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Comparison of signal and adaptive sensitivity profiles of the surround mechanism of cat retinal ganglion cells
EXPERIMENTAL
NEUROLOGY
87,46-57
(1985)
Comparison of Signal and Adaptive Sensitivity Profiles of the Surround Mechanism of Cat Retinal Ganglion Cells H. I. COHEN, R. W. WINTERS, T. W. ROBERTSON, AND W. G. CHRISTEN’ Department of Psychology, University Palmer Eye Institute, University Received
April
of Miami. Coral Gables, Florida 33124 and Bascom of Miami School of Medicine, Miami, Florida 33152
12, 1984; revision
received
August
15, 1984
Signal and adaptive sensitivity profiles of the surrounds of cat retinal ganglion cells were determined by varying the position of concentric annuli whose outside and inside diameters varied but whose total area remained constant. Signal sensitivity profiles were determined by adjusting the luminances of these annuli so as to produce a weak suprathreshold response of constant magnitude and time course. Adaptive sensitivity profiles were determined by varying the luminances of concentric equalarea, unmodulated annuli until the response to a temporally modulated annulus attained a criterion level. The results provided evidence that the retinal region over which the surround mechanism of an X cell pools adaptive information and pools signals are the same, and that the distribution of adaptive and signal sensitivities within these regions is similar. A small number of X cells showed local adaptation effects. The adaptive pooling area appeared to be smaller than the signal pooling area for Y Ceh. 0 1985 Academic PKZS, Inc. INTRODUCTION
The neural discharge of the retinal ganglion cell, the output neuron of the retina, reflects the activity of neural response mechanisms within the retina. Ganglion cells with concentric receptive fields ( 10) are believed to be influenced by the activity of two response mechanisms: one that predominates in the center of their receptive fields, the center response mechanism, and one that predominates in the receptive field periphery, the surround mechanism (14, 18, 20). Hochstein and Shapley ( 11) suggested ’ We thank Mr. 0. Navarro for his invaluable technical assistance. We are also grateful to David Wolff for the statistical analysis. This research is supported by U.S. Public Health Service grant EY 00701. Please send all correspondence to Dr. Ray Winters, Dept. of Psychology, University of Miami, Coral Gables, Florida 33 124. 46 0014-4886/85 $3.00 Copyright Q 1985 by Academic Press, Inc. All rights of reproduction in any form reserved.
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that a third mechanism, the nonlinear subunit, is involved in the control of the responses of Y cells. One factor that influences the magnitude of the signal sent to the ganglion cell by a response mechanism is the adaptation state of that mechanism. Steady illumination of portions of the receptive field renders the response mechanism less sensitive to modulated photic stimuli. Rushton ( 15) proposed that the desensitizing effects of unmodulated illumination in the visual field are spatially integrated within the retina. The neural substrate, the adaptive pool, was thought to cause a desensitization to regions in the visual field not directly stimulated by the adapting flux. There is evidence that both the center response mechanism (2, 3, 5, 13, 16, 17) and the surround mechanism (6) have adaptation pools. Furthermore, there is a substantial body of literature [6), for example] which has demonstrated that both retinal response mechanisms also spatially integrate signals generated by temporally modulated light: each response mechanism has a signal pool. Because both signals and adaptation are pooled physiologically by retinal response mechanisms, it is natural to query the relationship between the retinal circuitry underlying the two summation pools. In the rat, frog, and goldfish, the retinal region over which the center mechanism integrates signals, the signal pooling areu, is larger than the region over which the center mechanism integrates adaptive information, the adaptive pooling area (2, 5, 13, 17). In the cat the two pooling areas are the same size (3,8, 16). Moreover, the spatial distribution of adaptive and signal sensitivities within these regions are essentially the same (9). We sought to determine the size relationship between the signal and adaptive pooling areas of the surround response mechanism of cat retinal ganglion cells. It was also our intent to compare the spatial distribution of sensitivities within the two summing areas. The results provided evidence that for X cells, the surround integrates signals and adaptation over the same retinal region and, further, the spatial distribution of adaptive and signal sensitivity is very similar for these cells. MATERIALS
AND
METHODS
Preparation. Sodium pentobarbital (Nembutal, 35 mg/kg) was used to anesthetize the cats during surgery. Surgery included cannulation of the femoral vein and artery, a tracheotomy, a bilateral cervical sympathectomy, and a craniotomy. A light level of anesthesia was maintained during the experiments by continuously infusing urethane (40 mg/kg/h). The cannula in the femoral vein was used to infuse a mixture of urethane, gallamine triethiodide (Flaxedil, 40 mg/h), Ringer’s solution with lactate (3.0 ml/h), and atropine sulfate (0.05 ml/h). The EKG and EEG were
48
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monitored continuously and were used to assure the experimenters that the animals were not experiencing pain. The eyelids were sutured open and an intramuscular injection of ampicillin ( 12.5 mg/kg) was administered to diminish the possibility of infection. One drop each of atropine sulfate, to dilate the pupils, and neosynephrine, to retract the nictitating membranes, were placed on both eyes. To prevent cornea1 clouding, the cats were fitted with contact lenses. The lenses had 3.8-mm artificial pupils to improve the quality of the retinal images. Retinoscopy was carried out and the eyes appropriately refracted to focus on a translucent tangent screen positioned 120 cm in front of the cat. The animals were artificially ventilated by a Harvard Apparatus respiration pump. The stroke volume was between 30 and 40 cm3, and stroke rates averaged 25/min, according to the weight of the animal. Body temperature, Pco,, and femoral arterial blood pressure were monitored continuously. Body temperature was maintained at 38°C and PCO, between 4 and 5%. Recordings were discontinued if mean arterial blood pressure decreased to less than 80 mm Hg. Recording. Action potentials of 68 optic tract fibers in adult cats were monitored with tungsten microelectrodes. The recording system was a conventional one. Standard square wave pulses from a window discriminator were triggered by the action potentials. These standard pulses were fed to a loudspeaker to facilitate mapping of receptive fields. The pulses were also recorded on one channel of an Ampex analogue tape deck. The other channels of the tape deck were used for recording action potentials, voice commentary, and a stimulus marker. A trigger pulse, together with the standard pulses, was fed to a Texas Instrument 960A computer, which was programmed to give average response histograms, as well as a digital readout of the spike counts; bin size was 10 ms. All stimuli had a duration of 500 ms at 0.3 Hz. Each stimulus was repeated 20 times. The time course of the averaged responses to various stimuli could be compared by superimposing (on an oscilloscope) the average response histograms that were stored in computer memory. The magnitude of the responses to the stimuli were measured by examining digital printouts from the computer or those stored on magnetic tape. When maximum firing rate was estimated (see Fig. 2) it was measured during a IO-ms interval of the off-discharge for on-center cells and during a IO-ms interval of the on-discharge for off-center cells. Cell Classification. An 8” bipartite stimulus whose contrast reversed every 0.5 s was used to classify the cells as type X or Y. The X cells show linear spatial summation so there is a position in the receptive field where the response to the bipartite stimulus is “nulled” (7, 11). The Y cells do not show linear spatial summation and there is no “nuil” position in their
