J. Physiol. (1975), 247, pp. 579-588 With 4 text-figures Printed in Great Britain
579
SURROUND CONTRIBUTION TO LIGHT ADAPTATION IN CAT RETINAL GANGLION CELLS
By CHRISTINA ENROTH-CUGELL,* P. LENNIEt AND R. M. SHAPLEYt From the Departments of Biological Sciences and Electrical Engineering, Northwestern University, Evanston, Illinois, U.S.A. and Rockefeller University, New York, New York, U.S.A.:
(Received 12 July 1974) SUMMARY
1. The sensitivity of a cat's retinal ganglion cell to a small, dim, spot flashed upon the middle of the receptive field depends upon the size of a concentric steady background: sensitivity is reduced monotonically with background area. All backgrounds which equal or exceed in size the central summing area of the ganglion cell produce an equivalent reduction of sensitivity, even though only backgrounds which extend outside the central summing area depress the maintained discharge. 2. If a small background lies upon the middle of the receptive field, and the test spot is made intense enough to evoke a strong response, steady illumination of the periphery may make the response larger. 3. This change in response is not due to an enhancement of centre sensitivity by the surround, but is readily understood if steady illumination of the periphery adapts out the surround's antagonism of the centre's response to the test flash. 4. The failure of steady stimulation of the surround to alter centre sensitivity implies that signals from the surround subtract from, or add to, those from the centre. INTRODUCTION
The sensitivity of a ganglion cell in the cat retina is adjusted rapidly when background illumination is changed. But not only illumination is important, background size is too: sensitivity to a small spot centred on the receptive field depends upon the flux (illumination x area) of the background as long as that falls entirely within the receptive field centre * Mailing address: Biomedical Engineering Center, Technological Institute, Northwestern University, Evanston, Illinois 60201. t Present address: The Psychological Laboratory, Cambridge, England.
58050 CHRISTINA ENROTH-CUGELL AND OTHERS (Cleland & Enroth-Cugell, 1968). Previous work from this laboratory (Enroth-Cugell & Shapley, 1973) suggested that backgrounds larger than the centre cause no further change in sensitivity, but there are other indications (Maffei, 1968; Maffei, Cervetto & Fiorentini, 1970) that steady illumination of the periphery can alter the ganglion cell's sensitivity to a small spot in the middle. This paper describes experiments which help resolve the conflict of evidence. We show that steady illumination of the periphery has no influence upon the sensitivity of the centre even when the surround is known to be sending a steady signal to the ganglion cell. Although under certain conditions (resembling those used by Maffei and his colleagues), steady illumination of the surround may enhance the response to a stimulus in the receptive field middle, we have found that this is not due to a change in centre sensitivity. The results have an important corollary: since steady surround signals do not contribute to light adaptation of the centre, these signals interact linearly with signals from the centre. METHODS Our preparation and apparatus were as described in the preceding paper, except that three fluorescent sources were used in some experiments. Masks or diaphragms could be placed before each source to provide stimulus or background fields of different geometries. Two sources could be modulated, and when these were used as stimuli blue-green filters (Ilford 623) were interposed to help isolate rods. Retinal illuminations were calculated on the assumption that 75 % of the light falling on the cornea reaches the retina, and impulse/quantum ratios on the assumption that one third of the light reaching the retina is absorbed by rods (Bonds & MacLeod, 1974; Barlow, Levick & Yoon, 1971). Of the twenty on-centre units we studied in seven cats, ten were X-cells, eight Y-cells and for two units the distinction was not made. All receptive fields lay within 30° of the area-centralis. RESULTS
For the experiments described here, it was important to know something of the distribution of sensitivity in the ganglion cell receptive field. So at the start of each experiment sensitivity profiles for the centre were mapped. A small (0.180) spot, flashing at 4 c/s, was placed in several positions (0.5 or 0 25° apart) along the horizontal and vertical diameters of the dark adapted receptive field and its luminance adjusted for an audible modulation of the discharge. A surround profile could not similarly be mapped because the surround is masked by the centre over a large part of the receptive field. The size of the receptive field centre can be estimated also by calculating its effective summing area, At (Cleland & Enroth-Cugell, 1968), and to
SURROUND CONTRIBUTION TO LIGHT ADAPTATION 581 corroborate our estimate based upon sensitivity profiles, we did that too. At, which is the same as the 'equivalent centre' of Cleland, Levick & Sanderson (1973), may be viewed as the area of a circular region of uniform sensitivity which has the same integrated sensitivity and the same peak sensitivity as the actual centre. It is found by comparing sensitivity for a small spot, centred upon the receptive field, with sensitivity for a concentric spot which completely covers the centre. The two measures of centre size are consistently related, the diameter of the equivalent summing area being equal to that of the sensitivity profile at a point where sensitivity has declined from its maximum 0.4-1.0 and 1 0-2 0 log units for X- and Y-cells, respectively. The effect of background size. This experiment was a neurophysiological analogue of a psychophysical one first carried out by Crawford (1940); sensitivity to a small test spot was measured as a function of the size of a concentric