye thresholds might be due in part to the observers
attending to executing the voluntary saccade
rather than to the stimulus to be discriminated.
She substituted a voluntary hand-movement for
the saccade and found no elevation of visual
threshold (see also Greenhouse et al., 1977;
Latour, 1966; Mitrani et al., 1973). Pearce and
Porter (1970) addressed the possible effect of
changes in the observers response criteria. They
found a somewhat larger magnitude of suppression with bias-free forced choice psychophysical procedures than with yes-no procedures. While a wide variety of psychophysical

1405

procedures are applicable in this field, one

cannot fail to note in re-reading the literature
that there has been an insufficient attention to
using sound psychophysical procedures and to
evaluating experimental results in terms of the
procedures used.
Time-course of suppression. Most experiments
conducted to map the time-course of saccadic
suppression have used a frequency of seeing
technique in which a single value of stimulus
luminance that is just always visible to the
fixating eye is delivered on many trials in various temporal relations to the onset of a saccade,
and the observer reports after each trial whether
or not he detected the stimulus (Beeler, 1967;
Brooks et al., 1980a; Brooks and Fuchs, 1975;
Latour, 1962, 1966; Lederberg, 1970; Mitrani
et al., 1970b; Pearce and Porter, 1970; Richards,
1969; Volkmann et al., 1968; Zuber and Stark,
1966). The time-course of suppression has also
been assessed using suprathreshold stimuli and
a psychophysical matching procedure (Riggs
et al., 1982b), and by measurements of forced
choice psychophysical thresholds for stimuli of
varying contrast, delivered at a range of times
in relation to saccades (Volkmann and Moore,
1978; Volkmann et al., 1978a). In addition to
psychophysical methods of assessment, several
experiments have used the visual evoked response (a method to be described in the next
section of this issue) to estimate the time-course
of suppression (Brooks, 1977; Chase and Kalil,
1972; Duffy and Lombroso, 1968; Gross et al.,
1967; Michael and Stark, 1976; Starr et al.,
1969; Vaughan, 1973).
By whatever measures used, results show that
saccadic suppression begins to appear for stimuli delivered prior to the onset of the saccade. It
reaches a maximum (i.e. a minimum frequency
of seeing) for stimuli delivered during the saccade, and gradually dissipates over several tens
of milliseconds after the saccade has ended [see
Fig. l(A)]. In describing the time-course in these
terms, it is important to remember that we are
relating the perceptual response to the time of
arrival of a stimulus to the eye in relation to the
onset of a saccade. If suppression is in fact a
central neural event, the specification of its
actual time course would require knowledge of
the transmission times for the neural response to
the stimulus to reach the site of suppression.
The precise time course depends importantly, as
one would expect, upon the characteristics of
the background field, the adaptation of the eye,
the characteristics of the stimulus, the location

FRANCESC. VOLKMANN

w
#

100
75

Iii 50
Y
8 25
5

100

z:

too

id
m 75

Y
to

75

)r 50
Y
3 25

!z 50
Y
25
2
a
0

-100
TIME fMSECf

100

TIME

(MSEC)

200

Fig. I. Examples of the time-course of suppression associated with a variety of oculomotor and ocular
events. (A) Suppression of vision of brief flashes of light presented in temporal proximity to 6 deg
voluntary saccades under photopic viewing conditions for three observers (replotted from Volkmann,
1962); (B) suppression of vision of brief flashes of light presented in temporal proximity to involuntary
flicks of the eye under scotopic viewing conditions for two observers (replotted from Be&r, 1967); (C)
suppression of vision of brief flashes of light presented in temporal proximity to the fast phase of
postrotary vestibular nystagmus (replotted from Zuber and Stark, 1966); (D) suppression of vision of brief
light decrements presented in temporal proximity to reflex eyeblinks elicited by an air puff to the cornea
(replotted from Manning et al., 1983); (E) suppression of vision (circles) and of the pupillary response
(triangles) to brief light flashes presented in temporal proximity to 8deg voluntary saccades. Though
superposed in this figure for comparative purposes the pupillary responses is actually delayed (replotted
from Zuber er al., 1966); (F) suppression of vision of a briefly flashed target presented to the fixating eye
in temporal proximity to a saccade-like movement of a background field (replotted from MacKay, 197Oa).
In all examples except (D), the dependent variable is the percentage of trials on which a stimulus is seen;
a single value of stimulus luminance is chosen which is just above threshold for the fixating eye. In example
D, quantitative measurements of sensitivity have been derived using a forced choice psychophysical
procedure. The independent variable in all examplesis the time of occurrenceof the stimulusin relation
to the onset of the eye movement, eyeblink, or displacement of the background field.

