British Journal of Ophthalmology 1996; 80: 373-377 373

PERSPECTIVE

Physiology of suppression in strabismic amblyopia

Richard Harrad, Frank Sengpiel, Colin Blakemore

It is 100 years since von Graefe first demonstrated a binocular inhibitory process has been found to be present
suppression scotoma in an amblyopic eye.' A review of in some amblyopic subjects'9 and the work of Harrad and
publications on the subject of suppression in strabismus Hess has shown that, in the presence of reduced contrast
reveals that this has not been a very active area of research sensitivity in the amblyopic eye, it can at least partly
and that what literature there is contains many apparent account for suppression in some subjects with small angle
contradictions. strabismus or anisometropic amblyopia,7 15 as well as for
Early workers found strong suppression at the fovea of reduced stereoacuity in these patients.20
the deviating eye in strabismic amblyopia (the point of The loss of low contrast information as a result of
confusion) and also at the diplopic point (the point on the dichoptic masking is similar to the process whereby a pro-
retina of the deviating eye where the image of the target gressive reduction of the contrast of one of a pair of stereo
being fixated by the other eye falls).23 They made no half images leads to a decrease in stereoacuity21 22 and
attempt to describe the fate of images of objects in the rest eventually suppression of the lower contrast half image in
of the visual field of the deviating eye. Subsequent experi- normal subjects.23 Observers with normal stereopsis
mental results have been conflicting: Pratt-Johnson and suppress some of the monocular information contained in
Tillson found the entire visual field of the deviating each stereo half image, a phenomenon called fusional
eye except the temporal crescent was suppressed in all suppression.24 McKee and Harrad25 found that
strabismic subjects except those with monofixation syn- stereoanomalous subjects were able to extract monocular
drome4; Jampolsky reported hemiretinal suppression,5 and information from stereoscopic targets with the dominant
Sireteanu and Fronius described discrete areas of suppres- eye, while this information was not available to the non-
sion surrounded by regions of facilitation and stereopsis in dominant eye. They proposed that suppression in these
patients with monofixation syndrome.6 The area of sup- subjects might simply be the effect of fusional suppression
pression in the amblyopic eye depends on the nature of in the presence of a weakened binocular signal from the
the stimuli used in the experiment2 4 7; patches of grating, non-dominant or amblyopic eye.
different coloured lights,6 and geometrical patterns5 have Jampolsky5 and Schor'6 found that similar targets
all been used by various authors. There has been a ten- tended to be the most effective stimuli for strabismic sup-
dency by some authors to generalise from data collected pression (whereas binocular rivalry suppression in normal
from a few patients with a particular type of amblyopia in observers is produced only by dissimilar images in the two
an attempt to describe the condition in all patients. It is eyes). Since crossed or uncrossed disparities may be selec-
clear from detailed study of individual patients that no one tively affected in some stereoblind subjects,26 27 Schor
simple explanation of suppression in amblyopia is suffi- speculated that stimulation of one class of disparity detec-
cient and that a combination of physiological processes is tor (crossed or uncrossed) might lead to suppression.28 He
at play. found that in a group of subjects with small angle strabis-
mus suppression was stimulated by the presentation of
targets of a fixed disparity and that this disparity depen-
Psychophysical evidence dent suppression was present throughout the central visual
Binocular rivalry occurs in normal humans when field and was not confined to a particular retinal locus.
corresponding points in the two eyes view images that are In a binocular rivalry paradigm clear differences in
so dissimilar that they cannot be fused. The observer the depth of suppression between the different types of
experiences alternating dominance and suppression of amblyopia have been reported14: in anisometropic ambly-
each monocular image.89 The process that underlies opia suppression was weaker than in strabismic amblyopia
binocular rivalry has been proposed as the physiological and in alternate fixators it was strongest of all. Harrad and
basis of suppression in amblyopia.3 10(12 However, there Hess found similar results and proposed that suppression
are a number of objections to this proposition: the charac- was strongest where there was little or no capacity for
teristic alternation of binocular rivalry is not seen in stra- binocular facilitation in the presence of large monocular
bismic suppression; the wavelength dependence of pools of cells'5; a similar hypothesis has been put forward
suppression in binocular rivalry differs from that of by Blake.9 It seems that there is a combination of processes
strabismic suppression'3; suppression in strabismus has operating to bring about suppression; dichoptic mask-
been found to be much stronger than rivalry suppression in ing or disparity dependent suppression are seen in ani-
normal subjects'4 15 and the visual stimuli that lead to sometropia and small angle strabismus and, since normal
binocular rivalry, such as gratings of different orientation physiological processes are utilised, suppression need not
in the two eyes, when presented to amblyopes tend to pro- be very powerful. Where normal binocular interactions are
duce rivalry with alternation rather than suppression.5 16 not possible, in moderate and large angle strabismus, there
Dichoptic masking'7 18 is the physiological process seems to be a powerful form of binocular rivalry suppres-
whereby a stimulus of a given contrast presented to one eye sion.
can prevent the detection of a lower contrast but other- Where in the visual system is rivalry suppression
wise identical stimulus presented to the other eye. This taking place? Lehky and Blake29 have suggested the lateral
374 Harrad, Sengpiel, Blakemore