steady background. In our experiment the test spot, which was centred upon the receptive field and was 0.180 in diameter (0x025 deg2), was presented for 1-25 sec every 2-5 sec upon backgrounds of different sizes. The smallest background was the same size as the test spot and the largest 100 deg2, which was sufficient to cover completely all but the very largest receptive fields. Beginning with the smallest background, test spot luminance was adjusted to give an approximately constant criterion response (usually an averaged peak discharge rate of 50 impulses/sec above the steady discharge in the absence of a stimulus). This was repeated at successively larger backgrounds of fixed luminance and since background size did affect sensitivity, appropriate adjustments of stimulus luminance had to be made to keep response constant. Fig. 1 shows for two cells the results of this experiment. Sensitivity is expressed in terms of the impulse/quantum (I/Q) ratio, i.e. peak additional discharge in impulses/sec divided by stimulus flux absorbed in quanta/sec, and here I/Q ratio is plotted against the area of the adapting spot. As the background area was expanded from 0-025 deg2 to cover the middle (At), sensitivity dropped by more than a log unit. There was negligible additional loss of sensitivity once background area exceed At; that is, when the background extended into the receptive field periphery. The initial drop in sensitivity shows simply that the effects of adapting light add within the receptive field centre. That has fully been described before (Cleland & Enroth-Cugell, 1968; Enroth-Cugell & Shapley, 1973). Of greater interest now is the failure of steady peripheral illumination to influence sensitivity to a test spot on the middle of the receptive field. If surround signals had had any effect at all, the curves of Fig. 1 A would not have flattened out as they did. Instead, they would have turned up or
582 CHRISTINA ENROTH-CUGELL AND OTHERS down, depending upon whether the surround increased or decreased the centre's sensitivity. It might be objected that although larger adapting spots covered both centre and surround, for some reason they may have failed to elicit 10-1
A
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1-0 10 100 Background area (deg2) Fig. 1. A, the variation of impulse/quantum (I/Q) ratio with background size. Filled circles plot for Y-cell 5/3 the sensitivity to a 0-180 diameter spot presented on backgrounds of 4 x 104 quanta/deg2 sec. Open circles, sensitivity of X-cell 6/11 to a 1° test spot presented on backgrounds of 2*5 x I0O quanta/deg2 sec. Open and filled arrows on the abscissa mark respectively the limits of the central summing area for the X- and the Y-cell. Clearly only backgrounds which fall within this area influence sensitivity. B, the dependence of maintained discharge upon background size. Same units as in A, at the same background illuminations. Note the decline in mean rate as backgrounds extended beyond the centre on to the surround.
SURROUND CONTRIBUTION TO LIGHT ADAPTATION 583 surround activity. But this cannot be the case, because of the maintained discharge. This discharge was monitored throughout each experiment, and for the two units of Fig. 1 A the changes in it with background size have been plotted in Fig. 1 B. The maintained discharge was decreased by the large backgrounds that extended beyond the centre, presumably through surround activity (Barlow & Levick, 1969), yet these backgrounds failed to cause a change in sensitivity to the small flashing spot. For the Y-cell of Fig. 1 there was a modest drop in maintained discharge as the background was enlarged to cover the surround, but the graph is based upon the relatively steady levels reached some minutes after a change of background, and does not show the large transient reduction in impulse rate which occurred for these units whenever the background was enlarged from an area smaller than to an area larger than that of the centre. An example of such a change is shown in Fig. 12 of the previous paper (Enroth-Cugell & Lennie, 1975) and we think it demonstrates that the surround was being stimulated by the steady background. The change in maintained discharge was observed at a background illumination as low as 104 quanta (507)/deg2 sec. Enlarging the background from covering just the centre to covering the whole receptive field had negligible effect upon centre sensitivity. But if one uses a stronger test stimulus and/or a criterion more sensitive to the slow components of response, centre sensitivity may appear to be increased when the background is expanded from covering just the centre to covering the whole receptive field. The results of the following experiments show that this apparent enhancement of centre sensitivity is spurious. Effect of background size when surround contributes to response. A small steady background centred upon a receptive field will depress the sensitivity of the centre relatively more than that of the surround, for a larger fraction of the centre's summing area is being filled with adapting flux. Under these conditions the surround's involvement in the response to a modulated stimulus is more easily seen,, and in fact this method has often been used to help isolate it, e.g. Barlow, Hill & Levick (1964). By varying background size in our experiments we altered the relative sensitivities of centre and surround, tending to enhance any surround involvement in response when the background was small and diminishing it when the background was large. Probably surround involvement was avoided in the experiment of Fig. 1 because a weak stimulus was used to produce a small response; for small responses the surround has a latency such that it little affects peak discharge rate, our criterion for sensitivity (Enroth-Cugell & Lennie, 1975). But sometimes, especially with a stronger test flash which probably excited both centre and surround, the time 22