of the stimulus on the retina, and the amplitude

of the saccade.
The luminance of the backgroundfield appears
to be an important determiner of time-course.
While the magnitude of suppression decreases at
low luminance levels, its time-course becomes
broader. Using a suprathreshold matching technique, for example, Riggs et al. (1982b) found
that at a field luminance of 3Oft-L the timecourse of suppression to a full-field decrement
was quite steep, with a maximum at O-10 msec

after saccade onset. At a field luminance of

0.03 ft-L, the time-course was much broader,
showing an earlier onset of suppression and a
broad maximum from about 20 msec before to
about 30 msec after the beginning of the saccade. Saccade duration was apptox. 40 msec.
Volkmann et al. (1968) have argued that peripheral stimuli or stimuli delivered to the eye under
conditions of dark adaptation should require a
longer processing and transmission time than
fovea1 stimuli that are viewed under conditions

1407

Human visual suppression

of light adaptation. If one assumes that suppression is mediated by a central or extraretinal

inhibitory effect, the time-course of suppression
should appear to begin earlier prior to saccade
onset in the scotopic situation.
Various characteristics of the stimulus that are
important determiners of the time-course of
suppression include luminance, retinal location,
size and contour, and wavelength. Zuber and
Stark (1966) noted that in the dark adapted eye,
the duration of suppression is inversely related
to the intensity of the stimulus, with suppression
to dim stimuli beginning earlier in relation to
saccade onset, showing longer and broader
maxima, and declining in about the same temporal relation to the saccade as suppression to
brighter stimuli. Brooks and Fuchs (1975) also
found broader suppression curves with dimmer
stimuli, but their experiment also showed slower
recovery from suppression under these conditions. Mitrani et al. (1970b) found that the
time-course of suppression is different for stimuli falling on different retinal locations, but the
precise relations must depend on the adaptation
level of the eye and the size and contour of
the stimuli (see also Latour, 1966). Lederberg
(1970), using a wavelength discrimination task,
found that the time-course of suppression varies
with the wavelength of the test stimulus, with
maximum suppression occurring for red and
green stimuli presented during saccades and
for blue stimuli presented 40-80 msec after saccade onset (see also Richards, 1968).
The time-course of suppression varies as a
function of saccade amplitude (Mitrani et al.,
1970; Brooks et al., 1980a; Stevenson et al.,
1986; Volkmann et al., 1981). Stevenson et al.
(1986) found that the onset of suppression prior
to saccades of 2 and 32deg arc followed a
similar time-course, but for the large saccade
maximum suppression lasted somewhat longer
and the recovery of sensitivity was slower. It
is clear, however, that neither the magnitude
nor the time-course of suppression is tightly
linked to saccade amplitude; as Beeler (1967)
has shown, substantial amounts of suppression
accompany microsaccades, and the period of
time around the saccade during which there is
some loss of sensitivity may be as long as
lOO-200msec [see Fig. l(B)].
Lorber et al. (1975) have reported suppression of the pupillary light reflex during saccades,
with a time-course similar to that determined
psychophysically. An example of their results is
shown in Fig. l(E).