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receptive fields. Contrast, defined as (L,,, - L&/(&x + Z&i,) was 33% for this stimulus and the contrast reversal was sine-wave modulated in time. Cells classified in this manner could also be distinguished by their responses to a small (0. I”), unmodulated luminous spot in the receptive field. The X cells had a maintained response to this standing contrast and Y cells had a transient response. The X and Y cells also were distinguished by their responses to a drifting grating: Y cells showed an elevation of average firing to a drifting grating of high spatial frequency but X cells did not. Stimuli. Stimuli were presented on a translucent tangent screen by a three-channel rear projection optical system. The stimuli were projections of metal slides or transparencies (Kodalith-Ortho, type 3) placed in the optical channels. The dark portion of the transparencies was covered with an opaque paint to ensure that light was transmitted only through the clear portion of the transparencies. Quartz-iodide lamps (150 W) were used as light sources. The steady background illumination of the screen was provided by a Kodak projector placed above and behind the cat. All stimuli and background illumination could be selectively attenuated by neutral density filters. Flashing stimuli were square-wave modulated in time. RESULTS Adaptive and signal sensitivity profiles were determined in order to assess the adaptive and signal pooling areas of the surround and to assess the spatial distribution of sensitivity within these regions. The analysis was restricted to the periphery of the receptive field even though the surround mechanism may be affected by illumination of the receptive field center. Modulated stimuli at or near the receptive field center produce responses which show a clear contribution from the center response mechanism. It was our intent to study only pure surround responses. For the purpose of this study, a pure surround response is defined as one in which the time course of the response remained constant over a 0.9 log unit range of luminances, beginning at threshold luminance. Threshold luminance is defined as the lowest luminance at which the average response histogram to the stimulus was clearly different from the histogram obtained when no stimulus was presented. In general this method of defining threshold agreed with the threshold obtained by listening to the audio monitor for changes from background activity. The method of obtaining pure surround responses is that described by Bishop and Rodieck (1). With this method, the luminance and size of a field adapting spot, positioned in the center of the receptive field, is varied until a pure surround response is generated by a modulated stimulus in the periphery of the receptive field. The purpose of the adapting spot is to desensitize the center mechanism.
50
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After mapping the receptive field with a small luminous spot on the tangent screen, the cell was classified as type X or type Y; all receptive fields were within 20% of the area centralis. Signal sensitivity profiles were then determined. The stimuli were annuli with variable inside and outside diameters but whose total area remained constant, and was centered with respect to the receptive field center. Signal sensitivity profiles were determined by adjusting the luminance of each (temporally) modulated annulus so as to produce a weak surround response (peak firing rate between 20 and 70 spikes/s) of constant magnitude and time course-the criterion response. The relation between the position of the annulus (diameter of the annulus) and the log of the reciprocal of the luminance required for the cell to yield the criterion response defines the signal sensitivity profile. The adaptive sensitivity profiles were measured in the following manner. First, the criterion response was produced by a modulated annulus in the receptive field surround. The luminance of this annulus was then increased by 0.7 log units so that the ganglion cell yielded a surround response that was considerably larger in magnitude than the criterion response. Next, an unmodulated field adapting annulus was positioned in the receptive field surround and its luminance adjusted until the criterion response was produced. This procedure was repeated for a series of adapting annuli to measure the adaptive spread function. The field adapting annuli were the same stimuli used in the signal sensitivity study. The adaptive sensitivity profile, then, is defined by the relation between annulus position (diameter) and the log of the reciprocal of the luminance required to produce the criterion response. Adaptive and signal sensitivity curves were obtained from 17 X cells (15 on-center and 2 off-center) and 15 Y cells (12 on-center and 3 off-center). Recordings were made from an additional 16 Y cells but it was not possible to isolate their surround mechanisms so the experiment was discontinued on those cells. We found no obvious difference between the receptive properties of Y cells whose surrounds could be isolated and those whose surrounds could not be isolated. The results for a typical X cell are shown in Fig. IA. As seen, the adaptive and signal sensitivity profiles were very similar; two Y cells showed similar results. Thirteen of the 15 Y cells showed profiles similar to those shown in Fig. 1B. For these cells the adaptive spread function was narrower than the signal spread function. A correlation analysis did not reveal a difference in the average slope (0.28 and 0.25) of the descending portion of the two sensitivity profiles (t = 1.31, P > 0.1) for the 17 X cells tested or the 15 Y cells (0.25 and 0.29) tested (t = 1.4, P > 0.1). The annuli chosen for this experiment and described in the remainder
ADAPTATION
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1.2 -
X-cell 0~~~~~~~0 Signal Sign01 .--a
Adoptive
0.8 -
-
0.4
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I 5 ?
I
L ’
1
I
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Y-cell 0..-0
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-.B
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l
.\*
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"k..._.,o,. Y.,
0.4
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.
"...o '... "4.
