J. Physiol. (1975), 247, pp. 551-578 With 12 text-ftigure8 Printed in Great Britain

551

THE CONTROL OF RETINAL GANGLION CELL DISCHARGE BY RECEPTIVE FIELD SURROUNDS

BY CHRISTINA ENROTH-CUGELL* AND P. LENNIEt From the Departments of Biological Sciences and Electrical Engineering, Northwestern University, Evanston, Illinois 60201, U.S.A.

(Received 12 July 1974) SUMMARY

1. This paper describes the behaviour of the receptive field surround, and how surround signals combine with those from the centre to generate the discharge of the retinal ganglion cells of the cat. 2. A small test spot is flashed upon the middle of the receptive field of an on-centre X-cell, alone, or together with a concentric annulus of fixed luminance. The reduction in discharge brought about by the annulus is independent of spot luminance. From this it is inferred that centre and surround signals combine additively. 3. Knowing that the combination of signals is additive, the surround signal can be estimated by comparing the ganglion cell's response to diffuse illumination of its receptive field with that to an equiluminous spot which optimally stimulates the centre while encroaching minimally upon the periphery. 4. Application of this technique to X-cells shows that although the surround seems to have a threshold, it is at its most sensitive in the darkadapted eye, and typically is only 0S3-O05 log units less sensitive than the centre. 5. Centre and surround sensitivities are decreased from their darkadapted levels by increasing background illumination, but the decline of surround sensitivity is initially less rapid than that of the centre. Thus with increasing light-adaptation the surround becomes relatively more sensitive. In the light-adapted eye centre and surround are about equally sensitive to diffuse illumination. 6. Although, in the dark-adapted eye, illumination of the receptive field periphery of an on-centre unit depresses firing, removal of that illumination produces no off-discharge. Off-discharges appear only when background * Mailing address: Biomedical Engineering Center, Technological Institute, Northwestern University, Evanston, Illinois 60201. t Present address: The Psychological Laboratory, Cambridge, England.

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552 CHRISTINA ENROTH-CUGELL AND P. LENNIE illumination exceeds about 104 quanta (507)/deg2 sec. This confirms Barlow & Levick (1969b). 7. In the dark-adapted eye surround latency is longer than that of the centre. With increasing background illumination the latency difference is reduced. 8. For X-cells, the rate of the maintained discharge depends to some extent on the balance of centre-surround antagonism. But this antagonism is not the major factor accounting for the relative constancy of mean rate at high background luminances, for the rate then can be almost independent of the size of a steady spot. 9. The mean rate of discharge of Y-cells seems to depend even less upon the balance of centre-surround antagonism. 10. Y-cell surrounds could not properly be isolated with the optimal spot-diffuse illumination technique, so detailed measurements of their behaviour were not made. However, the dark-adapted surrounds appear to be as sensitive as those of X-cells. INTRODUCTION

Most receptive fields of ganglion cells in the cat retina are concentrically organized: in the central, more sensitive region, light onset is in some cells excitatory, in others inhibitory, and this region is encircled and to some extent overlapped by an antagonistic surround (Kuffler, 1953). The surround's importance in controlling discharge is qualitatively understood: it produces spatial selectivity, for it will be little involved in the response to small, centred stimuli, but is likely to antagonize the centre when the stimulus is diffuse (Ratliff, 1965). This observation has made it possible for the form of some psychophysical threshold functions to be explained in terms of centre-surround interaction in retinal units. But little is known about the quantitative aspects of surround behaviour or about centre-surround interaction, and that is one reason why it is hard to evaluate these explanations. This paper describes our observations of the behaviour of the surround mechanism and how it interacts with the centre in generating the discharge of a retinal ganglion cell. We confirm earlier observations (e.g. Enroth-Cugell & Pinto, 1972) that transient signals from centre and surround probably combine additively. We find also that except in the fully dark-adapted eye the sensitivities of centre and surround are well balanced throughout the scotopic range, that at much lower adaptation levels than are required for the production of an off-discharge the surround can antagonize the centre, and that in the darkadapted eye the surround probably cannot influence the discharge of a

SURROUND CONTROL OF DISCHARGE

553 unit without the centre being stimulated. Other observations on the contribution of the surround to the maintained discharge show that it is sometimes important for X- but apparently not for Y-cells (EnrothCugell & Robson, 1966) and that for neither type of unit does surround behaviour account fully for the constancy or decline of the maintained discharge at high background luminances. METHODS

Our preparation and apparatus have been described before (Enroth-Cugell & Pinto, 1972; Enroth-Cugell & Shapley, 1973). Impulses were recorded with lacquered tungsten micro-electrodes from single optic tract fibres in cats lightly anaesthetized with urethane (10-20 mg/kg. hr) or a mixture of 70% nitrous oxide, 28-5% oxygen and 1-5% carbon dioxide; normally gas was used, for unlike urethane it did not depress blood pressure. However, in some cats, when using gas, we encountered units which were insensitive and had a fast rhythmic maintained discharge. This behaviour may be similar to that seen occasionally by Bishop & Rodieck (1965) in cats anaesthetized with nitrous oxide; the rhythmicity sometimes could be abolished, and sensitivity improved, by transferring to urethane. Animals were paralysed with gallamine triethiodide (Flaxedil) or, in the later experiments, with a mixture of Flaxedil and diallyl-nortoxiferine-dichloride. In these later experiments too the cervical sympathetic trunk was cut bilaterally. Pupils were dilated with atropine, and contact lenses of appropriate power, with 15 mm2 artificial pupils, focused stimuli upon the retina. Two fluorescent sources provided a test flash of variable size up to 11°, which could be superimposed when necessary upon a steady background 120 in diameter. In all experiments using transient stimuli the test flash was blue-green (Ilford 623) and the background red (Ilford 205). This helped keep cone sensitivity to the test flash below that of rods. All illuminations are expressed in equivalent quanta (507 nm)/deg2 sec at the retina and are calculated by assuming (from Aguilar & Stiles, 1954) that 1 scotopic td = 4-46 x 105 quanta (507 nm)/deg2 sec at the cornea. Three-quarters of the incident quanta are assumed to reach the retina. When records were made of discharges, action potentialswere convertedto standard pulses which, after smoothing, were averaged in a digital memory oscilloscope (Enhenacetron). Usually the discharges following thirty stimulus presentations were averaged to produce a pulse-density tracing, which is equivalent to a smoothed poststimulus-time histogram. RESULTS