VISUAL SUPPRESSION
DURING
NONSACCADIC
EYE MOVEMENTS

Several experiments have investigated visual

suppression during types of eye movements
other than saccades. While suppression does not
appear to accompany smooth pursuit eye movements (Starr et al., 1969) it has been shown to
accompany passive eye movements and the eye
movements of vergence.
Richards (1968) reported small but similar
elevations in threshold during voluntary saccades and during passive movements of the eye
produced by tapping the eyeball near the outer
canthus (see also Helmholtz, 1963). Suppression
thus appears to exist in the absence of a possible
centrally originating corollary discharge that
might accompany the neural signal for a saccade
(see below).
Manning and Riggs (1984) have now extended the investigation of visual suppression, to
vergence movements. Using full-field luminance
decrements as stimuli in a photopically illuminated Ganzfeld, they found thresholds to be
elevated over those for steady fixation by about
0.5 log unit when the stimuli were presented
near the beginning of a 2-3 deg convergent or
divergent eye movement. They suggest that
saccadic suppression may be only one example
of a more generally occurring phenomenon of
visual suppression associated with eye movement
initiation (Manning and Riggs 1984, p. 524).
VISUAL

SUPPRESSION
EYEBLINKS

DURING

Eyeblinks, like saccades, produce momentary

interruptions
of vision at least every few
seconds. Moreover, while a typical mid-sized
saccade lasts only about 50msec, the time
during which the pupil is occluded and vision
thereby interrupted during a normal blink is
100-150 msec. Yet we are seldom aware of this
blackout due to blinks. This observation has led
to several investigations of visual suppression
during eyeblinks. Volkmann et al. (1980) used a
technique to bypass the eyelids and deliver
comparable stimuli to the retina during fixation
and during voluntary eyeblinks. They found
thresholds to brief full-field decrements in otherwise steady retinal illumination to be increased
by 0.4-0.7 log unit during voluntary blinks (see
also Riggs et al., 1984). Although certain
deflections of the eye may accompany blinks
(Collewijn et al., 1985), the threshold elevation
seems unlikely to be attributable to such eye
movements.

1408

FRANCESC. VOLKMANN

Riggs et al. (1981) used a suprathreshold

matching procedure to estimate the visual
effects of a blink and to compare the effects of
real blinks with those of simulated blinks
produced by light decrements in a Ganzfeld.
Blink-related visual suppression was evaluated
by comparing the decrements under the two
conditions when the observer judged them to be
equal. Magnitudes of suppression ranged from
0.5 to 1.0 log unit at a photopic Ganzfeld
luminance and from 0.3 to 0.7 log unit at a
scotopic Ganzfeld luminance. Thus, the magnitude of suppression during voluntary eyeblinks
is similar to that often reported during saccades.
As well, it shows a similar variation with the
level of background illumination. Riggs et al.
(1982) showed a suppression of the pupillary
response using a similar procedure. In a further
analysis, Volkmann et al. (1982) measured the
magnitude of suppression during each of the
major activities performed by the eyelids during
blinking. They found suppression to be primarily related to lid-closing, and insignificantly
related to lid-opening.
Visual suppression accompanies spontaneous
and reflex blinks as well as voluntary blinks
(Manning et al., 1983a,b). The magnitude of
suppression is similar in the two cases; for reflex
blinks it is about O-2-0.5 log unit, using the
technique of bypassing the eyelids developed by
Volkmann et al. (1980) and eliciting blinks by
means of an airpuff to the cornea.
Visual suppression during eyeblinks follows a
time-course similar to that of suppression accompanying saccades (Volkmann et al., 1979;
White et al., 1984). although this comparison is
very general since, as shown above, the precise
time-course of saccadic suppression varies with
experimental conditions. Investigations to date
have not sampled sensitivity at intervals spaced
sufficiently close to map the fine structure of the
time-course of suppression, but the general form
of the curves can be seen in Fig. l(D). Suppression begins for test stimuli presented prior
to blink onset, and may even reach a maximum
value by 30-40 msec before the upper lid begins
to cover the pupil. This very early onset of
suppression measured psychophysically implies
a long latancy for the neural response to the
weak test stimuli to arrive at the site of suppression in the brain. Recovery from suppression is gradual over a period of 100-200 msec
after blink onset. Since, as noted above, blinks
tend to be of substantially longer duration than
saccades, the similar time-course of visual

suppression in the two cases must mean that the

eye has regained its sensitivity sooner after the
completion of a blink than after the completion
of a saccade.
VISUAL