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CHRISTINA ENROTH-CUGELL AND OTHERS 584 course of the response changed with background size. Some examples of this are shown in Fig. 2. Fig. 2A and B show responses to a moderately intense (108 quanta (507)/deg2 sec, incident on the retina) spot, 0.180 in diameter, which was presented upon a background 30 in diameter, chosen to cover just the
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~~~~~~~~~~301
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B A
50
impulses/sec 110
1 Zero impulses/sec Fig. 2. The interaction between stimulus strength and background size. A and B, responses to a strong stimulus spot (108 quanta/deg2 see), 0.180 in diameter, presented respectively on a background equal in size to the central summing area and on one which covered the whole receptive field. Background illumination in both cases was 2-4 x 105 quanta/deg2 sec. On the larger background the response was more sustained and the discharge recovered more slowly following stimulus offset. C and D, responses to a weaker stimulus (2-5 x 107 quanta/deg2 see) on the same two backgrounds as before. Note how little the time course of the small responses depended on background size. On centre X-cell, 5/2; central summing area 6 deg2.
receptive field middle, and upon one 11° in diameter. On the smaller background the response showed clear evidence of surround antagonism: the peak discharge decayed to a mean rate lower than that just before stimulus onset, and at stimulus offset there was only a brief dip in discharge. On the larger background the same stimulus caused a slightly higher peak discharge and more extra impulses, and after the drop in firing at stimulus offset there was a slow recovery. These differences in response pattern suggest that expansion of the background light-adapted
SURROUND CONTRIBUTION TO LIGHT ADAPTATION 585 the surround, making it less able to suppress firing during presentation of the test spot, and less able to excite the cell at stimulus offset, but similar changes might have occurred had the centre become more sensitive. The latter possibility is hard to reconcile with the observations of Fig. 2C and D. There are shown, for the same unit and the same backgrounds, responses to weaker test spots which would be expected to excite the surround less. Now the response on the smaller background shows little evidence of surround antagonism and the difference between the pulsedensity tracings is slight. Had steady illumination of the surround enhanced centre sensitivity, it should have altered large and small responses alike. Apparently it influences only the surround's sensitivity. Jso impulses/sec
C
A
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C and D
Flashing Steady Fig. 3. The effect of steady annular illumination upon sensitivity. A, __-
a
1° test spot (retinal illumination 2-5 x 106 quanta/deg2 see) was superimposed upon a steady adapting spot 1*6' in diameter which produced an illumination of 2.4 x 106 quanta/deg2 sec. In B, an annulus (70 inner, 120 outer diameter, illumination 1-3 x 106 quanta/deg2 see) was added to this arrangement. It barely altered the response. C and D, same configurations as in A and B, but with a stronger stimulus (106 quanta/deg2 sec). Their effects are compared in the lower part of the Figure; plainly the addition of the annulus in D enhanced the response. X-cell, 6/11, central summing area 1 deg2.
Dependence upon background configuration. We were interested to know if our findings depended upon the use of a uniform disk as a background, so in the following experiments another background configuration was used. First, a steady adapting spot of area less than At was centred upon the receptive field and the luminance of a small central test spot was adjusted to cause a weak response, apparently lacking surround antagonism (Fig. 3 A). Then to this configuration was added a steady annulus of inner diameter 70 and outer diameter 120 and the stimulus used before was 22-2
CHRISTINA ENROTH-CUGELL AND OTHERS presented (Fig. 3B). It left the response practically unchanged. However, with the same steady adapting spot, if the stimulus was made stronger (Fig. 3C), so as to increase the likelihood of surround involvement in the response, the addition of the same annulus as before (Fig. 3D) caused a 586
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Fig. 4. Effect of annular illumination on a small mixed response. A, a steady background of 1-5 x 106 quanta/deg2 sec, 0 450 in diameter was centred upon the receptive field and a test spot of the same size (at 1-5 x 105 quanta/deg2 see) was superimposed on it. In B an annulus of inner diameter 4.50, outer diameter 120 was added at a steady retinal illumination of 5-1 x 103 quanta/ deg2 sec, and in C annulus illuminance was increased to 5 x 104 quanta/deg2 sec. There was a progressive change in the time course of response as annular illumination was increased, which can be seen most clearly from the comparison of A and C in the lower part of the figure. Probably a Ycell, 41/8. The central summing area was 12 deg2, and its diameter is marked by the bar under the stimulus profile in C.
big increase in discharge. The changes in discharge brought about by adding the annulus, and their dependence upon the size of the response to the test flash, match well the changes observed in the corresponding experiments using uniform backgrounds (Fig. 2). Background configuration thus appears to be of little importance in these experiments. Steady illumination of the surround affects only mixed responses from centre and surround, but these responses need not always be large. Fig. 4 shows how, with centre sensitivity heavily depressed by the adapting spot, even a weak response may involve the surround, and how surround antagonism is progressively diminished by brighter annuli.