Throughout this paper and the next, the terms 'middle' and 'periphery' refer respectively to the corresponding regions of the receptive field. We have reserved the terms 'centre' and 'surround' to denote respectively the mechanism causing the response characteristic of the middle and that causing the response characteristic of the periphery. The distinction is made because selective stimulation of a region rarely guarantees that only one antagonistic response mechanism will be excited. We studied only oncentre units, and most of these were X-cells (Enroth-Cugell & Robson, 1966; Fukada, 1971; Cleland, Dubin & Levick, 1971). 21-2

554 CHRISTINA ENROTH-CUGELL AND P. LENNIE A new method is introduced which makes easier the isolation of the surround; we begin by describing the technique and some limitations to its usefulness. Then we apply it to estimate, for various conditions of stimulation, the contribution of the surround to the discharge of a ganglion cell. Tendency to increase

Light on

Lgto

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Centre contribution

Surround contribution

Tendency to decrease discharge

_

Time

Fig. 1. Hypothetical contributions of centre and surround to the discharge of the light-adapted on-centre cell. At onset of illumination, the centre tends to cause an increase in discharge, at stimulus offset there is a tendency for the discharge to be depressed below its original level (interrupted line). The surround acts oppositely, tending to depress discharge at stimulus onset and to increase it at offset. The resulting discharge of the ganglion cell will reflect the balance of centre and surround contributions, and that depends upon stimulus configuration and intensity.

Isolation of surround General. Surrounds express themselves in two ways: (a) at stimulus onset in off-centre cells and at offset in on-centre cells surround antagonism tends to increase the cell's discharge; (b) at stimulus onset in on-centre cells and at offset in off-centre cells the surround tends to decrease the discharge. Fig. 1 shows diagrammatically the probable contributions of centre and surround to the response of ganglion cells in the light-adapted eye. It is derived from a number of studies which attempted to separate the mechanisms (e.g. Kuffler, 1953; Rodieck & Stone, 1965a). If this scheme reasonably represents ganglion cell behaviour it is easy to see that the centre tends to increase discharge when the surround tends to decrease it, and vice versa. So it is important, if we want accurately to estimate the surround's contribution to response, that we eliminate, or know exactly, the contribution of the centre. Frequently (e.g. Barlow, Fitzhugh & Kuffler, 1957) the surround is stimulated by the withdrawal

555 SURROUND CONTROL OF DISCHARGE or application of an annulus concentric with the receptive field, and surround sensitivity measured by the threshold for an off-discharge (an overshoot at stimulus offset) in on-centre units or an on-discharge in offcentre ones. But there are difficulties with this approach, both practical and theoretical. First, through scattered light, an annulus often will influence the sensitive centre even more than it will the surround, and it is most difficult to produce an unambiguous surround response. This can be

seen in Enroth-Cugell & Pinto (1972, Fig. 2). Moreover, an annulus of inner diameter large enough to minimize scatter on to the centre will miss also much of the surround. Second, measuring the surround's sensitivity in on-centre units by the threshold for an off-discharge ignores its complementary, and possibly equally important, role as a suppressor of discharge. These considerations led us to approach the problem differently. Optimum spot-diffuse illumination technique. If we could choose a spot which optimally stimulated the centre, it should be possible, by measuring the difference between discharge to this 'optimal' spot and to diffuse illumination, to observe how the surround contributes to the latter response. The optimal spot must be just the right size; were it too small, enlargement of it to cover the whole receptive field would cast additional light upon the centre; were it too large, the surround already might be substantially stimulated. Either case would result in an underestimate of surround involvement in the response to diffuse illumination. However, with a carefully chosen spot, the technique seems to work well, and we have been able to use it to describe the behaviour of the surrounds of X-cells. For each unit the optimal spot was found in the following way. After the eye had become dark-adapted, a small spot centred upon the receptive field was presented for 1 sec every 2-5 sec, and its luminance adjusted for threshold (in on-centre units a just audible increase in firing about 50 % of the time). As the spot was enlarged, threshold became lower, for ganglion cells sum the effects of light falling on the middle of the receptive field (Barlow et al. 1957; Wiesel, 1960). Spot size was increased until the smallest was found which gave the lowest threshold; it optimally stimulated the centre. This 'optimum' spot was larger than the conventional index of centre size, At (Cleland & Enroth-Cugell, 1968) and usually intersected the sensitivity profile at a point where sensitivity had declined between 0 7 and 1-7 log units from its maximum (cf. next paper). The change in discharge brought about by enlarging the optimum spot to cover the whole receptive field will show how the surround modifies the response of the centre, but we cannot infer from this change the size of the surround signal unless we know whether the action of the surround is divisive or subtractive.