MASKING

Eye movements, blinks, and movements of

the head and body continuously translate even
constant physical stimuli into a series of transient retinal stimuli (Matin, 1975). An understanding of the visual effects of transients is
therefore basic to our understanding of visual
processing, and a large body of research has
developed in this field, much of it in the last 25
years. This research can be characterized as
measuring changes in the response to a briefly
presented target stimulus as a function of
another stimulus that is also presented briefly in
some specified temporal and spatial relation to
the target. The term visual masking refers to the
destructive interaction or interference that is
typically measured in experiments of this kind.
It is beyond the scope of this paper to attempt
a summary of results in this complCx field, but
a number of excellent reviews are available
(Breitmeyer, 1980, 1984; Breitmeyer and Ganz,
1976; Fox, 1978; E. Matin, 1975).
h4etacontrast
Visual interference that is produced with respect to a target stimulus by a masking stimulus
which follows it in time and which stimulates
a non-overlapping retinal location is termed
metacontrost. This particular form of backward
masking has received a great deal of attention in
the literature (for reviews, see, in addition to
those cited above, Alpern, 1953; Bridgeman,
1971; Lefton, 1973; Weisstein, 1972). In addition to being an interesting field of investigation
in its own right, metaconlrast is of special
interest because of its relation to research on
saccadic suppression (Alpern, 1969; E. Matin,
1974; see also Dodge, 1900). According to the
metacontrast paradigm, when the eye executes a
saccade, conditions are set up by which the
image of the object of fixation at the end of the
saccade may interfere with perception of the
blurred streak that might otherwise be visible
during the saccade. Ethel Matin explicitly raised
the possibility that the lateral masking ordinarily studied in the laboratory is only a weak
case of a much more powerful phenomenon and
that we must look at the image generated on the
retina by the saccading eye for the optimal

Human visual suppression

stimulus for masking (Matin, 1974, p. 907).

Investigations of masking in relation to saccadic suppression have taken several forms. In
a relatively early experiment, E. Matin et al.
(1972) stimulated the horizontally saccading eye
with a veritical slit of light at luminances high
enough to be visible in the dark, and varied the
duration of stimulation. They found that when
stimulation ended prior to the conclusion of the
saccade, the observer reported having seen a
blurred streak of light and could estimate its
length by means of a comparison stimulus. With
longer stimulus exposures which extended into
the period after the saccade, the streak appeared
shorter and dimmer until, with sufficiently long
presentations, the observer saw no streak at all
but only the sharply defined light slit. The clear,
relatively brighter (on any given photoreceptor)
slit visible at the end of the saccade thus
appeared to mask the blurred streak during the
saccade; this streak would otherwise have been
visible. In a similar experiment, Campbell and
Wurtz (1978) illuminated a contoured visual
scene for various durations of time before,
during and after saccades and found evidence of
both forward masking and metacontrast. They
suggest that the term saccadic omission is
more descriptive of these effects than the term
saccadic suppression. Corfield et al. (1978)
went on to simulate with the fixating eye the
retinal events associated with saccades by
presenting a blank field of short but variable
duration bracketed in time by vertical gratings
of space average luminance equal to that of the
blank. They found that with high spatial frequency gratings, blank field durations as long as
350 msec may not be perceived.
A substantial number of experiments have
demonstrated that saccadic suppression can be
simulated by presenting to the fixating eye a
target stimulus in close temporal proximity to a
rapid displacement of a background field. Both
the magnitude and the time-course of the masking effects produced with this paradigm are
within the range of those measured for saccadic
suppression (Brooks and Fuchs, 1975; Brooks
and Impelman, 1981; Brooks et al., 1980a;
MacKay, 1970a, 1970b; Mateeff et al., 1976;
Mitrani et al., 1971; Mitrani et al., 1975; Mitrani
et al., 1973). Figure l(F) shows a sample curve,
from MacKay (1970a).
Most of these experiments have used a
relatively small test flash as the stimulus to be
detected, though a a few have varied the size of
the test stimulus (Brooks and Fuchs, 1975;