geniculate nucleus (LGN) or layer 4 of the primary visual A

cortex (V1) as likely sites, since most neurons in both of
these loci are excitable through only one eye. Moreover, 90
they are themselves selective for the orientation of line
stimuli (layer 4 of the cortex, at least in the cat) or receive
feedback input from orientation selective cells (for the
LGN): such selectivity seems to be required to explain the
orientation dependence of binocular rivalry.
On the basis of his own psychophysical findings, Hess30
reached a similar conclusion concerning the site of sup- 1801 Direction
0 (degrees)
pression in amblyopia. He investigated the perceptual
adaptation caused by prolonged exposure to high contrast
gratings31; because of its orientation dependence this
phenomenon is thought to arise from neural effects within
the visual cortex. He found that strabismic amblyopic
subjects do not exhibit orientation dependent threshold
elevation through the amblyopic eye after adaptation with
both eyes open, but such an adaptation effect is seen when 0 20 40
a grating is viewed by the amblyopic eye alone. He con- Spikes/s
cluded that suppression takes place at (or before) the site B
of adaptation, probably in Vl.
Since binocular rivalry may be implicated in strabismic 40
suppression we undertook a neurophysiological investiga-
tion, looking for evidence of inhibitory binocular inter- U'
actions in the LGN and VI that might provide the neural 30 _
basis of binocular rivalry suppression. a

a)
20 H
Neurophysiology
Varela and Singer32 had already reported that, when stim- 0.CA
U)
ulated with a grating in their dominant eye, the responses
of some cells in the LGN of the anaesthetised cats
were suppressed if a grating of orthogonal orienta-
tion was presented to the other 'silent' eye, but were
unaffected by a grating of the same orientation. However, 0 30 60 90
neither we33 nor others34 have been able to confirm these Interocular orientation difference (degrees)
findings. Figure 1 Orientation dependence of binocular interaction in a layer 6
Although several workers have carried out single cell complex cell recordedfrom a normal cat. (A) Polar plots of
recordings from cat primary visual cortex during the pre- orientation/direction tuning, showing mean responses (+ 1 SEM) during
sentation of non-fusible stimuli,35-37 they did not find monocular stimulation through the dominant eye (solid lines) and the
non-dominant eye (broken line) alone, as a function of the direction of
powerful interocular suppressive effects. But recently we drift of sinusoidally modulated gratings (spatialfrequency=0-56 cpd
have found conditions under which the majority of cortical [cycles per degree]; dnift frequency =4 d/s; contrast= 0.8). The dotted circle
neurons (outside layer 4) exhibit strong interocular in the centre indicates mean spontaneous activity. (B) Results of binocular
inhibitory interactions which might account for binocular interaction protocol. The dominant (contralateral) eye was continuously
stimulated with a 'conditioning' grating of optimal orientation (direction
rivalry.33 38 We studied the responses of 52 neurons in VI of drift=247-5°; spatial frequency =056 cpd; temporal frequency=4 cds;
of five normal adult cats to dichoptic grating stimuli and contrast= 0 4) while gratings of the same spatial and temporalfrequency
found that, while binocular facilitation was observed with (contrast= 0-8) appeared intermittently in the ipsilateral eye atfive
different orientations, over a 90° range, clockwise from that of the
gratings of similar orientation, the response to a grating of 'conditioning' stimulus. The abscissa indicates the difference in orientation
optimal orientation presented to one eye was suppressed, between the stimuli shown to the two eyes. (*) Plots the mean response
for more than half of the 45 binocular cells (25 cells, 56%), (± 1 SEM) during binocular stimulation with a particular combination of
gratings, while (0) plotted at the same position on the abscissa shows
by a grating of very different orientation shown to the other activity averaged over the immediately preceding periods of monocular
eye (Fig 1). Facilitation with iso-oriented gratings stimulation. The open arrow indicates the mean level of spontaneous
amounted to 120-7% ±10O4% (mean ±SEM) of mono- discharge. For this cell, binocular interaction changed from 285%
facilitation above monocular response for iso-oriented gratings to 60%
cular, dominant eye responses, while orthogonally oriented inhibition for orthogonal gratings.
gratings reduced monocular responses by 37.7% /±38%
(mean ±SEM). In most cells, these effects are evident only
if the suppressive stimulus is introduced while the cell is until recently concentrated on a search for monocular
already responding through its dominant eye, not when the response anomalies of cells at various stages in the primary
onset of stimulation in the two eyes is simultaneous.38 This visual pathway that might account for the severe acuity
correlates with the finding that simultaneously presented deficits that are often observed in strabismic humans as
conflicting stimuli are temporarily fused by humans before well as in animals with surgically induced squint. However,
the onset of rivalry."1 This temporal non-linearity explains unless surgical intervention was so comprehensive as to
why other workers, who used stimuli of simultaneous severely compromise ocular motility, function and,
onset, did not see distinct suppressive interactions. perhaps, even the blood supply of the operated eye,40 41 no
A recent preliminary report39 suggests that in awake differences were found between normal and strabismic
monkeys a proportion of neurons in Vl similarly show animals in the properties of neurons in the visual pathway
suppression of neuronal activity that is correlated with per- peripheral to the cortex.42
ceptual suppression of vision in one eye during episodes of For cells in the primary visual cortex of strabismic
binocular rivalry. cats4348 and monkeys,49-51 the most striking and also
Neurophysiological research into strabismic amblyopia the only generally accepted consequence of squint is the
Physiology ofsuppression in strabismic amblyopia 375

