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Vision

Res. Vol. 26, No. 9,

pp.

1401-1416. 1986

0042-6989186 3.00 +

0.00

Printed in Great Britain. All rights reserved

Copyright 0 1986 Pergamon Journals L&d

HUMAN VISUAL SUPPRESSION

FRANCES C. VOLKMANN

Department of Psychology, Smith College, Northampton, MA 01063,

U S A

~~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 evolution-

ary 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 rela-

tion 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

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 sup-

pression 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 impair-

ment 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 re-

spective roles that retinal and extraretinal events

play in the impairment of vision that accom-

panies 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 psycho-

physical 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 SUPPRE~ION

Observations and theories prior to 1960

Almost a century ago, Erdmann and Dodge

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FRANCES 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 investi-

gators 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 mech-

anism(s) responsible for it. Variations on the

models which they proposed to account for

suppression have in large measure set the frame-

work 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 inhib-

itive 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 stimu-

lation 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 stimula-

tion (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 electro-

oculogram, and limbus, pupil, and eyelid track-

ing (Young and Sheena, 1975). It required the

development of techniques of stimulus presenta-

tion, 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 appropri-

ate psychophysical techniques for determining

and evaluating the observers perceptual re-

sponse (Green and Swets, 1966). In general, the

recent work that has contributed most to the

field is that which has moved the analysis to-

ward 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 Vi sion Research. M y work, conducted in

Lorrin Riggs active laboratory at Brown Uni-

versity, showed that under conditions of equiv-

alent 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.

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Human visual suppression

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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 prim-

arily using psychophysical threshold techniques.

Many experiments have asked observers to indi-

cate 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 discrimin-

ated, including luminance increments or decre-

ments, 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 veloc-

ity, 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

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 some-

what 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 origin-

ating components of suppression. Many experi-

ments 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 back-

ground field raises saccadic thresholds substan-

tially 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 back-

grounds 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 con-

toured 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

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FRANCES . VOLKMANN

punctate stimuli are more affected by field con-

tour, 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 con-

trolled 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 suppres-

sion 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 sup-

pression 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 super-

posed upon a background of equal space aver-

age luminance, Volkmann et al. (1978b) com-

pared 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 sup-

pression 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 dis-

placement has received considerable attention

(Beeler, 1967; Bridgeman et al., 1975; Bridge-

man 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 suffi-

cient 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 deter-

minants 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 eccen-

tric 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 attri-

butable 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 sup-

pression of stimuli that arrive during saccades in

normal photopic vision in a structured environ-

ment. As well, it is clear that saccadic sup-

pression is not eliminated under conditions in

which image smear does not occur.

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Human visual suppression

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The characteri sti cs of t he saccades during

which suppression is measured are, as might be

expected, important determiners of the mag-

nitude 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 mag-

nitude 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 aver-

age 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 di recti on of at t ent i on

or by his or

her crit eri a o f responding. Lederberg (1970), for

example, addressed the question of whether the

elevation of saccadic over fixating eye thresh-

olds 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 sup-

pression with bias-free forced choice psycho-

physical procedures than with yes-no proce-

dures. While a wide variety of psychophysical

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 vari-

ous 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 a l ., 1970b; Pearce and Porter, 1970; Richards,

1969; Volkmann et a l ., 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 re-

sponse (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 a l .,

1967; Michael and Stark, 1976; Starr et al.,

1969; Vaughan, 1973).

By whatever measures used, results show that

saccadic suppression begins to appear for stim-

uli delivered prior to the onset of the saccade. It

reaches a maximum (i.e. a minimum frequency

of seeing) for stimuli delivered during the sac-

cade, 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

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FRANCESC VOLKMANN

D

z

100

w

# 75

Iii 50

Y

8 25

5 0

z

100

id

m 75

)r 50

Y

3 25

a 0

TIME fMSECf

z: too

Y

to 75

z 50

Y

2

25

a 0

-100 0

100 200

TIME (MSEC)

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 examples s the time of occurrenceof the stimulus n 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 tech-

nique, for example, Riggs et al. (1982b) found

that at a field luminance of 3Oft-L the time-

course 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 sac-

cade. Saccade duration was apptox. 40 msec.