1409

Brooks and Impelman, 1981). The characteristics of the background fields used have been
quite varied. Brooks and Fuchs (1975) and
Brooks et al. (1980a) included in their studies
large background fields which were uniform
except, sometimes, for fixation points, and
which were varied in luminance. Their results
showed similar elevations of threshold whether
the eye moved across the background in a
saccade or the background was displaced in a
saccadic fashion across the retina of the fixating
eye. Thresholds increased as a function of field
luminance, and the increase was larger for large
or full-field test stimuli than for small stimuli.
Books et al. (1980a) found similar threshold
elevations when the background was momentarily brightened rather than displaced. As an
example of the threshold elevations measured,
Brook and Fuchs (1975) found, under comparable conditions for two subjects, elevations of
0.80 and 0.95 log unit of luminance for diffuse
stimuli presented during saccades, and 0.79 and
0.88 log unit for the same stimuli presented to
the fixating eye during displacement of the
background field.
A number of studies have used contoured or
patterned background fields. The contour may
be provided only by the edges of the field
(Mackay, 1970a) or may be introduced in
the form of gratings (Breitmeyer and Valberg,
1979; Brooks and Fuchs, 1975; Brooks and
Impelman, 1981; Mateeff et al., 1976) or other
patterns (Brooks and Fuchs, 1975; Mitrani et
al., 1971) located in the periphery of the visual
field. Results show a pronounced elevation of
threshold as a function of the movement of
contours across the retina of the fixating eye.
In a comparison experiment, for example,
Brooks and Fuchs (1975) found that detection
threshold for a stripe stimulus presented on a
striped background increased by 2.15 log units
when the stimulus was delivered during a saccade, and by 2.27 log units when the stimulus
was delivered to the fixating eye during displace:
ment of the background.
Lateral masking effects are typically considered to operate over a maximum distance on the
retina of 2-3 deg separation between the target
and the mask (Breitmeyer, 1984). The type of
peripheral stimulation provided by the background contours in many of the above experiments, however, produces a substantial elevation of threshold for fovea1 stimuli, even though
the contours may lie in a remote retinal location
(Breitmeyer and Valberg, 1979). This effect,

1410

FRANCESC. VOLKMANN

termed the far-out jerk effect by Breitmeyer

and Valberg, is found only in the fovea. It may
well be an important determiner of threshold
elevations measured for stimuli dehvered during
saccades across highly contoured visual fields
under photopic conditions of vision.
The time-course for masking, like that for
saccadic suppression, varies with intensity of the
test stimulus (Brooks and Fuchs, 1975), with the
angular displacement of the background contour (Brooks et al., 1980b; Mateeff et al., 1976),
and with the luminance of the background field
(Brooks and Fuchs, 1975; Brooks et al., 1980a).
In the case of fields consisting of gratings, it
varies as well with the spatial frequency of the
gratings (Corfield er al., 1978; Mitrani et al.,
1975; Mateeff et al., 1976).
DETERMINANTS
OF VISUAL
SUPPR~ION

The research of the last 25 years has both

clarified and complicated the theoretical issues
raised by the early investigators. With respect to
saccadic suppression, we are much better able to
delineate the conditions under which threshold
elevations associated with saccades may be attributable to events originating in the retina and
events originating extraretinally or centrally in
the brain: I think that most investigators are
moving away from the type of dichotomous
thinking that attempts to account for a11of the
findings with one mechanism. At the same time,
the extension of research on saccadic suppression to nonsaccadic eye movements and to
eyeblinks has complicated the matter considerably. On the one hand, one cannot help but nbte
the remarkable similarity in both magnitude
and time course between saccadic suppression
and suppression accompanying these other
quite different activities. This similarity might
lead one to suspect that all of these types
of suppression are mediated by common
mechanisms. On the other hand, some of the
mechanisms that seem to offer considerable
explanatory
power for describing saccadic
suppression, such as some of the afferent
mechanisms elaborated below, do not work well
for explaining other forms of suppression. We
do not yet know to what degree common mechanisms may mediate the various forms of suppression. It is therefore productive to see how
well the major mechanisms proposed to account
for saccadic suppression also account for the
other forms.