556 CHRISTINA ENROTH-CUGELL AND P. LENNIE Linearity of centre-surround interaction. A number of observations may be explained by additive combination of transient signals from centre and surround. Rodieck (1965) was able satisfactorily to account for many of the experimental findings of Rodieck & Stone (1965a, b) by assuming linearity of interaction. Maffei & Cervetto (1968) and Enroth-Cugell & Pinto (1972) attempted directly to measure how the ganglion cell combines transient signals from centre and surround, and their results suggested that the cell responds to the difference between centre and surround signals. But no experiment has been able solidly to exclude the possibility of the interaction being divisive, because then the steady components of centre and surround signals must also be considered in the calculations, and these steady components are unknown. Suitable values for the steady components may cause a divisive surround to act indistinguishably from a subtractive one. This problem is discussed thoroughly in Enroth-Cugell & Pinto (1972). In the following experiment we tried to pin down more securely the manner in which centre and surround interact. The receptive field was illuminated by a diffuse steady background bright enough to bring the maintained discharge up to 30-40 impulses/sec. A small spot was flashed upon the centre and its luminance adjusted to give a response which was just detectable by listening. Then the spot was presented again, this time with an annulus which when flashed alone could bring about a substantial depression of maintained discharge. If an annulus stimulates only the surround, and surround signals subtract from those of the centre, the reduction of discharge brought about by adding the annulus should not depend on spot luminance. Fig. 2 shows what happened when the small spot alone was presented at different luminances (upper curve), and when at these luminances it was accompanied by an annulus of fixed luminance (lower curve). The addition of the annulus produced a constant difference in discharge (varying only between 49 and 53 impulses/sec as spot luminance was varied by a log unit) and so the upper and lower sets of points are fitted by straight lines of the same slope. Division could not uniformly have displaced the upper curve unless the centre signal divided by that from the surround had an enormous steady component to which the spot contributed negligibly. Barlow & Levick (1969a) showed that, for small stimuli applied to the centre, the increase in discharge was proportional to stimulus luminance over a considerable range. Until the increase in discharge rate exceeded about 60 impulses/sec this was true for the unit of Fig. 2, and only within this range can one confidently assert additive combination. Beyond it, the response becomes approximately proportional to the logarithm of

SURROUND CONTROL OF DISCHARGE 557 stimulus luminance, and then one cannot distinguish between a logarithmic transformation which occurs in both centre and surround signals before they combine linearly, and logarithmic transformation of the result of surround division of centre signals. When taken with the evidence reviewed at the beginning of this section, our experiment seems firmly to support the view that centre and surround signals combine additively, at least for X-cells. Later in the paper (p. 564) we have to qualify this conclusion, for we find some evidence for a threshold non-linearity in the behaviour of the fully dark-adapted surround. The experiment of Fig. 2 has not been carried out on Y-cells, because of the difficulty, peculiar to these units, of isolating centre and surround with spots and annuli respectively (see Discussion). 120-

90

.

60

30 Le_

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5 X106 1 3 illumination (quanta/deg2 sec)

Fig. 2. Centre-surround interaction. Upper curve: responses of a cell to the presentation of a 0.180 spot at successively increasing illuminations. Each point plots the number of impulses discharged in a 1 sec period which begins 60 msec after onset of the 1 sec stimulus. The mean rate of the maintained discharge (background 6 5 x 104 quanta (507) deg2 sec) is marked by the open arrow. Pulse-density tracings (which show the mean firing rate of the cell at any instant during stimulus presentation) of responses to the dimmest and the brightest spots are drawn beside the curve; the horizontal bar under each tracing marks zero impulses/sec, and the vertical bar represents 50 impulses/sec. Lower curve: discharge rate to the same spot at the same illuminations, but this time presented with a I5-1 1 annulus at 7-0 x 104 quanta (507)/deg2 see. The point for zero spot illumination (open circle) plots the discharge rate during presentation of the annulus alone. Note how the addition of the annulus uniformly lowered the curve, without change of slope. This implies additive combination of signals from centre and surround. X-cell, 33/2.

558

CHRISTINA ENROTH-CUGELL AND P. LENNIE

Time-varying responses Relative sensitivity of surround and centre. Barlow et al. (1957) described results which suggested that in the dark-adapted eye the surround 'drops out' leaving only the centre. This finding has been basic to the interpretation of many psychophysical and physiological experiments, and to document it further we made the observations shown in Fig. 3. First, a check on dark-adapted sensitivity was made by calculating, from the averaged response to a small, weak stimulus presented to the centre of the receptive field, the number of quantal absorptions required to elicit an extra impulse from the ganglion cell. The quantum/spike ratios usually were close to 10, but could range from 3 to 20 in healthy units (cf. Barlow, Levick & Yoon, 1971). Then the optimum-sized spot was found; its luminance was adjusted until the response could just be heard, and responses to 30 representations of this threshold stimulus were averaged to produce a pulse-density tracing like that at the top, left of Fig. 3a. After this, the test spot was expanded to 110 ('diffuse illumination') and responses to a further 30 presentations of the stimulus at that luminance were averaged (top, centre, Fig. 3a). For the typical X-cell we found at absolute threshold that expanding the test spot from covering just the centre to covering the whole receptive field changed the cell's response little or not at all. This can be seen in the right-hand column of Fig. 3a, where the response to an optimal stimulus has been subtracted (in the averaging computer) from the response to diffuse illumination. Just above absolute threshold one starts to see a change. All 27 units studied showed a smaller discharge to diffuse illumination between 0-2 and 0 4 log units above threshold for the spot, the difference becoming more pronounced with stronger stimuli (Fig. 3a, second and third rows). Presumably this is the work of the surround. These results show that, in the dark-adapted eye, surrounds of X-cells are only a little less sensitive to diffuse illumination than are centres (although of course, overall, the surround's sensitivity per unit area is vastly poorer, for light is collected over a much larger region). We repeated the experiment at different levels of background illumination and found as did Barlow et al. (1957) that at the higher levels surround antagonism was increased, for even threshold responses to the optimum spot (Fig. 3 b top) were diminished by spot enlargement. The relation between centre and surround sensitivity to uniform illumination can be estimated more accurately than from Fig. 3 by plotting stimulus-response curves for the two mechanisms. This was done for 6 units and an example is shown in Fig. 4. Here is plotted, for two different states of adaptation, the number of extra spikes elicited by the optimum spot

SURROUND CONTROL OF DISCHARGE 559 as a function of incremental luminance. For the surround a similar relation has been derived, but what is shown is the decrease in discharge brought about by expanding the optimum spot to cover the whole receptive field. In the dark-adapted eye (Fig. 4a) there is a range over which response is proportional to stimulus luminance. This is the same for centre and surround, which suggests that the non-linearity arises before centre and surround signals enter their independent pathways. The surround of this unit also had what appeared to be a threshold; its stimulus-response curve ()