SURROUND CONTRIBUTION TO LIGHT ADAPTATION
587
DISCUSSION
These experiments examined the conditions under which steady illumination of the receptive field periphery alters a ganglion cell's sensitivity to a stimulus presented to the centre. We have shown that only when the stimulus is strong and/or the sensitivity of the centre is depressed by an adapting spot, does steady surround illumination perceptibly alter the response of the ganglion cell. The increase in discharge which appears under these conditions reflects the removal by light-adaptation of the surround's antagonistic response to the test stimulus; it is not the consequence of enhanced centre sensitivity. Choice of sensitivity measure. Had we chosen a criterion for sensitivity which was weighted more in favour of the slow components of ganglion cell response, we would have found often that sensitivity to a small spot depended upon steady illumination of the surround (Figs. 3 and 4). Perhaps this is why Maffei (1968) found that the response to modulation of a spot presented to the receptive field centre was enhanced by steady illumination of the surround, and why Nakayama (1971) found in units of the lateral geniculate nucleus that steady surround illumination increased sensitivity to a small flash. By using response measures which are sensitive to the slower components of discharge, and therefore to time-modulated surround activity, one may be led erroneously to conclude that steady illumination of the surround influences centre sensitivity. Slow components of discharge are probably relevant for some aspects of visual performance, but in trying to understand how centre sensitivity is controlled, peak discharge rate is the most suitable measure of response. Relation to previous work. Earlier work from this laboratory (Cleland & Enroth-Cugell, 1968; Enroth-Cugell & Shapley, 1973) suggested that the sensitivity of the centre was uninfluenced by steady light falling upon the periphery. The present experiments more firmly established this idea, for we used backgrounds and annuli so large that the surround had every opportunity to alter centre sensitivity were it capable of doing so. These backgrounds and annuli apparently caused a steady input from the surround, for they depressed the maintained discharge. Work broadly in agreement has been described by Sakmann, Creutzfeldt & Scheich (1969). Linearity of centre-surround interaction. Since steady signals from the surround have no influence upon the centre's sensitivity to flashes, these signals can only subtract from, or add to, signals from the centre. A number of observations suggest that transient signals from the two mechanisms also subtract arithmetically, and some are described in the preceding paper (Enroth-Cugell & Lennie, 1975). There it was shown that
588 88CHRISTINA ENROTH-CUGELL AND OTHERS an annulus of constant luminance, when flashed together with a concentric small spot, decreases the response to the spot by a constant amount which is independent of spot luminance. From different experiments Maffei & Cervetto (1968) and Enroth-Cugell & Pinto (1972) also have concluded that centre and surround signals interact linearly.
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 Hoffmann-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
BARLOW, H. B., HILL, R. M. & LEVICK, W. R. (1964). Retinal ganglion cells respond-
ing selectively to direction and speed of image motion in the rabbit. J. Physiol.
173, 373-407. BARLOW, H. B. & LEVICK, W. R. (1969). Changes in maintained discharge with adaptation level in the cat retina. J. Physiol. 202, 699-718. BARLOW, H. B., LEVIcK, W. R. & YooN, M. (1971). Responses to single quanta of light in retinal ganglion cells of the cat. Vision Res. suppl. 3, 87-101. BONDS. A. B. & MAcLEOD D. I. A. (1974). The bleaching and regeneration of rhodopsin in the cat. J. Physiol. 242, 237-253. CLELAND, B. G. & ENROTH-CUGELL, C. (1968). Quantitative aspects of sensitivity and summation in the cat retina. J. Physiol. 198, 17-38. CLELAND, B. G., LEVIcK, W. R. & SANDERSON, K. J. (1973). Properties of sustained and transient ganglion cells in the cat retina. J. Physiol. 228, 649-680. CRAWFORD, B. H. (1940). The effect of field size and pattern on the change of visual sensitivity with time. Proc. R. Soc. B 129, 94-106. ENROTH-CUGELL, C. & LENNIE, P. (1975). The control of retinal ganglion cell discharge by receptive field surrounds. J. Physiol. 247, 551-578. ENROTH-CUGELL, C. & PINTO, L. H. (1972). Properties of the surround response mechanism of cat retinal ganglion cells and centre-surround interaction. J. Physiol. 220, 403-439. ENROTH-CUGELL, C. & SHAIPLEY, R. M. (1973). Flux, not retinal illumination, is what cat retinal ganglioni cells really care about. J. Physiol. 233, 311-326. MAFFEI, L. (196 8). Inhibitory and facilitatory spatial interactions in retinal receptive fields. Vision Res. 8, 1187-1194. MAFFEI, L. & CERVETTO, L. (1968). Dynamic interactions in retinal receptive fields. Vision Res. 8, 1299 1303. MAFFEI, L., CERVETTO, L. & FiORENTINI, A. (1970). Transfer characteristics of excitation and inhibition in cat retinal ganglion cells. J. Neurophysiol. 33, 276-284. NAKAYAMA, K. (1971). Local adaptation in cat LGN cells: evidence for a surround antagonism. Vision Res. 11, 501 509. SAKMANN, B., CREUTZFELDT, 0. & SCHEICH, H. (1969). An experimental comparison between the ganglion cell receptive field and the receptive field of the adaptation pool in the cat retina. Pflilqers Arch. qes. Physiol. 307, 133-137.