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2.0
Inside
diameter
-"a.' 4.0
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: 6.0
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FIG. 1. Signal and adaptive sensitivity profiles. Insert shows superimposed average response histograms for an X cell (upper tracings) and a Y cell (lower tracing) for the criterion responses for stimuli with inside diameters of 2.1, 3.0, and 4.2”. Response bar represents 50 spikes/s. Stimuli: A-on-center X cell, luminance of 0.3” central adapting spot, 12 candles/m2; luminance of 3.0” X 4.0” (inside diameter of 3.0” and outside diameter of 4.0”), modulated annulus for adaptation study, 3.2” X IO-’ candles/m*; background luminance, 3.6” X W4 candles/m*. B-on-center Y cell, 1.0” central adapting spot luminance, 0.83 candles/m2; luminance of 3.0” X 4.0” modulated annulus for adaptation study, 6.8 X IO-’ candles/m*; background luminance, 3.6 X 1O-4 candles/m’; ah modulated stimuli had a duration of 500 ms at 0.3 Hz.
of the paper were those that elicited a response that was uncontaminated by the center mechanism at the luminances that produced criteria responses. The locus of the abscissa intercept of the signal and adaptive curves were also compared. The abscissa intercept is defined as the point at which the
52
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least square line, fitted to the descending part of the curve, crossed the abscissa. For X cells the average values for abscissa intercepts of the signal and adaptation profiles were 5.8 and 5.9”, respectively; these values are not statistically different (t = 0.7; P > 0.4). For Y cells these values were 5.2 and 6.7” for the signal and adaptation profiles, respectively, and the mean value for the adaptation profile was found to be significantly (t = 4.35; P < 0.001) smaller than the value for the signal profile. In addition, the value for the signal profile was found to be significantly smaller for X cells than for Y cells (t = 2.67; P < 0.01). This was found not to be the case for the abscissa intercepts of the two adaptation profiles (t = 0.08; P > 0.4). These fundamental differences between X and Y cells are also seen by examining the response functions in Fig. 2. This figure illustrates the effect of variations in annulus position (diameter) on the peak firing rate (during a lo-ms period) of an off-center X cell (A) and an off-center Y cell (B). The open symbols show how variations in the position of modulated annuli of equal flux alter the peak discharge rate of these cells. The same set of annuli were used as field adapting targets and their effects upon the response to a modulated annulus is shown by the closed symbols. The Y cell shown in the figure is one in which the peripheral extent of the surround’s adaptation profile, as assessed by the location of abscissa intercept, was not as great as that of the signal profile. Tests for Local Adaptation. The similarity of the adaptive and signal sensitivity profiles provided evidence that the distribution of the sensitivities associated with the surround’s two summation pools coincided spatially in X cells and some Y cells. These findings, however, did not exclude the possibility that there were local adaptation effects in the periphery of the receptive field. To test further for local adaptation effects, two additional experiments were conducted. First, the adaptation profile was determined for test annuli situated in two different regions of the receptive field surround; the test annuli had the same total area. If there is local adaptation, the shape of the adaptive sensitivity profile should be dependent on the position of the test annulus: adaptive sensitivity should be disproportionately high in the region where the test and adapting targets spatially coincide. Data were obtained for 19 X cells and 12 Y cells. One of the X cells and 7 Y cells showed evidence for local adaptation. The X cells and 3 of the 7 Y cells had signal sensitivity profiles that were similar in shape and spatial extent to their adaptive sensitivity profiles. Figure 3 shows the results from an X cell (A) that did not show evidence for local adaptation and from a Y cell (B) that did show local adaptation effects. For the X cell, the adaptive profile was independent of the test annulus position but for the Y cell, the profile was clearly dependent on its position. Another way to test for local adaptation is to determine the signal
ADAPTATION
25
OF
53
SURROUND
-
2
2
4
Inside FIG. period). luminance 3.5”
2. Effect Stimuli: of
X 5.0”
of variations A-off-center modulated
modulated
unmodulated annuli X 10m4 candles/m’. luminance modulated annulus modulated
in
annulus
X cell. annuli for annulus
for
for adaptive B-off-center
of annuli for signal annulus for adaptation for
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of annulus
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maximum
0.6” central adapting spot signal curve 6.2 X 10.’
adaptation
curve. Y cell,
6
1.3
X lo-’
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luminance, candles/m’; candles/m’:
X IO-‘, candles/m’; background central adapting spot luminance,
5.1 X 10m2 6.4 X 10-l
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candles/m’; candles/m’;
luminance luminance
(during
a IO-ms
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of of
luminance, 3.6 1.6 candles/m’: of 3.0” X 5.0” of unmodulated
luminance 3.6 X 10m4 candles/m’. of 500 ms at 0.3 Hz.
All
sensitivity profile in the presence of an adaptation target. If there is local adaptation there should be a disproportionate decrease in sensitivity in the region of the adapting target. Two of the thirteen X cells tested in this experiment showed evidence of local effects, whereas 5 of the 10 Y cells tested did; the two X cells and 2 of the 5 Y cells had similar adaptive and signal sensitivity profiles. Figure 4 shows the results from an X cell (A) not
54
COHEN ET AL.
1.4
-
1.0
-
0.6
-
4 6 zL :
B
1.4
Y-cell 0%.
t
x.
'....
X.,
o---cl
2.2O
x 3.10
.-.
4.2’
X 4.7’
~. 3.0
2.0
Inside
dimeter
4.0
of annulus
5.0
6.0
Co)
FIG. 3. Effect of test target position on shape of adaptive sensitivity profile. Stimuli: A-oncenter X cell, 0.3” adapting spot luminance 62 candles/m*; background luminance, 9.7 X lo-’ candles/m2; both modulated test annuli had the same area. B-on-center Y cell, 1.3” adapting spot luminance, 56 candles/m2; background luminance, 8.7 X low3 candles/m*; both modulated annuli had the same area. Modulated annuli for X and Y cells had 500 ms duration at 0.3 Hz.
showing local adaptation and from a Y cell that did show local adaptation. The shape of the signal sensitivity profile was dependent on the presence of the adaptive target for the Y cell but not for the X cell. DISCUSSION Electrophysiological studies of retinal ganglion cells in a variety demonstrate that adaptive signals are pooled physiologically by mechanism. For cat retinal ganglion cells, the adaptive summing same size as its signal summing area (3, 9, 16) and the signal profile and adaptive sensitivity profiles for the center mechanism identical (9).
of animals the center area is the sensitivity are nearly
ADAPTATION
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OF SURROUND
Y-cell “...,
“._.,
“....o,
/\>
o---o
None
.-.