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Fig. 3. a, averaged pulse-density tracings of a dark-adapted ganglion cell's response to 30 stimulus presentations. Top row, left: threshold response to the optimum stimulus (diam. 2.5°) centred upon the receptive field. Centre: response to a spot of the same luminance, but this time of diameter 110. In the right-hand column the response to the small spot has been subtracted (by the averaging computer) from that to the large one. Plainly, expanding the spot from 2'5 to 11° has had no effect. The second and third rows show responses to brighter stimuli (respectively 0 4 and 0-8 log units above threshold). Enlargement of the spot from 2-5 to 11° now clearly diminishes the response. b, same as a except stimuli appear against a bright background (1 0 x 106 quanta (507)/deg2 sec), 120 in diameter. Now even at threshold for the 2.50 spot (top row) there is some effect of spot enlargement. In the second and third rows, stimuli were respectively 0 4 and 07 log units brighter. Comparison of these responses with the corresponding dark-adapted ones shows a relatively increased suppressive effect of the surround. Note the development, with higher stimulus luminances, of a transient overshoot ('off-discharge') in the surround response (right column, centre and bottom). X-cell, 27/1.

did not intercept the abscissa at zero luminance. Some units did have zero intercepts, so the peculiarity here might have been the result of errors in measuring small changes in discharge. However, later (p. 564) we describe more evidence for a threshold, and we believe that for the unit of Fig. 4

CHRISTINA ENROTH-CUGELL AND P. LENNIE 560 it is real. The relationship between centre and surround sensitivities can be simply characterized by taking the ratio of the slopes of the linear parts of the stimulus response curves. For this unit the ratio was 3*0, indicating that the surround was about 0.5 log units less sensitive to diffuse illumination. In other units the ratio of slopes varied between 1P9 and 3 0. 90

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1 0 2x105 Stimulus illumination (quanta/deg2 sec) Fig. 4. Stimulus-response functions for centre and surround. a, dark-adapted eye. Filled circles plot the extra impulses brought about by a 1 sec presentation of the optimum spot (diam. 2.50), open circles the difference between the response to this spot and to diffuse illumination, i.e., the number of impulses removed by expanding the spot. The two curves therefore represent respectively centre and surround responses. b, light-adapted eye (background 1.0 x 106 quanta (507)/deg2 sec). Stimulus-response functions for centre and surround, derived as in a. Note the changed scale of the abscissa. X-cell 27/1.

In the light-adapted eye (Fig. 4b) the situation is different: both centre and surround are about equally sensitive to diffuse illumination, and their stimulus-response curves follow the same course. We were interested to know over what range of backgrounds the change in relative sensitivities occurred; this was examined in another experiment

561 SURROUND CONTROL OF DISCHARGE which attempted to follow the change in antagonism as background luminance was increased. As before, an optimal spot was chosen and its luminance adjusted to evoke a peak discharge of about 50 impulses/sec. (about twice threshold by listening). In the dark-adapted eye this response was substantially reduced upon spot enlargement, and the surround's contribution could be derived by subtraction in the usual way. The experiment was repeated at successively greater background luminances, with spot luminance being adjusted each time to elicit the criterion peak discharge before the spot was enlarged to cover the receptive field. Since for small responses both centre and surround respond linearly with stimulus luminance (Fig. 4), we can derive from these results, directly for the centre, and by subtraction for the surround, increment sensitivity curves for both mechanisms. In computing the values plotted in Fig. 5 we took as 'threshold' the incremental stimulus luminance required by each mechanism to produce a change in discharge of 10 impulses/sec. The curves show, for both mechanisms that, following an initial region where it is independent of background illumination, sensitivity becomes approximately proportional to background luminance (Weber's law). But the most interesting result is that the centre and surround enter the Weber region at different levels of background illumination. The surround loses its darkadapted sensitivity less rapidly, and because of this its sensitivity improves relative to that of the centre. Once surround sensitivity has passed through the transition zone and it too is following Weber's law, the ratio of centre to surround sensitivity remains constant, and this results in a constant difference between responses to the optimum spot and to diffuse illumination. The two graphs in Fig. 5 show that in the dark-adapted eye the relation between centre and surround sensitivity varies from unit to unit. Many units behave as shown in the upper graph, with the surround only a little less sensitive than the centre; this situation seems to be even more common in off-centre units (H. B. Barlow & W. R. Levick, in preparation). But in some units the surround is relatively less sensitive (Fig. 5, lower) and may not discernibly alter discharge until stimulus luminance is well above the threshold level for the optimal spot. Off-discharges and the time course of surround response. The appearance of an off-discharge has been a common indicator of surround activity (Barlow et al. 1957; Cleland, Levick & Sanderson, 1973), and because our results suggested a surround more sensitive than had previously been supposed, we compared this measure with the one used in our experiments. Fig. 6 shows, for a succession of background luminances, pulse-density tracings of centre and surround responses obtained in. the usual way. Stimulus luminances were chosen so that on all backgrounds the optimum

562 CHRISTINA ENROTH-CUGELL AND P. LENNIE spot elicited the same moderate peak discharge (for X-cells the size of the optimal spot changes negligibly with adaptation level, so all observations were made using the same-sized spot). In the dark-adapted eye, stimulation of the centre leads to a sustained discharge (left) and in diffuse illumination the surround produces sustained antagonism (right). At light Surround / Centre ' 104 0)~~~~~~~~~01 S 103

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Fig. 5. Increment sensitivity curves for centre and surround, for two X-cells. Filled circles plot the illumination of the optimum spot calculated to evoke 10 extra impulses during a 1 see presentation, and therefore show the change in centre sensitivity. The corresponding relation for the surround (open circles) has been derived by plotting the illumination which would have been needed to reduce the response to the optimum spot by 10 impulses. Most of the change in relative sensitivity of centre and surround has occurred by the time threshold to the optimum spot is 1 log unit higher than its dark. adapted level. X-cells 27/1, 34/3. Optimum spot sizes respectively, 2.50, 2.50.