579
SURROUND CONTRIBUTION TO LIGHT ADAPTATION IN CAT RETINAL GANGLION CELLS
By CHRISTINA ENROTH-CUGELL,* P. LENNIEt AND R. M. SHAPLEYt From the Departments of Biological Sciences and Electrical Engineering, Northwestern University, Evanston, Illinois, U.S.A. and Rockefeller University, New York, New York, U.S.A.:
(Received 12 July 1974) SUMMARY
1. The sensitivity of a cat's retinal ganglion cell to a small, dim, spot flashed upon the middle of the receptive field depends upon the size of a concentric steady background: sensitivity is reduced monotonically with background area. All backgrounds which equal or exceed in size the central summing area of the ganglion cell produce an equivalent reduction of sensitivity, even though only backgrounds which extend outside the central summing area depress the maintained discharge. 2. If a small background lies upon the middle of the receptive field, and the test spot is made intense enough to evoke a strong response, steady illumination of the periphery may make the response larger. 3. This change in response is not due to an enhancement of centre sensitivity by the surround, but is readily understood if steady illumination of the periphery adapts out the surround's antagonism of the centre's response to the test flash. 4. The failure of steady stimulation of the surround to alter centre sensitivity implies that signals from the surround subtract from, or add to, those from the centre. INTRODUCTION
The sensitivity of a ganglion cell in the cat retina is adjusted rapidly when background illumination is changed. But not only illumination is important, background size is too: sensitivity to a small spot centred on the receptive field depends upon the flux (illumination x area) of the background as long as that falls entirely within the receptive field centre * Mailing address: Biomedical Engineering Center, Technological Institute, Northwestern University, Evanston, Illinois 60201. t Present address: The Psychological Laboratory, Cambridge, England.
58050 CHRISTINA ENROTH-CUGELL AND OTHERS (Cleland & Enroth-Cugell, 1968). Previous work from this laboratory (Enroth-Cugell & Shapley, 1973) suggested that backgrounds larger than the centre cause no further change in sensitivity, but there are other indications (Maffei, 1968; Maffei, Cervetto & Fiorentini, 1970) that steady illumination of the periphery can alter the ganglion cell's sensitivity to a small spot in the middle. This paper describes experiments which help resolve the conflict of evidence. We show that steady illumination of the periphery has no influence upon the sensitivity of the centre even when the surround is known to be sending a steady signal to the ganglion cell. Although under certain conditions (resembling those used by Maffei and his colleagues), steady illumination of the surround may enhance the response to a stimulus in the receptive field middle, we have found that this is not due to a change in centre sensitivity. The results have an important corollary: since steady surround signals do not contribute to light adaptation of the centre, these signals interact linearly with signals from the centre. METHODS Our preparation and apparatus were as described in the preceding paper, except that three fluorescent sources were used in some experiments. Masks or diaphragms could be placed before each source to provide stimulus or background fields of different geometries. Two sources could be modulated, and when these were used as stimuli blue-green filters (Ilford 623) were interposed to help isolate rods. Retinal illuminations were calculated on the assumption that 75 % of the light falling on the cornea reaches the retina, and impulse/quantum ratios on the assumption that one third of the light reaching the retina is absorbed by rods (Bonds & MacLeod, 1974; Barlow, Levick & Yoon, 1971). Of the twenty on-centre units we studied in seven cats, ten were X-cells, eight Y-cells and for two units the distinction was not made. All receptive fields lay within 30° of the area-centralis. RESULTS
For the experiments described here, it was important to know something of the distribution of sensitivity in the ganglion cell receptive field. So at the start of each experiment sensitivity profiles for the centre were mapped. A small (0.180) spot, flashing at 4 c/s, was placed in several positions (0.5 or 0 25° apart) along the horizontal and vertical diameters of the dark adapted receptive field and its luminance adjusted for an audible modulation of the discharge. A surround profile could not similarly be mapped because the surround is masked by the centre over a large part of the receptive field. The size of the receptive field centre can be estimated also by calculating its effective summing area, At (Cleland & Enroth-Cugell, 1968), and to
