li'sion Rcr. Vol. IS.pp. 1407-1410.Pergamon Press 1975.Printed in
Grmt Britain
RESEARCH NOTE GAIN
CONTROL
MECHANISMS WITHIN THE RECEPTIVE OF CAT’S RETINAL GANGLION CELLS’ HIDE-AKI
SAITO
Research Group on Auditory and Visual Infomation
FIELD
CENTER
and YOSHIRO FUUDA
Processing, NHK Broadcasting
Science Research Laboratories.
Setagaya-ku, Tokyo 157.Japan (Receiued
18 November
1974; in recisedform
1 Prhrunry 1975)
In the previous studies (Fukada, 1971; Fukada and Saito, 1971X the cat’s retinal ganglion cells have been classified into Type-I and Type-II, independently of
light (5’ dia) were presented on a tangent screen which was placed 1.37m in front of the cat’s eyes and illuminated at 59 cd/m2 by distant fluorescent tubes. The
on- or off-center subdivision, on the basis of the receptive field proper&s and the axonal conduction velocities. Since then, accumulated data by us (&to, Shimahara and F&da, 1970, 1971)and others (Cleland, Dubin and Levi& 1971; Hoflinann, Stone and Sherman, 1972; Ikeda and Wright, 1972; Cleland, Levick and San&son, 1973)suggest that our Type-I cells correspond to Y-cells of Enroth-Cugell and Robson (1966)and Type-II to X-&Is. In this paper, X/Y terminology will be used because of its familiarity. It was observed that the response of on-center Xcell to a flashing spot of light presented at the center of the receptive field (RF) was gradually suppressed with successive stimulation. The suppression of the response was aIso observed even when the preceding spots had been presented at a little diierent position of the center region. By contrast, the response of Ycell remained constant for the repetitive stimulation (Fukada, 1971).From these observations, some kind of inhibition is suggested to develop in the neuronal network which organizes the RF of Xcell with successive stimulation, and to spread over the RF center region. An inhibitory mechanism in Y-cell, if any, may be different. In the present study, the inhibitory processes caused by a flashing spot itself in the on-center fields of X- and Y-cells were investigated by two-spot experiment: Response to the RF-centered spot (test spot, TS) was measured when an additional spot (conditioning spot, CS) was presented in the same RF center region. Experiments were conducted on 13 adult cats anaesthetized with nitrous oxide and immobilized with gallamine triethiodide. Extracellular spikes were
TS was presented at the center of the RF (the most sensitive part of the center region) and CS was located 15’ eccentric to TS. The CS was still well within the center region of the RF. In some experiments, the positions of TS and CS were interchanged with essentially the same results. The CS was presented once every 12 set and lasted for 3 sec. The TS was flashed for 100 or 200 msec with a variable delay relative to the onset or the cessation of CS. The luminance of the spots of light, which were maximally available at 3.9 x ld and 6.8 x 103 cd/m2 for TS and CS respectively, were adjusted with neutral density filters so that an algebraic sum of the responses to TS and CS was well within the dynamic range of the cell’s response. To focus the spot stimuli on the retina and to keep high image quality, a contact lens (usually, + 10 D) with 4mm aperture was used. The magnitude of the test response (TR) was measured as follows. First, the averaged PST-histograms were obtained from 20 consecutive responses to TS alone, CS alone and to combined stimuli of TS and CS, respectively. They were expressed as the number of impulses for each bin (bin width was usually 20 msec). The maintained discharge rate averaged for 1 set prior to the presentation of TS alone was ’ expressed also in impulses/bin. The unconditioned TR was defined by a total number of impulses which were elicited by TS alone and exceeded the maintained discharge rate. When TS was combined with CS. the conditioned TR was obtained in the same way except that the maintained discharge rate was substituted by
recorded from the optic tract with tungsten microelectrodes. Spikes were fed to a Schmitt trigger circuit
PST-histograms
to CS alone.
Forty on-center cells were classitied as either X (20) or Y (20) depending on the two criteria. One criterion is the difference in the tonic (X) or phasic (Y) response profile of the cell to a long-lasting spot stimulus. The
1A preliminary report of this work was presented at XXVIICPS SatelliteSymposiumon Visionheld in Sydney.
other is the difference in the fine structure of the impulse train of the initial transient response to the stimulus onset; Y-cells have a clear discontinuity in their discharge rate between the initial burst and SUCceeding discharges whereas Xcells do not show such discontinuity (Saito et al.. 1970, 1971).It is worth noting that this difference in the initial transient part of response was so marked that it proved to be a good criterion for X/Y-classiication. For both types of cells, TR was suppressed by CS
October 1974.