offset the unit's discharge rate returns rapidly to its resting level, with neither the centre nor the surround having a tendency to overshoot. As background luminance is raised, the response patterns change: stimulation of the centre leads to a more transient discharge, with a complementary

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563 SURROUND CONTROL OF DISCHARGE dip in firing at light offset. This change in discharge pattern, which is seen in all units, probably is linked to the change in sensitivity brought about by light adaptation, for it appears just as sensitivity is reduced from its Centre

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Fig. 6. Development of off-discharges. As background illumination is increased (top to bottom) there develops a progressive change in the time courses of centre and surround responses. Initially, both are sustained, but they become less so with increasing light-adaptation, and overshoots develop at both light onset and offset. The surround's overshoot at offset (the 'off-discharge'), which here is derived by subtraction, appears first on the second brightest background, and is pronounced on the highest. Notice how well matched are centre and surround responses on the higher backgrounds. Stimulus illumination, from top to bottom: 1-8 x 103; 4-4 x 103; 2-5 x 104; 8-0 x 104; 1-0 x 106 quanta (507)/deg2 sec. X-cell, 27/1, optimum spot diameter, 2.50.

dark-adapted value and begins to follow Weber's law (Yoon, 1972; EnrothCugell & Shapley, 1973). With increasing background illumination, surround responses inferred by subtraction also become less sustained, and at light offset there develops a transient overshoot (lower right of

CHRISTINA ENROTH-CUGELL AND P. LENNIE 564 Fig. 6). Barlow & Levick (1969b) found, using an annulus, that this offdischarge first appeared on backgrounds of about 10-2cd. M-2 (3 x 104 quanta (507 nm)/deg2 sec, with their artificial pupil) and our results derived by subtraction agree with theirs. The off-discharge becomes more pronounced with increasing light-adaptation, as does the brief dip in discharge which follows offset of the optimum stimulus. The response of the light-adapted surround thus mirrors closely that of the centre, with the result that the ganglion cell responds poorly to diffuse illumination: a weak transient at onset is followed by an enfeebled discharge at offset (Fig. 3b, bottom centre). Different centre and surround latencies largely account for the transients (see p. 566). Here we wish to emphasize the discrepancy between estimates of surround sensitivity based on the appearance of off-discharges, and those based upon the suppression of discharge which accompanies illumination of the periphery. Often we have found that a perceptible off-discharge appears in the pulse-density tracings only when the background has raised threshold for 'on' suppression to between 10 and 30 times its level in the dark-adapted eye. Surround sensitivity and illumination of the receptive field middle. Perhaps when the centre provides excitatory signals the surround more easily shows itself. That could have contributed to our low surround thresholds, and it has been postulated (Krilger & Fischer, 1973) in attempts to account for the result that an off-discharge is most easily seen when the middle is steadily illuminated (Barlow, Hill & Levick, 1964; Bishop & Rodieck, 1965; Enroth-Cugell & Pinto, 1972). The observations of Fig. 7a tend to support this view. To the darkadapted eye we presented an annulus of inner diameter 30 and outer diameter 4.5°. This excited the centre more than it did the surround, so produced a small increase in discharge (top). Then the outer diameter was increased to 11°, and at the same luminance the annulus was presented again. The discharge was abolished, so we know that the 4.5110 annulus and the 34A5° one exercise equal and opposite effects upon the ganglion cell. But when the 4.5-11 annulus was presented alone (bottom) there was a barely discernible drop in dark-discharge. These observations suggest that the centre must be active before the surround can be active too, and are consistent with the results of Figs. 3a and 4a, from which it appeared that in the dark-adapted eye the surround had a threshold. We tried similar experiments on seven other units: an annulus of outer diameter 1 1 was presented periodically to the dark-adapted receptive field, and its luminance and inner diameter were varied over a considerable range in an effort to produce some suppression. With rare exceptions, when its diameter was small the annulus produced a small on-discharge, and when its

565 SURROUND CONTROL OF DISCHARGE diameter was increased it produced a negligible depression or had no effect at all. The interpretation of this result is complicated by the possibility that annular illumination which is intended exclusively to stimulate the surround might also excite the very sensitive centre. If it did, excitation a

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Fig. 7. Dependence of surround response upon illumination of the centre. a, from top: pulse-density tracings of responses to a small (3-4.5°) annulus, a larger (3-1 1) annulus and one representing the difference between the first and the second. All had a luminance of 3 9 x 103 quanta (507)/deg2 sec. Although the optimum spot diameter was 2.50, the smallest annulus excited the centre, producing a weak on-discharge. Expansion of the annulus to 110 (middle) abolished the response, presumably through surround antagonism, but the 4-5-11' annulus alone (bottom) produced no corresponding depression of the dark-discharge. Short bars under the tracings mark zero impulses/sec. X-cell, 32/3. b, depression of darkdischarge by a 2.5-110 annulus (14 x 1 04quanta.(507)/deg2 sec). This X-cell, 32/4, was one of the few that behaved in this way, and that may be related to the unit's unusually high rate of maintained discharge. Optimum spot diameter, 20.

via the centre might counterbalance exactly suppression via the surround, and we would be led inevitably to underestimate the sensitivity of the dark-adapted surround. However, the observations of Figs. 3a, 4a and 7a, together with the fact that in all but a few units (see below) we were unable