breakdown of conventional binocularity - that is, most A

neurons can only be driven through the left or the right
eye, seldom through both. In esotropic monkeys, a preva- 90
lence of cells dominated by the non-deviated eye has been
reported,50 though most studies of strabismic monkeys and
cats have reported equal proportions of cells dominated by
each eye.43A48 51 A range of further anomalies has been
described, none of which is without controversy or severe
enough to account for the phenomenon of strabismic Direction
amblyopia.5253 In animals that have been deprived of 0 (degrees)
vision in one eye, even for a very short time early in life,
cells that are excitable through the previously deprived eye
have a lower 'neural acuity' (the highest spatial frequency
that evokes a detectable response) than do cells driven
through the normal eye.54 This reduction in neural acuity
clearly correlates with reduced behavioural acuity in an
amblyopic eye and it might therefore be expected that cells
in the visual cortex of esotropic animals would be similarly
affected. In fact, Crewther and Crewther47 found only a Spikes/s
small difference in the average acuity of cells through the B
two eyes, while the cells with the highest resolution
through the squinting eye (which might be expected to 30
determine behavioural acuity) were hardly different from
those driven through the normal eye. Indeed, most authors 'I,

have reported no difference at all in the spatial perfor-

mance of neurons dominated by the fixing and the deviat- a) 20 H
ing eye in squinting cats and monkeys.55-57 However, it aI)
must be said that amblyopia verified by behavioural tests 0.
occurs in only a minority of esotropic (and probably even
fewer exotropic) cats.57 But in most neurophysiological (0
studies of the effects of strabismus, visual acuity has not
et n1 10 _ I ---4
been behaviourally tested and therefore it is not known
whether the animals actually had amblyopia or not.
Only very few studies have investigated interocular sup- n
u
pression and its part in binocular integration as a possible 0 30 60 90
basis for strabismic amblyopia. We addressed the possibility Interocular orientation difference (degrees)
that mechanisms underlying normal binocular rivalry might Figure 2 Orientation independence of binocular interaction in a layer 5
be the basis of suppression in strabismic amblyopia.48 58 complex ceUl recordedfrom an exotropic cat (angle of squint, 30°).
Exotropia or esotropia were induced in five kittens by teno- (A) Polar plot of orientation/direction tuning, as in Figure IA, showing
mean responses (+ 1 SEM) during monocular stimulation with drifting
tomy of the medial or lateral rectus, respectively, just after gratings (spatialfrequency=0-56 cpd; driftfrequency= 4 d/s;
eye opening. We recorded responses from 85 neurons in Vl contrast=0-7) through the deviating eye, which was dominant for this cell.
of the adult cats, to pairs of drifting gratings covering 10 There was no significant response through the other (non-deviating) eye.
The spontaneous activity of this cell was very low (< 1 spikels).
degrees of visual angle that were presented to corresponding (B) Results of binocular interaction protocol, as in Figure lB. The
positions in the visual fields of the two eyes (for further deviating (dominant) eye was continuously stimulated with a
details of stimulation procedures, see captions to Figs 1 and 'conditioning' grating ofoptimal direction ofdrift (0"; spatial
2). Receptive fields of all cells studied in these animals were frequency=0-56 cpd, temporalfrequency=4 cs; contrast=0 18), while
gratings appeared intermittently in the normal ('silent') eye at five
within 4 degrees of the area centralis. Only seven cells (90/O) different orientations (same spatial and temporalfrequency;
showed facilitatory binocular interactions close to normal. contrast= 0-7), clockwise from that of the 'conditioning' stimulus. The
For 47 cells (55% of the total), presentation of a grating of abscissa indicates the difference in orientation between the stimuli shown to
the two eyes. (a) Plots the mean response (± 1 SEM) during binocular