2.z”x
3.10
_,,_,,_ ‘..
-.._._, o... o... ‘...
o.-...., 0.6
\
‘\*
’
‘...,. . .. o,.
p,,, \
0.2 I 2.0 lnslde
I
I
3.0
4.0 dimeter
of annulus
,,, .\
““.?
“‘..,
1 1
.-0.-o .-0.-o II
5.0
6.0
Co)
FIG. 4. Effect of adapting annuli in the receptive field surround on the shape of the signal sensitivity profile. Stimuli: A-on-center X cell adapting annulus luminance, 1.6 X 10-l candles/m2; 0.9’ adapting spot luminance, 62 candles/m2; background luminance 9.7 X 10e3 candles/m2. B-on-center Y cell: adapting annulus luminance, 3.2 X 10e2 candles/m2; 1.2” luminance 1.3 candles/m2; background luminance, 3.6 X 10e4 candles/m2; modulated annuli for both X and Y cells had duration of 500 ms at 0.3 Hz.
Although the spatial relationship between the center mechanism’s adaptive and signal pooling areas are similar in the cat, this has not been found to be the case in other animals. In the goldfish (5), frog (2), and rat (8, 17), the adaptive sensitivity profile appears to be narrower than the signal sensitivity profile. This suggests that sensitivity changes produced by steady illumination occur at an earlier stage of processing in the retina than the point at which signals are summed (17). The results of the present study provide evidence that surround mechanisms of X and Y cells process adaptive information in very different ways. The X cell results are similar to those reported for the center mechanism of cat retinal ganglion cells in that the spatial distributions of signal
56
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sensitivity and adaptive sensitivity are very similar. The surrounds of most Y cells, in contrast, integrate adaptive information over a smaller retinal region than they pool signals. Are There Adaptive Subunits within the Surround’s Adaptation Pool? Harding (9), in his studies of field adaptation within the center mechanism of cat retinal ganglion cells, found evidence for local adaptation subunits within the center’s adaptive pooling area. He inferred from those results that there are two stages of adaptation for the center mechanism, one which is restricted to or near the site of the adapting target, and one in which adaptive signals are physiologically pooled before reducing the sensitivity of the center mechanism. Two tests for local adaptation effects were made in our study (see Figs. 3 and 4) and it is of some theoretical significance that many of the X and Y cells that showed local adaptation had signal and adaptive sensitivity profiles that were similar. These findings may be interpreted as evidence for more than one stage of adaptation within the surround mechanism. It is important to point out that the results of our tests for local adaptation do not exclude the possibility that most, or all X and Y cells have adaptation subunits. The sensitivity per unit of the surround mechanism is low relative to the center mechanism so it is necessary to use relatively large targets in order to stimulate the surround mechanism at luminances that do not produce a significant amount of stray light. Thus, small adaptation subunits may go undetected. There is a substantial amount of evidence from studies of other animals that individual photoreceptors have adaptation mechanisms [e.g., (4, 12, 19)]. If this were true for cat photoreceptors, the methods used here certainly would not have revealed these adaptation subunits or, for that matter, small subunits resulting from interactions among receptors or from horizontal and/or amacrine cells with small receptive fields. REFERENCES 1. BISHOP, P. O., AND R. W. RODIECK. 1965. Proceedings of the Symposium on Information Processing in Sight Sensory Systems, 116-127, California Institute of Technology, Pasadena, CA. 2. BURKHARDT, D. A., AND G. G. BERNSTON. 1977. Light adaptation and excitation: lateral spread of signals within the frog retina. Vision Res. 12: 1095-l 111. 3. CLELAND, B. G., AND C. ENROTH-CUGELL. 1968. Quantitative aspects of sensitivity and summation in the cat retina. J. Physiol. (London) 198: 17-38. 4. DOWLLNG, J. E., AND H. RIPPS. 1971. S-potentials in the skate retina: intracellular recordings during the light dark adaptation. J. Gen. Physiol. 58: 163-189. 5. EASTER, S. W. 1968. Adaptation in the goldfish retina. J. Physiol. (London) 195: 273-28 1. 6. ENROTH-CUGELL, C., AND L. H. PINTO. 1972. Properties of the surround mechanisms of cat retinal ganglion cells and center-surround interactions. J. Physiol. (London) 220: 403-440.
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7. ENROTH-CUGELL, C., AND J. G. ROBSON. 1966. The contrast sensitivity of retinal ganglion cells of the cat. J. Physiol. (London) 187: 517-522. 8. GREEN, D. G., L. TONG, AND C. M. CICERONE. 1977. Lateral spread of light adaptation in the rat retina. Vision Res. 17: 479-486. 9. HARDING, T. 1977. Field Adaptation and Signal Summation within the Receptive Field Center of Cat Retinal Ganglion Cells. Ph.D. Dissertation, Purdue University. 10. KUFFLER, S. W. 1953. Discharge patterns and functional organization of mammalian retina. J. Neurophysiol. 16: 37-68. 11. HOCHSTEIN, S. AND R. M. SHAPLEY. 1976. Quantitative analysis of retinal ganglion cell classifications. J. Physiol. (London) 262: 237-264. 12. H~KID, D. C., AND P. A. HOCK. Recovery of cone receptor activity in the frog’s isolated retina. Vision Res. 13: 1843-1951. 13. LIPETZ, L. E. 1961. A mechanism of light adaptation. Science 155: 639-640. 14. RODIECK, R. W., AND J. STONE. 1965. Analysis of receptive fields of cat retinal ganglion cells. J. Neurophysiol. 28: 833-849. 15. RUSHTON, W. A. H. 1965. The Ferrier lecture, 1962, visual adaptation. Proc. R. Sot. Bit. 162: 20-46.