566 CHRISTINA ENROTH-CUGELL AND P. LENNIE to depress the dark-discharge with an annulus, lead us to believe that in the dark-adapted eye surround activity in most units depends upon activity in the centre. We discuss later the implications of this finding for linearity of centre-surround interaction. The behaviour of an unusual unit is shown in Fig. 7b. In the dark-adapted eye, the brief presentation of a 2.5-11o annulus (the optimum spot diameter was 20) produced a substantial suppression of the dark-discharge; steady illumination of the surround reduced the discharge from 25 to 5 impulses/sec (not shown in Figure). Latencies of centre and surround respon8e8. In the light-adapted eye, most X-cells give a sharp transient discharge to the onset of diffuse illumination (Fig. 3b, bottom centre). Probably this reflects a difference between centre and surround latencies, for in the light-adapted eye surround and centre have well-matched sensitivities (Figs. 4-6). Relative latencies have been discussed by Barlow et al. (1957), Rodieck & Stone (1965b) and Maffei, Cervetto & Fiorentini (1970), but have not been measured when both mechanisms are optimally stimulated. Centre latency may be measured directly, and by subtracting the response to the optimum spot from that to diffuse illumination, it is easy to estimate the latency of the surround. The points plotted in Fig. 8, showing centre and surround latencies of moderate responses as a function of background luminance, are derived from pulse-density tracings by the method indicated in the inset to the Figure. Latencies of both mechanisms are progressively reduced by light-adaptation, although the centre remains faster. Centre and surround latencies varied from unit to unit, and in the dark-adapted eye ranged respectively from 55 to 80 and 80 to 105 msec (means 65 and 95 msec). In the light-adapted eye the range was smaller: 45-50 msec for the centre (mean 46 msec) and 60-75 msec for the surround (mean 63 msec). An interesting feature of Fig. 8 is that surround latency is reduced from its dark-adapted value by more than that of the centre, and begins to decline rapidly when the background has started to light adapt the centre (open arrow on abscissa). Probably the change in relative latency reflects the relatively improved sensitivity of the surround: as background luminance is raised the surround's response grows relative to the centre's until they are almost matched (Fig. 6). Since latency decreases as response strength increases (Cleland & Enroth-Cugell, 1968) we should expect a larger absolute decrease in surround latency. Y-cells. The subtraction technique could not satisfactorily separate centre and surround components of the responses of Y-cells. The problem arose when we attempted to find the optimum spot. This had been done for X-cells by increasing spot diameter until one was found which gave

SURROUND CONTROL OF DISCHARGE 567 the lowest threshold, and invariably the pulse-density tracings we obtained confirmed the choice; larger spots gave identical or smaller responses. But for Y-cells the optimal spot never fully isolated the centre. Pulsedensity tracings showed that the spot which gave the lowest threshold

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already seemed to excite the surround and larger spots regularly caused larger 'on' transients (Fig. 9). The reason for this may be that in Y-cells there is a substantial region of the receptive field within which centre and surround are about equally sensitive. Once a stimulus is sufficiently large to enter this region, further moderate increases in size affect centre and surround about equally (see Discussion). It is difficult otherwise to explain how enlargement of an 'optimal' spot tends to bring about increasingly large 'on' transients with increasingly strong suppression of later stages in the response.

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Fig. 9. Responses from the surround of a dark-adapted Y-cell. Top row, left; threshold response to the 'optimal' spot (diam. 2.25°). Centre: response to an 11° spot of the same luminance. Right: the difference between responses to the 2-25 and 110 spots. This estimates the surround response. Second and third rows show tracings of responses to stimuli of higher luminances. The conspicuous excitatory transients in the tracings of the right-hand column show that enlargement of the 'optimal' spot to cover the whole receptive field brought about an increased response from the centre. The surround's contribution is therefore underestimated. No change in optimum spot diameter better exposed the surround. Note how sustained are responses to the optimum spot when the eye is dark-adapted. Unit 25/5.

This behaviour of Y-cells precluded the neat separation of centre and surround which was possible for X-cells, for always the subtraction technique led to an underestimate of the surround's involvement in the response to diffuse illumination. However, we were able to show (Fig. 9) that the surrounds of Y-cells also are active in the dark-adapted eye. Note the large excitatory transient which appears in the 'surround' responses. We could have diminished this by making the optimum spot larger, but then the surround contribution would have been more obscured. Maintained discharge In the next paper (Enroth-Cugell, Lennie & Shapley, 1975) it is shown that enlargement of a small steady spot, concentric with the receptive field, causes the ganglion cell's maintained discharge first to rise a little and then to fall. The rise may be attributed to increasing summation of signals within the receptive field centre, and the fall to the increasingly

569 SURROUND CONTROL OF DISCHARGE suppressive action of light shone upon the surround (Barlow & Levick, 1969b). To repeat this experiment at a number of background luminances takes many hours, for each change in background size or illumination may leave the maintained discharge unstable for 10 min or more (Fig. 12b). So to observe how the surround's contribution depends upon background luminance we carried out a simpler experiment using the optimal spot/ diffuse illumination technique which had been so helpful in analysing time-varying responses. X-cells. After dark-adaptation the maintained discharge was recorded first without a background, then in the presence of a steady background which covered just the middle (optimal spot) or the whole receptive field. Fig. 10 shows, for two units, how the maintained discharge varied with steady luminance, for both optimal spot and diffuse illumination. The points plotted, which are the steady levels reached after each change of background, show that mean rate to the optimal spot rises faster and stays higher than does that rate to diffuse illumination. This confirms the suggestion of Barlow & Levick (1969b) and the observation of Sakmann & Creutzfeldt (1969) that the surround helps moderate the maintained discharge. At intermediate luminances, centre-surround balance appears to have an important influence upon the mean rate of some units (Fig. 10, lower; Sakmann & Creutzfeldt, 1969, Fig. 3; Enroth-Cugell et al. 1975, Fig. 1), and changes in maintained discharge with adaptation level may be predicted from the spatial organization of the receptive field. But it seems from Fig. 10 that the surround was not the major factor causing the changes in mean rate at the higher background luminances, for the break in the monotonic rise, and subsequent decline, occurred also with the steady spot which optimally stimulated the centre. We have more evidence on this point. The graphs in Fig. 11 a plot for two units the mean rate of the maintained discharge as a function of the size of a bright steady spot. For one unit the discharge rate dropped for every increase in spot size; for the other it stayed relatively constant before dropping on the largest spots. Area-threshold curves for the same units are plotted in Fig. 1lb. Thresholds were obtained upon a diffuse background of the luminance used for the maintained-v8.-background curve, and 'threshold' luminance was that test flash intensity needed for a perceptible modulation of the maintained discharge. If the curves which describe the variation of maintained discharge with background size reflect the changing balance ofsignals from centre and surround, qualitative changes in mean rate with steady spot size might be expected to follow the area-threshold curve, rising monotomically for spots within Ricco's area, where the surround contribution is negligible, and declining for