any orientation caused significant suppression of the stimulation with a particular combination ofgratings, while (0) plotted at
response being elicited through the cell's dominant eye (Fig the same position on the abscissa shows activity averaged over the
2), even though, when stimulated through the non-domi- immediately preceding periods of monocular stimulation. The open arrow
indicates the very low level of spontaneous discharge. For this cell,
nant eye alone, most cells were 'silent'. The remaining cells interocular suppression varied between 65 and 90% of monocular response
did not display significant binocular interactions. For the levels.
whole population of neurons, suppression with iso-oriented
dichoptic gratings amounted to 29-5% ±4-8% (mean frequencies that would trigger an excitatory monocular
+SEM) of monocular, dominant eye responses; orthogo- response). It should be noted, that even for some 'binocu-
nally orientated gratings suppressed monocular responses lar' neurons suppression of responses elicited through one
by 36-4% ±3 0% (mean ±SEM). In contrast, in five normal eye was seen when an additional grating was presented to
animals, 42 out of 52 neurons (81%) showed significant the other eye; a similar finding has been reported by
binocular facilitation and only four (8%) showed orientation Crewther and Crewther.59
independent interocular suppression.33 Since, in all animals tested, most cells had lost conven-
Interocular suppression in the strabismic animals was tional (that is, excitatory) input from one eye or the other,
characterised by a relative independence of stimulus the 'monocular' cells (69% of the total) behaved in a way
variables,48 in particular a virtual absence of orientation that would be expected on the basis of the results from nor-
selectivity. Suppression with iso-oriented dichoptic mal animals and in the absence of binocular facilitatory
gratings was also independent of the relative disparity of interactions for stimuli of matched orientation. The
the two gratings (and therefore not related to perceived response properties of single cells in Vl of normal and stra-
depth), and it could be elicited by gratings of a wide range bismic animals were similar in many respects; for dichoptic
of spatial frequencies (often wider than the range of spatial gratings of orthogonal orientations (where facilitation is
376 Harrad, Sengpiel, Blakemore

absent in normal as well as in strabismic animals), average disparity dependent suppression, and rivalry-like inter-
suppression was of very similar strength (35-40%) in both ocular suppression. The first appears to prevail in aniso-
normal and strabismic cats (see above). Moreover, neu- metropic amblyopia,7 the latter three in strabismic
ronal interocular suppression in both normal and strabis- amblyopia. That these processes are not identical psycho-
mic animals was characterised by disparity independence, physically or physiologically with those found in normal
broad spatial frequency tuning, dependence on the subjects can be accounted for by minor modifications in
sequence of stimulus presentation, and divisive response the underlying neural circuitry occurring during visual
gain reduction.3848 Thus normal binocular interaction development.
appears to be the sum of highly stimulus specific facilita-
tion and rather non-selective suppression60; strabismus This work was in part supported by the Medical Research Council and the
Oxford McDonnell-Pew Centre for Cognitive Neuroscience. FS holds a fellow-
seems to reduce or eliminate the facilitatory interactions, ship at Magdalen College, Oxford.
but leaves the non-selective suppression intact. RICHARD HARRAD
Bristol Eye Hospital,
Lower Maudlin Street,
A neural model of suppression Bristol BS1 2LX
We speculate that strabismic suppression in moderate and FRANK SENGPIEL
COLIN BLAKEMORE
large angle strabismus is based on inhibitory interactions University Laboratory of Physiology,
between neighbouring ocular dominance columns with Parks Road, Oxford OXI 3PT
input from all orientations, combined with the loss of dis-
parity selective interactions for matched stimuli. In small
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