Retinal mechanisms
tasking. The similarity in both magnitude
and time-course of threshold elevation produced by masking and by saccadic suppression
has led a number of investigators to conclude
that saccadic suppression can be accounted
for largely or entirely in terms of events that
originate in the retina (Brooks and Fuchs, 1975;
Brooks and Impelman, 1981; Brooks et al.,
1980a; Campbell and Wurtz, 1978; Corfield et al.,
1978; Mitrani et al., 1971; Mitrani et al., 1975).
It is clear that the rapid movement of luminance
gradients or contours across the retina, whether
produced by saccades or by displacement of the
visual field, results in comparable changes in
perception. As well, stimuli reaching the stationary eye just after the conclusion of a saccade
may interfere with perception of stimuli which
might otherwise have been visible during
the saccade. Masking effects, therefore, undoubtedly play a primary role in threshold
elevations which accompany saccades in lighted,
contoured environments. It is equally clear,
however, that saccadic suppression can be
shown to exist under experimental conditions in
which masking effects are minimized, such as in
a lighted Ganzfeld where no abrupt luminance
changes occur (Riggs and Manning, 1982;
Volkmann et al., 1978b) or in total darkness
(Riggs et al., 1974). Further, masking would be
expected to have IittIe effect during microsaccades, slow convergence or divergence movements, or eyeblinks made in darkness. Masking
effects, important as they are, may thus account
for visual suppression only under a limited
range of conditions. Breitmeyer (1984) has proposed a neurophysiological model for masking
that is based upon inhibitory effects mutually
exerted by transient and sustained neural
channels. He views these afferent effects as
working in conjunction with a central or efferent
corollary discharge to produce the threshold
elevations that we call saccadic suppression
(see Breitmeyer, 1984, pp. 324335).
Effects of rapid retinal image motion. The
rapid sweep of the image of a stimulus across
the retina during a saccade may act in two
obvious ways to decrease vision of the stimulus.
First, unless the stimulus is presented very
briefly, its image is smeared across the retina so
as to be substantially unidentifiable. Second, the
saccade has the effect of decreasing the duration
of stimuIation on each retinal receptor. For
brief durations of stimulation, time and inten-

Human visual suppression

sity are reciprocally related for a given photochemical effect; therefore, decreasing the duration of stimulation decreases the effective
stimulation at the receptor (Blochs law). Thus,
under normal conditions of viewing, a stimulus
may not be noticed during a saccade both
because it is smeared and because its effective
brightness is reduced.
Saccadic suppression, however, is not eliminated by the use of very brief test flashes or
other stimulus arrangements which minimize
the effects of the rapid eye movement (Mitrani
et al., 1970a; Volkmann, 1962; Volkmann et al.,
1978a). Smear or reduced photochemical effects
could also not account for the elevation of
threshold that precedes and follows saccades or
for the elevation of threshold accompanying
vergence movements or eyeblinks.
Shearing forces in the retina. A model of
saccadic suppression that has been often cited
but little investigated is that of Richards (1968,
1969). He suggested that a saccade has an
effect on the eyeball similar to rapidly rotating
a bowl of jelly; different intraocular materials,
including different layers of the retina, might be
expected to accelerate and decelerate at different
relative velocities. Thus mechanical shearing
forces are set up which may disrupt the processing of neural signals. More specifically, under
conditions of light adaptation these forces could
raise the level of background noise in the retina
at times during and near a saccade, and could
thus interfere with perception of a test stimulus.
Results of experiments which show an increase
in the magnitude and duration of suppression
with an increase in saccade amplitude are to
some degree consistent with Richards model.
Shear, however, would be expected to be determined by acceleration, and the magnitude of
suppression does not vary linearly with acceleration. Further, Richards model would not predict threshold elevations to stimuli presented
during microsaccades [see Fig. l(B)] or during
saccades in total darkness, and does not seem
relevant to experiments showing suppression
during vergence movements or eyeblinks.
Extraretinal mechanisms
Retinal mechanisms of suppression are best
investigated by presenting to the fixating eye
stimulus situations in which the effects of conditions such as masking the retinal smear can be
evaluated evaluted separately from any central
of efferent effects. Conversely, extraretinal
mechanisms are best illuminated by presenting