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larger ones. Actually, as Fig. 11 shows, the area-threshold curve was a predictor of the area-maintained curve. In four other units, the mean rate at high background luminances was even less well predicted from the area-threshold curve. Our observations on the maintained discharge may be understood if the centre's contribution to the maintained discharge begins to saturate at luminances greater than about 105 quanta/deg2 sec, and the surround's contribution at similar or slightly higher ones. Y-cells. We found it difficult to separate centre and surround poor

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571

572 CHRISTINA ENROTH-CUGELL AND P. LENNIE contributions to the discharge of Y-cells, but in an attempt to get some idea of surround influence we repeated the experiments which had been carried out on X-cells. Fig. 12a plots mean rate against the luminance of a diffuse and of an 'optimal' background. The relation resembles that for the X-cells of Fig. 10, but diffuse illumination produced a less consistent reduction in 60

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level of illumination. Filled circles plot the rate to an 'optimal' (40 diameter) spot, open circles that to diffuse illumination. The surround does not uniformly lower the discharge rate. b, recovery of maintained discharge following a change in background size from 4 to 11° (arrowed), at an illumination of 35 x 107 quanta (507)/degI sec. The mean rate is traced by a heavily damped pen-recorder. Unit 31/4.

discharge rate, and at the highest luminances the mean rate was higher than to the optimal spot. This might have been a consequence of our poor choice of ' optimal' spot leading to an underestimate of surround influence (see Fig. 9) but we think there is an additional reason. When the spot was enlarged to cover the receptive field, often there was a marked drop in discharge, followed by a slow recovery over a period of up to 15 mm,. especially at higher background luminances (Fig. 12b). This suppression

SURROUND CONTROL OF DISCHARGE 573 and recovery was seen in X-cells too, but always recovery was more complete in the Y-cell. In the latter unit, surround control of maintained discharge seems to be less persistent. DISCUSSION

The 8ubtraction method. In interpreting the results of many experiments described in this paper we have assumed additive combination of signals from centre and surround. Although the experiment of Fig. 2 provides a strong backing to this assumption, we want to point out that even were the combination not additive, most of our generalizations about surround behaviour would hold. Where a 'surround' response is described, it would be necessary to substitute 'change in discharge brought about by the surround', and our conclusions would be weakened to the extent that the experiments did not accurately estimate the surround signal. An obvious question is why our method can separate the behaviour of centre and surround when there is abundant evidence that the surround overlaps the centre extensively or completely (Rodieck & Stone 1965 b; Enroth-Cugell & IRobson, 1966; Enroth-Cugell & Pinto, 1972). We believe that for X-cells the method works well: a strong test for surround involvement in the response to a small spot is to change spot area, and see if by adjusting its luminance an identical response can be produced. Changing spot size alters the balance between centre and surround components, and unless centre and surround components have identical latencies, it should not be possible to elicit identical responses to different sized spots were the surround involved in the response to one of them. Procedures like this (and others discussed in Cleland & Enroth-Cugell, 1968) make possible the recognition of responses which are entirely due to, or are overwhelmingly dominated by, the centre. Identical responses to spots of 'optimal' diameters and smaller were obtained easily from X- but not from Y-cells. We believe, with Winters, Hickey & Pollack (1973), that the sensitivity profiles of the receptive field centres of X- and of Y-cells bear different relations to those of their respective surrounds. The X-cell has a small centre (Enroth-Cugell & Robson, 1966; Cleland et al. 1973) whose steepsided sensitivity profile sits within that of a much larger surround. In the middle of the receptive field, centre sensitivity is so very much greater than that of the surround that the latter mechanism is negligibly involved in responses to small, centred stimuli. But stimuli which extend beyond the middle fall upon regions where surround sensitivity is still high, so antagonism appears abruptly. For a Y-cell the situation is different. Its receptive field centre is larger, and seems to be matched more closely in size to the

574 CHRISTINA ENROTH-CUGELL AND P. LENNIE surround. Surrounds of Y-cells may be relatively smaller than are those of X-cells, or their distribution of sensitivity may be different, but we have no evidence that Y-cell surrounds are absolutely smaller. The reverse is probably true (Cleland et al. 1973). Nor do our results indicate that surrounds of Y-cells are less potent than those of X-cells; they are just better masked by the centres. This scheme accounts for our results and it accommodates other observations. Enroth-Cugell & Pinto (1972) were able dichotomously to classify units as 'surround revealing' or 'surround concealing' depending upon whether or not a surround response could be elicited uncontaminated by centre antagonism. We believe now that these units were X- and Y-cells respectively. Permsitence of surrounds in dark-adaptation. It is widely believed, following Barlow et al. (1957), that in the dark-adapted eye the surround 'drops out' and cannot be activated. This conclusion must be qualified a little in the light of our results, for although centre sensitivity is sufficiently greater than that of the surround that a diffuse, long-duration, stimulus will elicit negligible surround suppression at absolute threshold (Figs. 3a, 4a), a slightly more intense stimulus produces marked suppression. The most conspicuous change in the surround with increasing darkadaptation is not the weakening of its suppressive properties, but the complete loss of its capacity to increase discharge at stimulus offset (the off-discharge). If this discharge, instead of suppression, is used as the index of surround sensitivity, one will be led to estimates of surround sensitivity much lower than those described here. Origin of off-discharges. The development of the off-discharge is closely linked with the level of light-adaptation, and in the following paragraphs we indicate how it could be due to the surround's adaptation mechanism, its 'automatic gain control' (Rushton, 1965). Our account is based upon a recent formal treatment of adaptation in the central mechanism (Enroth-Cugell & Shapley, 1973). For some range of low background luminances the sensitivity of neither the centre nor the surround is reduced from its dark-adapted value (Fig. 5); the gain control of both mechanisms seems to have a threshold. This threshold may be exceeded either by raising background luminance and/or by using a stronger stimulus, for it is the total amount of light falling upon the relevant region of the receptive field that is presumed to trigger the corresponding gain control. As long as the gain control's threshold is not exceeded, the ganglion cell will receive a faithful copy of the signal from the receptors. So, in the dark-adapted eye, ganglion cell discharge closely follows changes in stimulus luminance and a sustained response is elicited by a sustained stimulus (Fig. 3a). At slightly higher