Volkmann et al. (1968) have argued that periph-

eral 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

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Human visual suppression

1407

of light adaptation. If one assumes that sup-

pression 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 characteri stics 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 tem-

poral 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 condi-

tions. Mitrani et al. (1970b) found that the

time-course of suppression is different for stim-

uli 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 sac-

cade 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 suppres-

sion 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 move-

ments (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 sac-

cades 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 ex-

tended the investigation of visual suppression, to

vergence movements. Using full-field luminance

decrements as stimuli in a photopically illumin-

ated 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 DURING

EYEBLINKS

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 other-

wise 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.

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FRANCES 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 magni-

tude 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 primar-

ily 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 ac-

companying 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). Sup-

pression 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 sup-

pression in the brain. Recovery from suppres-

sion 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 tran-

sient retinal stimuli (Matin, 1975). An under-

standing 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 re-

spect 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 addi-

tion 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 ordin-

arily 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

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Human visual suppression

1409

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

Investigations of masking in relation to sac-

cadic 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 fre-

quency 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 mask-

ing 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;

Brooks and Impelman, 1981). The character-

istics 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 momen-

tarily brightened rather than displaced. As an

example of the threshold elevations measured,

Brook and Fuchs (1975) found, under compar-

able 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 sac-

cade, 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 consid-

ered 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 back-

ground contours in many of the above experi-

ments, however, produces a substantial eleva-

tion of threshold for fovea1 stimuli, even though

the contours may lie in a remote retinal location

(Breitmeyer and Valberg, 1979). This effect,

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FRANCES

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 con-

tour (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).

VOLKMANN

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 attri-

butable 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 sup-

pression to nonsaccadic eye movements and to

eyeblinks has complicated the matter consider-

ably. 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 mech-

anisms may mediate the various forms of sup-

pression. 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 pro-

duced 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 station-

ary 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, un-

doubtedly 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 micro-

saccades, slow convergence or divergence move-

ments, 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 pro-

posed 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-

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Human visual suppression

1411

sity are reciprocally related for a given photo-

to the moving or blinking eye stimulus

chemical effect; therefore, decreasing the dur- situations in which these retinal effects are

ation of stimulation decreases the effective

minimized or eliminated. Unfortunately, many

stimulation at the receptor (Blochs law). Thus,

experiments have confounded the delineation

under normal conditions of viewing, a stimulus of extraretinal mechanisms by measuring

may not be noticed during a saccade both

suppression under conditions in which these

because it is smeared and because its effective

mechanisms cannot be separated from retinally

brightness is reduced.

originating mechanisms.

Saccadic suppression, however, is not elimin-

ated 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.

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.

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 process-

ing 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 deter-

mined by acceleration, and the magnitude of

suppression does not vary linearly with acceler-

ation. Further, Richards model would not pre-

dict 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.

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 feed-

back 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 sup-

pression prior to the onset of activity in the

extraocular muscles. Inflow from the extra-

ocular muscles may, however, provide informa-

tion regarding eye position that is used in the

maintenance of visual stability (E. Matin, 1974,

1982; see also Shebilski, 1977).

Extraretinal mechanisms

Retinal mechanisms of suppression are best

investigated by presenting to the fixating eye

stimulus situations in which the effects of condi-

tions 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

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 dia-

grammed in Fig. 2. Here, the oculomotor com-

mand 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

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FRANCES . VOLKMANN

CONSCIOUS

LEVEL

VOLUNTARY IMPULSE

PERCEPTION

t

OCULOMOTOR

EFFERENCE COPY I RESULTANT

COMMAND L

h SIGNAL

UNCONSCIOUS

-

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 oculo-

motor 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 condi-

tions, 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 t

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 posi-

tion is the eyepress. Subjects are asked to mono-

cularly 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 move-

ment, 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 ade-

quately explain the findings that displacement of

a target stimulus that occurs during a saccade is

not perceived. MacKay (1972, 1973) has pro-

posed 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 re-

cently 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 (Bridge-

man, 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 saccade-

contingent compensatory shift produced by an

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Human visual suppression

1413

extraretinal signal in the perceived direction

(or directional local sign) of a stimulus. Imper-

fections 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 percep-

tion 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 hypoth-

esis 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 experi-

ments 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 dur-

ing oculomotor behaviours of quite diverse dur-

ations, 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 momen-

tary interruptions of vision produced by eye-

blinks. To meet these requirements, the human

perceptual system has evolved both afferent and

efferent selective mechanisms, including mech-

anisms 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 enorm-

ously 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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VOLKMANN

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