1411

to the moving or blinking eye stimulus

situations in which these retinal effects are
minimized or eliminated. Unfortunately, many
experiments have confounded the delineation
of extraretinal
mechanisms by measuring
suppression under conditions in which these
mechanisms cannot be separated from retinally
originating mechanisms.
As reviewed above, the results of carefully
controlled experiments which minimize or
eliminate the effects of afferent mechanisms
show significant suppression of vision during
saccades, vergence movements and blinks.
Such results have typically been interpreted as
supportive of the notion of an extraretinally
originating neural inhibitory mechanism which
acts to decrease visual sensitivity during these
behaviors.
Holt (1903; see also Sherrington,
1918)
attributed this neural suppression to signals
originating in the extraocular muscles; this
model has since come to be known as feedback or inflow theory. Without additional
reliance upon afferent mechanisms such as
masking, inflow theory is not supported by
evidence regrading the temporal characteristics
of suppression, particularly the onset of suppression prior to the onset of activity in the
extraocular muscles. Inflow from the extraocular muscles may, however, provide information regarding eye position that is used in the
maintenance of visual stability (E. Matin, 1974,
1982; see also Shebilski, 1977).
The general model of neural inhibition that
describes many of the experimental results has
come to be referred to as an efferent,
outflow or feedforward theory, in which a
signal originating in the brain and associated
with the central command to the extraocular
muscles feeds forward
to inhibit visual
perception at some central site in the visual
system. The outflow theory is based upon
Helmholtzs effort of will (Helmholtz, 1963),
von Holst and Mittelstaedts Efferenzkopie
(von Holst and Mittelstaedt, 1950; von Holst,
1954), and Sperrys corollary discharge (CD)
(Sperry, 1950). One form of the theory is diagrammed in Fig. 2. Here, the oculomotor command signal gives rise to an efference copy or
corollary discharge of equal and opposite sign
to the reafference signal arising from changes
in retinal stimulation that occur as a result of
the saccade; the two signals combine to cancel
the effects of the changes, all at the unconscious
level. Thus the efference copy or corrollary

FRANCESC. VOLKMANN

1412

CONSCIOUS
LEVEL

VOLUNTARY

IMPULSE

PERCEPTION

OCULOMOTOR
COMMAND

EFFERENCE
L

UNCONSCIOUS

COPY

I RESULTANT

SIGNAL

REAFFERENCE

Fig. 2. Von Hoists proposal to account for visual stability by the subtraction of an efference copy from
incoming visual signals (redrawn from MacKay, 1972).

discharge may in general be envisoned as an

extraretinal signal that informs the visual system
of the intended position of the eye (Bridgeman
and Fishman, 1985; Skavenski, 1972; Skaven,ski
et al,, 1972; Stark, 1985; Schiller, this issue).
It is possible to study situations in which a
mismatch exists between the CD and the
afferent signals from the retina. Helmholtz
(1963) pointed out that patients with oculomotor paralysis reported a shift in the location
of visual images when they tried unsuccessfully
to move their eyes. Further study by L. Matin
et al. (1982, 1983) with subjects under the effects
of systemic D-tubocurarine showed that the
effect of CD depended on the conditions of
visual stimulation. They instructed observers to
try to fixate with the paralyzed eye a display of
illuminated points located at a constant offset
from the primary position, producing a constant
CD (or effort of will). Under these conditions, perception of straight ahead was normal
as long as a structured visual field was present;
the extraretinal signal was superseded by the
visual field stimuli arriving at the retina. When
structure was removed from the field, however,
the illuminated points appeared to the subject to
drift in the direction of the deviated CD; the CD
became the predominant factor in determining
the perception of location.
Another manipulation which has been used to
induce a mismatch between CD and,eye position is the eyepress. Subjects are asked to monocularly fixate a target, and then the eye is moved
passively by pressing upon the outer canthus or
lower lid. The extra innervation required to
maintain fixation reflects an increase in CD. The
eyepress produces a perception of target movement, which can be attributed to the mismatch