16. SAKMANN, B., 0. CREUTZFELDT, AND H. SCHEICH. 1969. An experimental comparison between the ganglion cell receptive field and the receptive field of the adaptation pool. P/liigers Arch. 307: 133-l 37. 17. TONG, L. AND D. G. GREEN. 1977. Adaptation pools and excitation receptive fields of retinal ganglion cells. Vision Res. 17: 1233-1236. 18. WAGNER, J. G., E. F. MACNICHOL, AND M. L. WOLBARSHT. 1963. Functional basis for on-center and off-center receptive fields in the retina. J. Opt. Sot. Am. 53: 66-70. 19. WITKOWSKY, P., J. NELSON, AND H. RIPPS. 1973. Spectral properties of the isolated receptor potential of the carp retina. J. Gen. Physiol. 61: 401-423. 20. WUI-~KE, W., AND 0. J. GRUSSER. 1966. Die funktionelle Organization der rezeptiven Felder von On-Centrum-Neuronen der Katzenretina. Pfiigers Arch. 289: 83.
NEUROLOGY
87,46-57
(1985)
Comparison of Signal and Adaptive Sensitivity Profiles of the Surround Mechanism of Cat Retinal Ganglion Cells H. I. COHEN, R. W. WINTERS, T. W. ROBERTSON, AND W. G. CHRISTEN’ Department of Psychology, University Palmer Eye Institute, University Received
April
of Miami. Coral Gables, Florida 33124 and Bascom of Miami School of Medicine, Miami, Florida 33152
12, 1984; revision
received
August
15, 1984
Signal and adaptive sensitivity profiles of the surrounds of cat retinal ganglion cells were determined by varying the position of concentric annuli whose outside and inside diameters varied but whose total area remained constant. Signal sensitivity profiles were determined by adjusting the luminances of these annuli so as to produce a weak suprathreshold response of constant magnitude and time course. Adaptive sensitivity profiles were determined by varying the luminances of concentric equalarea, unmodulated annuli until the response to a temporally modulated annulus attained a criterion level. The results provided evidence that the retinal region over which the surround mechanism of an X cell pools adaptive information and pools signals are the same, and that the distribution of adaptive and signal sensitivities within these regions is similar. A small number of X cells showed local adaptation effects. The adaptive pooling area appeared to be smaller than the signal pooling area for Y Ceh. 0 1985 Academic PKZS, Inc. INTRODUCTION
The neural discharge of the retinal ganglion cell, the output neuron of the retina, reflects the activity of neural response mechanisms within the retina. Ganglion cells with concentric receptive fields ( 10) are believed to be influenced by the activity of two response mechanisms: one that predominates in the center of their receptive fields, the center response mechanism, and one that predominates in the receptive field periphery, the surround mechanism (14, 18, 20). Hochstein and Shapley ( 11) suggested ’ We thank Mr. 0. Navarro for his invaluable technical assistance. We are also grateful to David Wolff for the statistical analysis. This research is supported by U.S. Public Health Service grant EY 00701. Please send all correspondence to Dr. Ray Winters, Dept. of Psychology, University of Miami, Coral Gables, Florida 33 124. 46 0014-4886/85 $3.00 Copyright Q 1985 by Academic Press, Inc. All rights of reproduction in any form reserved.
ADAPTATION
OF
SURROUND
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that a third mechanism, the nonlinear subunit, is involved in the control of the responses of Y cells. One factor that influences the magnitude of the signal sent to the ganglion cell by a response mechanism is the adaptation state of that mechanism. Steady illumination of portions of the receptive field renders the response mechanism less sensitive to modulated photic stimuli. Rushton ( 15) proposed that the desensitizing effects of unmodulated illumination in the visual field are spatially integrated within the retina. The neural substrate, the adaptive pool, was thought to cause a desensitization to regions in the visual field not directly stimulated by the adapting flux. There is evidence that both the center response mechanism (2, 3, 5, 13, 16, 17) and the surround mechanism (6) have adaptation pools. Furthermore, there is a substantial body of literature [6), for example] which has demonstrated that both retinal response mechanisms also spatially integrate signals generated by temporally modulated light: each response mechanism has a signal pool. Because both signals and adaptation are pooled physiologically by retinal response mechanisms, it is natural to query the relationship between the retinal circuitry underlying the two summation pools. In the rat, frog, and goldfish, the retinal region over which the center mechanism integrates signals, the signal pooling areu, is larger than the region over which the center mechanism integrates adaptive information, the adaptive pooling area (2, 5, 13, 17). In the cat the two pooling areas are the same size (3,8, 16). Moreover, the spatial distribution of adaptive and signal sensitivities within these regions are essentially the same (9). We sought to determine the size relationship between the signal and adaptive pooling areas of the surround response mechanism of cat retinal ganglion cells. It was also our intent to compare the spatial distribution of sensitivities within the two summing areas. The results provided evidence that for X cells, the surround integrates signals and adaptation over the same retinal region and, further, the spatial distribution of adaptive and signal sensitivity is very similar for these cells. MATERIALS
AND
METHODS
Preparation. Sodium pentobarbital (Nembutal, 35 mg/kg) was used to anesthetize the cats during surgery. Surgery included cannulation of the femoral vein and artery, a tracheotomy, a bilateral cervical sympathectomy, and a craniotomy. A light level of anesthesia was maintained during the experiments by continuously infusing urethane (40 mg/kg/h). The cannula in the femoral vein was used to infuse a mixture of urethane, gallamine triethiodide (Flaxedil, 40 mg/h), Ringer’s solution with lactate (3.0 ml/h), and atropine sulfate (0.05 ml/h). The EKG and EEG were
48
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monitored continuously and were used to assure the experimenters that the animals were not experiencing pain. The eyelids were sutured open and an intramuscular injection of ampicillin ( 12.5 mg/kg) was administered to diminish the possibility of infection. One drop each of atropine sulfate, to dilate the pupils, and neosynephrine, to retract the nictitating membranes, were placed on both eyes. To prevent cornea1 clouding, the cats were fitted with contact lenses. The lenses had 3.8-mm artificial pupils to improve the quality of the retinal images. Retinoscopy was carried out and the eyes appropriately refracted to focus on a translucent tangent screen positioned 120 cm in front of the cat. The animals were artificially ventilated by a Harvard Apparatus respiration pump. The stroke volume was between 30 and 40 cm3, and stroke rates averaged 25/min, according to the weight of the animal. Body temperature, Pco,, and femoral arterial blood pressure were monitored continuously. Body temperature was maintained at 38°C and PCO, between 4 and 5%. Recordings were discontinued if mean arterial blood pressure decreased to less than 80 mm Hg. Recording. Action potentials of 68 optic tract fibers in adult cats were monitored with tungsten microelectrodes. The recording system was a conventional one. Standard square wave pulses from a window discriminator were triggered by the action potentials. These standard pulses were fed to a loudspeaker to facilitate mapping of receptive fields. The pulses were also recorded on one channel of an Ampex analogue tape deck. The other channels of the tape deck were used for recording action potentials, voice commentary, and a stimulus marker. A trigger pulse, together with the standard pulses, was fed to a Texas Instrument 960A computer, which was programmed to give average response histograms, as well as a digital readout of the spike counts; bin size was 10 ms. All stimuli had a duration of 500 ms at 0.3 Hz. Each stimulus was repeated 20 times. The time course of the averaged responses to various stimuli could be compared by superimposing (on an oscilloscope) the average response histograms that were stored in computer memory. The magnitude of the responses to the stimuli were measured by examining digital printouts from the computer or those stored on magnetic tape. When maximum firing rate was estimated (see Fig. 2) it was measured during a IO-ms interval of the off-discharge for on-center cells and during a IO-ms interval of the on-discharge for off-center cells. Cell Classification. An 8” bipartite stimulus whose contrast reversed every 0.5 s was used to classify the cells as type X or Y. The X cells show linear spatial summation so there is a position in the receptive field where the response to the bipartite stimulus is “nulled” (7, 11). The Y cells do not show linear spatial summation and there is no “nuil” position in their