SURROUND CONTRIBUTION TO LIGHT ADAPTATION 581 corroborate our estimate based upon sensitivity profiles, we did that too. At, which is the same as the 'equivalent centre' of Cleland, Levick & Sanderson (1973), may be viewed as the area of a circular region of uniform sensitivity which has the same integrated sensitivity and the same peak sensitivity as the actual centre. It is found by comparing sensitivity for a small spot, centred upon the receptive field, with sensitivity for a concentric spot which completely covers the centre. The two measures of centre size are consistently related, the diameter of the equivalent summing area being equal to that of the sensitivity profile at a point where sensitivity has declined from its maximum 0.4-1.0 and 1 0-2 0 log units for X- and Y-cells, respectively. The effect of background size. This experiment was a neurophysiological analogue of a psychophysical one first carried out by Crawford (1940); sensitivity to a small test spot was measured as a function of the size of a concentric steady background. In our experiment the test spot, which was centred upon the receptive field and was 0.180 in diameter (0x025 deg2), was presented for 1-25 sec every 2-5 sec upon backgrounds of different sizes. The smallest background was the same size as the test spot and the largest 100 deg2, which was sufficient to cover completely all but the very largest receptive fields. Beginning with the smallest background, test spot luminance was adjusted to give an approximately constant criterion response (usually an averaged peak discharge rate of 50 impulses/sec above the steady discharge in the absence of a stimulus). This was repeated at successively larger backgrounds of fixed luminance and since background size did affect sensitivity, appropriate adjustments of stimulus luminance had to be made to keep response constant. Fig. 1 shows for two cells the results of this experiment. Sensitivity is expressed in terms of the impulse/quantum (I/Q) ratio, i.e. peak additional discharge in impulses/sec divided by stimulus flux absorbed in quanta/sec, and here I/Q ratio is plotted against the area of the adapting spot. As the background area was expanded from 0-025 deg2 to cover the middle (At), sensitivity dropped by more than a log unit. There was negligible additional loss of sensitivity once background area exceed At; that is, when the background extended into the receptive field periphery. The initial drop in sensitivity shows simply that the effects of adapting light add within the receptive field centre. That has fully been described before (Cleland & Enroth-Cugell, 1968; Enroth-Cugell & Shapley, 1973). Of greater interest now is the failure of steady peripheral illumination to influence sensitivity to a test spot on the middle of the receptive field. If surround signals had had any effect at all, the curves of Fig. 1 A would not have flattened out as they did. Instead, they would have turned up or
582 CHRISTINA ENROTH-CUGELL AND OTHERS down, depending upon whether the surround increased or decreased the centre's sensitivity. It might be objected that although larger adapting spots covered both centre and surround, for some reason they may have failed to elicit 10-1
A
10-2 0 c
10-3 10-4-\
0-5
0-01
0-1 1-0 10 Background area (deg2)
100
B. Maintained frequency 60-U 0~
E
20 I
0-01
,.
,,
01
,
I ,,,
1
,
1,,,,1
,
,,, ,,,,1
1-0 10 100 Background area (deg2) Fig. 1. A, the variation of impulse/quantum (I/Q) ratio with background size. Filled circles plot for Y-cell 5/3 the sensitivity to a 0-180 diameter spot presented on backgrounds of 4 x 104 quanta/deg2 sec. Open circles, sensitivity of X-cell 6/11 to a 1° test spot presented on backgrounds of 2*5 x I0O quanta/deg2 sec. Open and filled arrows on the abscissa mark respectively the limits of the central summing area for the X- and the Y-cell. Clearly only backgrounds which fall within this area influence sensitivity. B, the dependence of maintained discharge upon background size. Same units as in A, at the same background illuminations. Note the decline in mean rate as backgrounds extended beyond the centre on to the surround.