between the CD and the retinal signals. If the

subjects other eye is occluded, a deviation in
the occluded eye can be recorded as the result
of the binocular change in innervation to the
oculomotor muscles to counter the effect of the
eyepress (see Bridgeman, 1979; Bridgeman and
Delgado, 1984; Bridgeman and Fishman, 1985;
Post et al., 1984; Skavenski et al., 1972; Stark
and Bridgeman, 1983).
Since classical CD theory postulates that the
perception of stability in the visual world is
based upon a match between the CD and the
afferent signals generated by the shift in the
retinal image during a saccade, it cannot adequately explain the findings that displacement of
a target stimulus that occurs during a saccade is
not perceived. MacKay (1972, 1973) has proposed a modilied form of the theory, in which
the extraretinal signal simply informs the system
of an eye movement, and any resulting image
movement which is roughly consistent with the
extraretinal signal is interpreted as a movement
of the eye rather than as a movement of the
visual world.
Bridgeman and his collaborators have recently questioned all theories which treat visual
stability as a single vector, and have presented
data to support the hypothesis that stability is
determined by cognitive, attentional variables
rather than by oculomotor properties (Bridgeman, 1981; Bridgeman et al., 1979).
A commonly held view is that one of the
means by which CD maintains visual stability
and direction constancy is saccadic suppression.
E. Matin (1974, 1976, 1982) has proposed a dual
mechanism theory of direction constancy in
which the first mechanism is a saccadecontingent compensatory shift produced by an

1413

Human visual suppression

extraretinal signal in the perceived direction

(or directional local sign) of a stimulus. Imperfections exist in this system, however, and the
time-course of the shift does not follow precisely
the time-course of the saccade (see Shebilske,
1976, 1977). Yet the visual world appears
stable. Matin envisions saccadic suppression as
the second mechanism, contributing to visual
stability by preventing the perception of stimuli
received during the transient period just before,
during and after a saccade, when the mismatch
between the compensatory shift and the retinal
stimulation would otherwise destabilize perception of an objectively stable world. She supports
the notion that an extraretinal signal provides a
portion of the basis for saccadic suppression,
but explicitly leaves open the question of
whether this signal might be the same signal as
that which produces the compensatory shift in
local sign.
Matin suggests that the results of Nagle
et al. (1980), which show both suppression and
oscillopsia during voluntary nysta~us,
may
indicate that the two extraretinal factors are in
fact different (E. Matin, 1982). An alternative
explanation is possible, based upon the hypothesis that (a) there is a loose rather than a tight
linkage between the CD and the eye movement
and (b) the duration of suppression exceeds the
intersaccade interval for voluntary nystagmus.
Under these conditions, a stimulus sufficiently
bright to be seen during nystagmus might well
be expected to be perceived as jumping back and
forth.
The linkage between suppression and the CD
clearly seems to be loose rather than tight. Such
a notion is supported by the results of experiments which show that the magnitude and time
course of suppression do not increase linearly
with increases in saccade amplitude. As well, it
is supported by the findings of comparable
magnitude and time-course of suppression during oculomotor behaviours of quite diverse durations, namely saccades, vergence movements,
and blinks (see Fig. 1).
CONCLUSIONS

The perception of a stable visual world

requires a system that discriminates between
image motion on the retina that is produced by
movements of the eyes and image motion that
is produced by movements of external objects.
The perception of a clear and continuous visual
world requires a system that ignores blurred

images produced by retinal motion and momentary interruptions of vision produced by eyeblinks. To meet these requirements, the human
perceptual system has evolved both afferent and
efferent selective mechanisms, including mechanisms of visual suppression of stimuli which
would otherwise interrupt or destabilize perceg
tion. These mechanisms, taken together, operate
over the entire dynamic range of vision and
in every possible stimulus environment with
the effect of selectively discarding info~ation
that might lead to maladaptive responses. They
operate with every blink, with every change in
fixation from a near to a far object or the
reverse, and with every glance from one object
to another in the visual scene.
We know more about the retinal mechanisms
than we do about the extraretinal ones, and
more about their perceptual consequences
than about their physiological foundations.
Undoubtedly, in the next 25 years the precise
relations among the mechanisms and the
different levels of analyses of the systems will be
illuminated much further.
Those of us who have worked in this field
over the last 25 years have experienced the
rewards of solving small pieces of an enormously complex puzzle, and of imagining how our
pieces fit with others into a coherent whole. For
myself, perhaps the greatest reward has been to
learn about a beautiful and intricate adaptive
system and to come to appreciate increasingly
the evolutionary processes through which it
evolved.

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