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receptive fields. Contrast, defined as (L,,, - L&/(&x + Z&i,) was 33% for this stimulus and the contrast reversal was sine-wave modulated in time. Cells classified in this manner could also be distinguished by their responses to a small (0. I”), unmodulated luminous spot in the receptive field. The X cells had a maintained response to this standing contrast and Y cells had a transient response. The X and Y cells also were distinguished by their responses to a drifting grating: Y cells showed an elevation of average firing to a drifting grating of high spatial frequency but X cells did not. Stimuli. Stimuli were presented on a translucent tangent screen by a three-channel rear projection optical system. The stimuli were projections of metal slides or transparencies (Kodalith-Ortho, type 3) placed in the optical channels. The dark portion of the transparencies was covered with an opaque paint to ensure that light was transmitted only through the clear portion of the transparencies. Quartz-iodide lamps (150 W) were used as light sources. The steady background illumination of the screen was provided by a Kodak projector placed above and behind the cat. All stimuli and background illumination could be selectively attenuated by neutral density filters. Flashing stimuli were square-wave modulated in time. RESULTS Adaptive and signal sensitivity profiles were determined in order to assess the adaptive and signal pooling areas of the surround and to assess the spatial distribution of sensitivity within these regions. The analysis was restricted to the periphery of the receptive field even though the surround mechanism may be affected by illumination of the receptive field center. Modulated stimuli at or near the receptive field center produce responses which show a clear contribution from the center response mechanism. It was our intent to study only pure surround responses. For the purpose of this study, a pure surround response is defined as one in which the time course of the response remained constant over a 0.9 log unit range of luminances, beginning at threshold luminance. Threshold luminance is defined as the lowest luminance at which the average response histogram to the stimulus was clearly different from the histogram obtained when no stimulus was presented. In general this method of defining threshold agreed with the threshold obtained by listening to the audio monitor for changes from background activity. The method of obtaining pure surround responses is that described by Bishop and Rodieck (1). With this method, the luminance and size of a field adapting spot, positioned in the center of the receptive field, is varied until a pure surround response is generated by a modulated stimulus in the periphery of the receptive field. The purpose of the adapting spot is to desensitize the center mechanism.
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After mapping the receptive field with a small luminous spot on the tangent screen, the cell was classified as type X or type Y; all receptive fields were within 20% of the area centralis. Signal sensitivity profiles were then determined. The stimuli were annuli with variable inside and outside diameters but whose total area remained constant, and was centered with respect to the receptive field center. Signal sensitivity profiles were determined by adjusting the luminance of each (temporally) modulated annulus so as to produce a weak surround response (peak firing rate between 20 and 70 spikes/s) of constant magnitude and time course-the criterion response. The relation between the position of the annulus (diameter of the annulus) and the log of the reciprocal of the luminance required for the cell to yield the criterion response defines the signal sensitivity profile. The adaptive sensitivity profiles were measured in the following manner. First, the criterion response was produced by a modulated annulus in the receptive field surround. The luminance of this annulus was then increased by 0.7 log units so that the ganglion cell yielded a surround response that was considerably larger in magnitude than the criterion response. Next, an unmodulated field adapting annulus was positioned in the receptive field surround and its luminance adjusted until the criterion response was produced. This procedure was repeated for a series of adapting annuli to measure the adaptive spread function. The field adapting annuli were the same stimuli used in the signal sensitivity study. The adaptive sensitivity profile, then, is defined by the relation between annulus position (diameter) and the log of the reciprocal of the luminance required to produce the criterion response. Adaptive and signal sensitivity curves were obtained from 17 X cells (15 on-center and 2 off-center) and 15 Y cells (12 on-center and 3 off-center). Recordings were made from an additional 16 Y cells but it was not possible to isolate their surround mechanisms so the experiment was discontinued on those cells. We found no obvious difference between the receptive properties of Y cells whose surrounds could be isolated and those whose surrounds could not be isolated. The results for a typical X cell are shown in Fig. IA. As seen, the adaptive and signal sensitivity profiles were very similar; two Y cells showed similar results. Thirteen of the 15 Y cells showed profiles similar to those shown in Fig. 1B. For these cells the adaptive spread function was narrower than the signal spread function. A correlation analysis did not reveal a difference in the average slope (0.28 and 0.25) of the descending portion of the two sensitivity profiles (t = 1.31, P > 0.1) for the 17 X cells tested or the 15 Y cells (0.25 and 0.29) tested (t = 1.4, P > 0.1). The annuli chosen for this experiment and described in the remainder
ADAPTATION
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1.2 -
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FIG. 1. Signal and adaptive sensitivity profiles. Insert shows superimposed average response histograms for an X cell (upper tracings) and a Y cell (lower tracing) for the criterion responses for stimuli with inside diameters of 2.1, 3.0, and 4.2”. Response bar represents 50 spikes/s. Stimuli: A-on-center X cell, luminance of 0.3” central adapting spot, 12 candles/m2; luminance of 3.0” X 4.0” (inside diameter of 3.0” and outside diameter of 4.0”), modulated annulus for adaptation study, 3.2” X IO-’ candles/m*; background luminance, 3.6” X W4 candles/m*. B-on-center Y cell, 1.0” central adapting spot luminance, 0.83 candles/m2; luminance of 3.0” X 4.0” modulated annulus for adaptation study, 6.8 X IO-’ candles/m*; background luminance, 3.6 X 1O-4 candles/m’; ah modulated stimuli had a duration of 500 ms at 0.3 Hz.