SURROUND CONTRIBUTION TO LIGHT ADAPTATION 583 surround activity. But this cannot be the case, because of the maintained discharge. This discharge was monitored throughout each experiment, and for the two units of Fig. 1 A the changes in it with background size have been plotted in Fig. 1 B. The maintained discharge was decreased by the large backgrounds that extended beyond the centre, presumably through surround activity (Barlow & Levick, 1969), yet these backgrounds failed to cause a change in sensitivity to the small flashing spot. For the Y-cell of Fig. 1 there was a modest drop in maintained discharge as the background was enlarged to cover the surround, but the graph is based upon the relatively steady levels reached some minutes after a change of background, and does not show the large transient reduction in impulse rate which occurred for these units whenever the background was enlarged from an area smaller than to an area larger than that of the centre. An example of such a change is shown in Fig. 12 of the previous paper (Enroth-Cugell & Lennie, 1975) and we think it demonstrates that the surround was being stimulated by the steady background. The change in maintained discharge was observed at a background illumination as low as 104 quanta (507)/deg2 sec. Enlarging the background from covering just the centre to covering the whole receptive field had negligible effect upon centre sensitivity. But if one uses a stronger test stimulus and/or a criterion more sensitive to the slow components of response, centre sensitivity may appear to be increased when the background is expanded from covering just the centre to covering the whole receptive field. The results of the following experiments show that this apparent enhancement of centre sensitivity is spurious. Effect of background size when surround contributes to response. A small steady background centred upon a receptive field will depress the sensitivity of the centre relatively more than that of the surround, for a larger fraction of the centre's summing area is being filled with adapting flux. Under these conditions the surround's involvement in the response to a modulated stimulus is more easily seen,, and in fact this method has often been used to help isolate it, e.g. Barlow, Hill & Levick (1964). By varying background size in our experiments we altered the relative sensitivities of centre and surround, tending to enhance any surround involvement in response when the background was small and diminishing it when the background was large. Probably surround involvement was avoided in the experiment of Fig. 1 because a weak stimulus was used to produce a small response; for small responses the surround has a latency such that it little affects peak discharge rate, our criterion for sensitivity (Enroth-Cugell & Lennie, 1975). But sometimes, especially with a stronger test flash which probably excited both centre and surround, the time 22
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CHRISTINA ENROTH-CUGELL AND OTHERS 584 course of the response changed with background size. Some examples of this are shown in Fig. 2. Fig. 2A and B show responses to a moderately intense (108 quanta (507)/deg2 sec, incident on the retina) spot, 0.180 in diameter, which was presented upon a background 30 in diameter, chosen to cover just the
M- Flashing
[--laSteady
I,0.18°
AA
~~~~~~~~~~301
J
B A
50
impulses/sec 110
1 Zero impulses/sec Fig. 2. The interaction between stimulus strength and background size. A and B, responses to a strong stimulus spot (108 quanta/deg2 see), 0.180 in diameter, presented respectively on a background equal in size to the central summing area and on one which covered the whole receptive field. Background illumination in both cases was 2-4 x 105 quanta/deg2 sec. On the larger background the response was more sustained and the discharge recovered more slowly following stimulus offset. C and D, responses to a weaker stimulus (2-5 x 107 quanta/deg2 see) on the same two backgrounds as before. Note how little the time course of the small responses depended on background size. On centre X-cell, 5/2; central summing area 6 deg2.
receptive field middle, and upon one 11° in diameter. On the smaller background the response showed clear evidence of surround antagonism: the peak discharge decayed to a mean rate lower than that just before stimulus onset, and at stimulus offset there was only a brief dip in discharge. On the larger background the same stimulus caused a slightly higher peak discharge and more extra impulses, and after the drop in firing at stimulus offset there was a slow recovery. These differences in response pattern suggest that expansion of the background light-adapted
SURROUND CONTRIBUTION TO LIGHT ADAPTATION 585 the surround, making it less able to suppress firing during presentation of the test spot, and less able to excite the cell at stimulus offset, but similar changes might have occurred had the centre become more sensitive. The latter possibility is hard to reconcile with the observations of Fig. 2C and D. There are shown, for the same unit and the same backgrounds, responses to weaker test spots which would be expected to excite the surround less. Now the response on the smaller background shows little evidence of surround antagonism and the difference between the pulsedensity tracings is slight. Had steady illumination of the surround enhanced centre sensitivity, it should have altered large and small responses alike. Apparently it influences only the surround's sensitivity. Jso impulses/sec
C
A
~~~~~~~~~~H
,_
5 , D25 sec_
- | ^
Zero impulses/sec
B
C and D
Flashing Steady Fig. 3. The effect of steady annular illumination upon sensitivity. A, __-
a
1° test spot (retinal illumination 2-5 x 106 quanta/deg2 see) was superimposed upon a steady adapting spot 1*6' in diameter which produced an illumination of 2.4 x 106 quanta/deg2 sec. In B, an annulus (70 inner, 120 outer diameter, illumination 1-3 x 106 quanta/deg2 see) was added to this arrangement. It barely altered the response. C and D, same configurations as in A and B, but with a stronger stimulus (106 quanta/deg2 sec). Their effects are compared in the lower part of the Figure; plainly the addition of the annulus in D enhanced the response. X-cell, 6/11, central summing area 1 deg2.