575 SURROUND CONTROL OF DISCHARGE backgrounds, or with strong stimuli, the gain control becomes active and after some delay an attenuating signal acts upon signals from the receptors. Thus the application of an incremental stimulus, which, like the steady background, provides an input to the gain control, leads to a more transient response whose time course reflects the relatively slow adjustment in gain (Fig. 6). The important point to note is that this process is symmetrical: the removal of an increment must also cause a gain adjustment, but this adjustment is slow, and there is for a short time an inappropriately strong attenuation of the signal from receptors. Thus, in the light adapted on-centre unit, the onset of diffuse illumination causes for the centre an initial sharp increase in discharge which declines over some hundreds of milliseconds, and for the surround an initial tendency, which also diminishes with time, to decrease discharge. At stimulus offset the opposite happens: the discharge due to the centre and response suppression due to the surround cease abruptly, but the sluggish gain controls are now wrongly set, and until they recover there is a marked suppression of excitation from the centre and a corresponding decrease in inhibition from the surround. It is the latter which tends to produce off-discharges. These we believe result from a momentary heavy depression of tonic (suppressive) input to the ganglion cell from its surround during the adjustment of gain. The balance of centre-&urround antagonism. When background illumination exceeds about 104 quanta/deg2 see the antagonism of centre and surround is well balanced: centre and surround are about equally sensitive to diffuse illumination (Fig. 5), and the surround response mirrors closely that of the centre (Fig. 6), albeit after some delay (Fig. 8). Previous observations (Maffei et al. 1970; Maffei, Fiorentini & Cervetto, 1971) have not revealed such well matched antagonism, and probably differences in method account for the discrepant results. Maffei et al. compared responses of centre and surround to a spot shone on the receptive field middle or on the periphery. They found, even at high background luminances, that the surround was less responsive and its temporal resolution poorer. But the surround is able to match the performance of the centre only by accumulating signals over a much larger area, and our measurements suggest that when adequately stimulated it weighs equally against the centre. This one would expect were its function to augment spatial selectivity. Potentiation of surround response by illumination of the centre. Steady illumination of the centre does make surround responses more conspicuous (Barlow et al. 1964; Maffei et al. 1971; Enroth-Cugell & Pinto, 1972; Kruger & Fischer, 1973) and Maffei et al. and Kruger & Fischer have inferred from this that illumination of the centre potentiates surround response. Some of our results (Figs. 4a, 7) support this conjecture, and

CHRISTINA ENROTH-CUGELL AND P. LENNIE 576 might be thought evidence for a divisive surround: if centre-surround interaction were truly linear, the surround's influence upon the ganglion cell should not depend upon activity in the centre, yet in the dark-adapted eye it clearly can. But the observations of Fig. 2, and those of Rodieck & Stone (1965a, b) and Enroth-Cugell & Pinto (1972) provide some substantial evidence for additive combination of centre and surround signals. These superficially conflicting findings might be reconciled by the following scheme. Consider an on-centre ganglion cell in which excitatory signals from the centre converge upon the ganglion cell directly, and inhibitory signals from the surround act upon this central path before the ganglion cell. The suppressive surround can act only by removing excitation transmitted to the ganglion cell via its centre; it cannot inhibit the cell directly. This being the case, even a subtractive surround must show a threshold dependence upon centre activity. Control of maintained discharge. Surrounds of X-cells generate steady signals which help keep down the maintained discharge (Fig. 10), but these signals produce a uniform or diminishing reduction of discharge at higher background luminances, and evidently are not alone responsible for the constancy or deline in mean rate. Barlow & Levick (1969b) explained the statistical properties of the maintained discharge in on-centre units by suggesting that the mean rate reflected the difference between the number of quanta absorbed by the centre, scaled according to adaptation level, and the similarly scaled number of quanta absorbed by the surround, while the variability reflected the variance in the number of quanta absorbed over the whole receptive field, also scaled according to adaptation level. No exact prediction could be made about the mean rate, since it depended upon the balance of inputs from centre and surround, but if the balance between centre and surround signals does account for the mean rate, both signals must be saturating or non-monotonic functions of luminance. It is difficult otherwise to explain why at high background illuminations the rate of maintained discharge is so poorly predicted from the spatial properties of the receptive field. Beyond suggesting that neither the centre nor the surround feeds a large steady signal to the ganglion cell, our observations help rather little in understanding the origins or control of the maintained discharge. Implications for psychophysics. Psychophysical performance on a number of tasks depends upon the level of light-adaptation: at higher levels of illumination resolution acuity improves (Riggs, 1965) and the range of spatial summation correspondingly declines (Hallett, 1963). Spatial interactions in scotopic vision (Westheimer, 1965) and the shape of the human contrast sensitivity function too, depend upon mean illumination in a

SURROUND CONTROL OF DISCHARGE 577 way which might be explained by a relative decrease in sensitivity of surrounds in the dark-adapted eye. In a number of respects the surround in the dark-adapted eye performs less well than the centre: it is less sensitive, probably is more sluggish, and has a longer latency. To determine whether these changes are sufficient to account for changes in psychophysical threshold we have to know more about the properties ofthe threshold device and in what aspects of ganglion cell discharge it is interested. Several of our colleagues read and generously commented upon the manuscript. We are grateful to the American Cyanamid Company for providing us with Flaxedil, and to Hoffman-La Roche Inc. for supplying us with toxiferine. This work was supported by NIH grants 5 R 01 EY00206 and 5 K 03 EY18537. P.L. held a Harkness Fellowship. REFERENCES

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