of the paper were those that elicited a response that was uncontaminated by the center mechanism at the luminances that produced criteria responses. The locus of the abscissa intercept of the signal and adaptive curves were also compared. The abscissa intercept is defined as the point at which the
52
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least square line, fitted to the descending part of the curve, crossed the abscissa. For X cells the average values for abscissa intercepts of the signal and adaptation profiles were 5.8 and 5.9”, respectively; these values are not statistically different (t = 0.7; P > 0.4). For Y cells these values were 5.2 and 6.7” for the signal and adaptation profiles, respectively, and the mean value for the adaptation profile was found to be significantly (t = 4.35; P < 0.001) smaller than the value for the signal profile. In addition, the value for the signal profile was found to be significantly smaller for X cells than for Y cells (t = 2.67; P < 0.01). This was found not to be the case for the abscissa intercepts of the two adaptation profiles (t = 0.08; P > 0.4). These fundamental differences between X and Y cells are also seen by examining the response functions in Fig. 2. This figure illustrates the effect of variations in annulus position (diameter) on the peak firing rate (during a lo-ms period) of an off-center X cell (A) and an off-center Y cell (B). The open symbols show how variations in the position of modulated annuli of equal flux alter the peak discharge rate of these cells. The same set of annuli were used as field adapting targets and their effects upon the response to a modulated annulus is shown by the closed symbols. The Y cell shown in the figure is one in which the peripheral extent of the surround’s adaptation profile, as assessed by the location of abscissa intercept, was not as great as that of the signal profile. Tests for Local Adaptation. The similarity of the adaptive and signal sensitivity profiles provided evidence that the distribution of the sensitivities associated with the surround’s two summation pools coincided spatially in X cells and some Y cells. These findings, however, did not exclude the possibility that there were local adaptation effects in the periphery of the receptive field. To test further for local adaptation effects, two additional experiments were conducted. First, the adaptation profile was determined for test annuli situated in two different regions of the receptive field surround; the test annuli had the same total area. If there is local adaptation, the shape of the adaptive sensitivity profile should be dependent on the position of the test annulus: adaptive sensitivity should be disproportionately high in the region where the test and adapting targets spatially coincide. Data were obtained for 19 X cells and 12 Y cells. One of the X cells and 7 Y cells showed evidence for local adaptation. The X cells and 3 of the 7 Y cells had signal sensitivity profiles that were similar in shape and spatial extent to their adaptive sensitivity profiles. Figure 3 shows the results from an X cell (A) that did not show evidence for local adaptation and from a Y cell (B) that did show local adaptation effects. For the X cell, the adaptive profile was independent of the test annulus position but for the Y cell, the profile was clearly dependent on its position. Another way to test for local adaptation is to determine the signal
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Inside FIG. period). luminance 3.5”
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sensitivity profile in the presence of an adaptation target. If there is local adaptation there should be a disproportionate decrease in sensitivity in the region of the adapting target. Two of the thirteen X cells tested in this experiment showed evidence of local effects, whereas 5 of the 10 Y cells tested did; the two X cells and 2 of the 5 Y cells had similar adaptive and signal sensitivity profiles. Figure 4 shows the results from an X cell (A) not
54
COHEN ET AL.
1.4
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-
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-
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FIG. 3. Effect of test target position on shape of adaptive sensitivity profile. Stimuli: A-oncenter X cell, 0.3” adapting spot luminance 62 candles/m*; background luminance, 9.7 X lo-’ candles/m2; both modulated test annuli had the same area. B-on-center Y cell, 1.3” adapting spot luminance, 56 candles/m2; background luminance, 8.7 X low3 candles/m*; both modulated annuli had the same area. Modulated annuli for X and Y cells had 500 ms duration at 0.3 Hz.
showing local adaptation and from a Y cell that did show local adaptation. The shape of the signal sensitivity profile was dependent on the presence of the adaptive target for the Y cell but not for the X cell. DISCUSSION Electrophysiological studies of retinal ganglion cells in a variety demonstrate that adaptive signals are pooled physiologically by mechanism. For cat retinal ganglion cells, the adaptive summing same size as its signal summing area (3, 9, 16) and the signal profile and adaptive sensitivity profiles for the center mechanism identical (9).
of animals the center area is the sensitivity are nearly
ADAPTATION
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Y-cell “...,
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/\>
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.-0.-o .-0.-o II
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FIG. 4. Effect of adapting annuli in the receptive field surround on the shape of the signal sensitivity profile. Stimuli: A-on-center X cell adapting annulus luminance, 1.6 X 10-l candles/m2; 0.9’ adapting spot luminance, 62 candles/m2; background luminance 9.7 X 10e3 candles/m2. B-on-center Y cell: adapting annulus luminance, 3.2 X 10e2 candles/m2; 1.2” luminance 1.3 candles/m2; background luminance, 3.6 X 10e4 candles/m2; modulated annuli for both X and Y cells had duration of 500 ms at 0.3 Hz.