Dependence upon background configuration. We were interested to know if our findings depended upon the use of a uniform disk as a background, so in the following experiments another background configuration was used. First, a steady adapting spot of area less than At was centred upon the receptive field and the luminance of a small central test spot was adjusted to cause a weak response, apparently lacking surround antagonism (Fig. 3 A). Then to this configuration was added a steady annulus of inner diameter 70 and outer diameter 120 and the stimulus used before was 22-2
CHRISTINA ENROTH-CUGELL AND OTHERS presented (Fig. 3B). It left the response practically unchanged. However, with the same steady adapting spot, if the stimulus was made stronger (Fig. 3C), so as to increase the likelihood of surround involvement in the response, the addition of the same annulus as before (Fig. 3D) caused a 586
Flashing A
1.
-
-
H 0.450
Steady
I_
I
I
Iq
I
F-\ I,.-.
I0 impulses/sec
-.`
ri....... -1
AandC
Fig. 4. Effect of annular illumination on a small mixed response. A, a steady background of 1-5 x 106 quanta/deg2 sec, 0 450 in diameter was centred upon the receptive field and a test spot of the same size (at 1-5 x 105 quanta/deg2 see) was superimposed on it. In B an annulus of inner diameter 4.50, outer diameter 120 was added at a steady retinal illumination of 5-1 x 103 quanta/ deg2 sec, and in C annulus illuminance was increased to 5 x 104 quanta/deg2 sec. There was a progressive change in the time course of response as annular illumination was increased, which can be seen most clearly from the comparison of A and C in the lower part of the figure. Probably a Ycell, 41/8. The central summing area was 12 deg2, and its diameter is marked by the bar under the stimulus profile in C.
big increase in discharge. The changes in discharge brought about by adding the annulus, and their dependence upon the size of the response to the test flash, match well the changes observed in the corresponding experiments using uniform backgrounds (Fig. 2). Background configuration thus appears to be of little importance in these experiments. Steady illumination of the surround affects only mixed responses from centre and surround, but these responses need not always be large. Fig. 4 shows how, with centre sensitivity heavily depressed by the adapting spot, even a weak response may involve the surround, and how surround antagonism is progressively diminished by brighter annuli.
SURROUND CONTRIBUTION TO LIGHT ADAPTATION
587
DISCUSSION
These experiments examined the conditions under which steady illumination of the receptive field periphery alters a ganglion cell's sensitivity to a stimulus presented to the centre. We have shown that only when the stimulus is strong and/or the sensitivity of the centre is depressed by an adapting spot, does steady surround illumination perceptibly alter the response of the ganglion cell. The increase in discharge which appears under these conditions reflects the removal by light-adaptation of the surround's antagonistic response to the test stimulus; it is not the consequence of enhanced centre sensitivity. Choice of sensitivity measure. Had we chosen a criterion for sensitivity which was weighted more in favour of the slow components of ganglion cell response, we would have found often that sensitivity to a small spot depended upon steady illumination of the surround (Figs. 3 and 4). Perhaps this is why Maffei (1968) found that the response to modulation of a spot presented to the receptive field centre was enhanced by steady illumination of the surround, and why Nakayama (1971) found in units of the lateral geniculate nucleus that steady surround illumination increased sensitivity to a small flash. By using response measures which are sensitive to the slower components of discharge, and therefore to time-modulated surround activity, one may be led erroneously to conclude that steady illumination of the surround influences centre sensitivity. Slow components of discharge are probably relevant for some aspects of visual performance, but in trying to understand how centre sensitivity is controlled, peak discharge rate is the most suitable measure of response. Relation to previous work. Earlier work from this laboratory (Cleland & Enroth-Cugell, 1968; Enroth-Cugell & Shapley, 1973) suggested that the sensitivity of the centre was uninfluenced by steady light falling upon the periphery. The present experiments more firmly established this idea, for we used backgrounds and annuli so large that the surround had every opportunity to alter centre sensitivity were it capable of doing so. These backgrounds and annuli apparently caused a steady input from the surround, for they depressed the maintained discharge. Work broadly in agreement has been described by Sakmann, Creutzfeldt & Scheich (1969). Linearity of centre-surround interaction. Since steady signals from the surround have no influence upon the centre's sensitivity to flashes, these signals can only subtract from, or add to, signals from the centre. A number of observations suggest that transient signals from the two mechanisms also subtract arithmetically, and some are described in the preceding paper (Enroth-Cugell & Lennie, 1975). There it was shown that
588 88CHRISTINA ENROTH-CUGELL AND OTHERS an annulus of constant luminance, when flashed together with a concentric small spot, decreases the response to the spot by a constant amount which is independent of spot luminance. From different experiments Maffei & Cervetto (1968) and Enroth-Cugell & Pinto (1972) also have concluded that centre and surround signals interact linearly.
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 Hoffmann-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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