Although the spatial relationship between the center mechanism’s adaptive and signal pooling areas are similar in the cat, this has not been found to be the case in other animals. In the goldfish (5), frog (2), and rat (8, 17), the adaptive sensitivity profile appears to be narrower than the signal sensitivity profile. This suggests that sensitivity changes produced by steady illumination occur at an earlier stage of processing in the retina than the point at which signals are summed (17). The results of the present study provide evidence that surround mechanisms of X and Y cells process adaptive information in very different ways. The X cell results are similar to those reported for the center mechanism of cat retinal ganglion cells in that the spatial distributions of signal
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sensitivity and adaptive sensitivity are very similar. The surrounds of most Y cells, in contrast, integrate adaptive information over a smaller retinal region than they pool signals. Are There Adaptive Subunits within the Surround’s Adaptation Pool? Harding (9), in his studies of field adaptation within the center mechanism of cat retinal ganglion cells, found evidence for local adaptation subunits within the center’s adaptive pooling area. He inferred from those results that there are two stages of adaptation for the center mechanism, one which is restricted to or near the site of the adapting target, and one in which adaptive signals are physiologically pooled before reducing the sensitivity of the center mechanism. Two tests for local adaptation effects were made in our study (see Figs. 3 and 4) and it is of some theoretical significance that many of the X and Y cells that showed local adaptation had signal and adaptive sensitivity profiles that were similar. These findings may be interpreted as evidence for more than one stage of adaptation within the surround mechanism. It is important to point out that the results of our tests for local adaptation do not exclude the possibility that most, or all X and Y cells have adaptation subunits. The sensitivity per unit of the surround mechanism is low relative to the center mechanism so it is necessary to use relatively large targets in order to stimulate the surround mechanism at luminances that do not produce a significant amount of stray light. Thus, small adaptation subunits may go undetected. There is a substantial amount of evidence from studies of other animals that individual photoreceptors have adaptation mechanisms [e.g., (4, 12, 19)]. If this were true for cat photoreceptors, the methods used here certainly would not have revealed these adaptation subunits or, for that matter, small subunits resulting from interactions among receptors or from horizontal and/or amacrine cells with small receptive fields. REFERENCES 1. BISHOP, P. O., AND R. W. RODIECK. 1965. Proceedings of the Symposium on Information Processing in Sight Sensory Systems, 116-127, California Institute of Technology, Pasadena, CA. 2. BURKHARDT, D. A., AND G. G. BERNSTON. 1977. Light adaptation and excitation: lateral spread of signals within the frog retina. Vision Res. 12: 1095-l 111. 3. CLELAND, B. G., AND C. ENROTH-CUGELL. 1968. Quantitative aspects of sensitivity and summation in the cat retina. J. Physiol. (London) 198: 17-38. 4. DOWLLNG, J. E., AND H. RIPPS. 1971. S-potentials in the skate retina: intracellular recordings during the light dark adaptation. J. Gen. Physiol. 58: 163-189. 5. EASTER, S. W. 1968. Adaptation in the goldfish retina. J. Physiol. (London) 195: 273-28 1. 6. ENROTH-CUGELL, C., AND L. H. PINTO. 1972. Properties of the surround mechanisms of cat retinal ganglion cells and center-surround interactions. J. Physiol. (London) 220: 403-440.
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7. ENROTH-CUGELL, C., AND J. G. ROBSON. 1966. The contrast sensitivity of retinal ganglion cells of the cat. J. Physiol. (London) 187: 517-522. 8. GREEN, D. G., L. TONG, AND C. M. CICERONE. 1977. Lateral spread of light adaptation in the rat retina. Vision Res. 17: 479-486. 9. HARDING, T. 1977. Field Adaptation and Signal Summation within the Receptive Field Center of Cat Retinal Ganglion Cells. Ph.D. Dissertation, Purdue University. 10. KUFFLER, S. W. 1953. Discharge patterns and functional organization of mammalian retina. J. Neurophysiol. 16: 37-68. 11. HOCHSTEIN, S. AND R. M. SHAPLEY. 1976. Quantitative analysis of retinal ganglion cell classifications. J. Physiol. (London) 262: 237-264. 12. H~KID, D. C., AND P. A. HOCK. Recovery of cone receptor activity in the frog’s isolated retina. Vision Res. 13: 1843-1951. 13. LIPETZ, L. E. 1961. A mechanism of light adaptation. Science 155: 639-640. 14. RODIECK, R. W., AND J. STONE. 1965. Analysis of receptive fields of cat retinal ganglion cells. J. Neurophysiol. 28: 833-849. 15. RUSHTON, W. A. H. 1965. The Ferrier lecture, 1962, visual adaptation. Proc. R. Sot. Bit. 162: 20-46.
16. SAKMANN, B., 0. CREUTZFELDT, AND H. SCHEICH. 1969. An experimental comparison between the ganglion cell receptive field and the receptive field of the adaptation pool. P/liigers Arch. 307: 133-l 37. 17. TONG, L. AND D. G. GREEN. 1977. Adaptation pools and excitation receptive fields of retinal ganglion cells. Vision Res. 17: 1233-1236. 18. WAGNER, J. G., E. F. MACNICHOL, AND M. L. WOLBARSHT. 1963. Functional basis for on-center and off-center receptive fields in the retina. J. Opt. Sot. Am. 53: 66-70. 19. WITKOWSKY, P., J. NELSON, AND H. RIPPS. 1973. Spectral properties of the isolated receptor potential of the carp retina. J. Gen. Physiol. 61: 401-423. 20. WUI-~KE, W., AND 0. J. GRUSSER. 1966. Die funktionelle Organization der rezeptiven Felder von On-Centrum-Neuronen der Katzenretina. Pfiigers Arch. 289: 83.