presentation,
to produce pulses of standard width and amplitude. and those pulses were fed to a mini-computer (TOSBAC-3CHM, Toshiba) to compile the post-stimulus time histograms (PST-histograms). The TS and CS were produced from glow modulator tubes (Sylvania, R1131Q and those spots of
1407
but the time course of the suppression
Research
Note
XON
YON
lYJ.&-
(0)
(e)
i
(f)
I
,
I(h)
Time,
Time.
set
set
Fig. I. Two-spot experiments for a X-cell [(a)-(d)] and for a Y-cell [(e)-(h)]. PST-histograms show examples of response profiles to the test spot (TS. short bar under the histograms) and to the conditioning spot (CS, long bar). (a) and (e): TS was presented 2 set after on of CS. (b) and (f): TS alone. (c) and (8): TS, 2 set after @of CS. TS duration; 200 msec for the X-cell, 100 msec for the Y-cell. CS duration; 3 sec. Vertical calibration; 50 impulses/set. Bin width; 20 msec. (d) and (h): Time courses of the change of the magnitude of the test response (TR) caused by CS presentation for the X-cell and the Y-cell respectively. Abscissa: the time of the onset of TS relative to the onset of Cs (first zero) and to the cessation of CS (second zero). Ordinate: the magnitude of the conditioned TR expressed as a relative unit with respect to that of the unconditioned TR.
is remarkably different between X- and Y-cells as shown in Figs. l(d) (X) and (h) (Y). The TR of X-cell is suppressed progressively after the onset of CS, and within about 200 msec, TR reaches very low steady level. This suppression is maintained as long as CS continues, although a slight recovery can be seen. After the cessation of CS, TR recovers monotonically. In Y-cell, on the other hand, TR is suppressed immediately after the onset of CS, then within about 500 msec it recovers to some level which is still lower than the unconditioned TR. One of the most striking differences from X-cell is seen at the cessation of CS: Y-cell shows another transient suppression which is generally stronger than that observed at the onset of CS. The recovery from this suppression at of was often followed by a rebound. Then, an effect of the CS intensity upon the suppression of TR was studied. Figure 2 shows an example of Y-cell for which the time courses of the suppression are obtained for three CS intensities separated by 0.4 log step. The increase of CS intensity causes a general increase of the amount of TR-suppression: the transient suppressions at the onset and the cessation of CS are strengthened and the level to which TR recovers during CS presentation is also lowered. In X-cell as well, the only effect of increase of CS intensity was to strengthen the suppression. The general characteristics of the time course of the suppression in X/Y cells were respectively kept unchanged when the positions of ‘IS and CS were interchanged: X-cell showed sustained suppression concomitant with CS, while Y-cell showed transient suppressions at 011and ofof CS. As has been described, for both X- and Y-cells, excitatory input by flashing a spot of light in the RF-
(0)
I.9
YON
Time,
+-4,
0j -3
set
-2
-I
0
Fig. 2. Effects of CS intensity upon the time course of TR-suppression in a Y-cell. (a): Time courses of the change of the magnitude of the conditioned TR obtained under three CS intensities separated by 04 log unit as indicated on each curve. Abscissa and ordinate; same as in Fig. 1 except that the time scale of the transient parts after on and oflof CS are expanded. (b): Stimulus-response relations of the same cell to TS (filled circles) and to CS (open circles). Abscissa; intensity of TS and CS in log unit. Zero log unit corresponds 3.9 x IO” and 68 x IO3 cd/m’ for TS and CS respectively. Response magnitudes (impulses/ set) averaged over 100 msec after the stimulus onset for TS alone and CS alone under the same luminance conditions as in (a) are indicated by arrows.
I409
Research Note
center makes the excitatory effect of another spot of light in the same center region smaller than if this second stimulus were presented alone. Intrinsic properties of the ganglion cell membrane (Stone and Fabian. 1968) would account for some of the nonlinearity in the signal summation especially when the TS is presented concomitantly with the onset of CS in Y-cell. But the suppression in response to T’Sinversely correlates to the ongoing firing rate of X cell. If the non-linearity is located in the ganglion cell dendrites as suggested by Creutzfeldt, Sakmann, Scheich and Kom (1970). mo~hologi~l differences between X- and Y-cells claimed in recent studies (Fukuda and Stone, 1974; Boycott and W&ie. 1974)may provide us with some clue to account for the differences in the suppression of X/y-cells. However. the dendritic geometry of the ganglion cell would not be sufficient to explain the marked difference in the time course of suppression of X/y-cells. There is plenty of physiological and anatomical studies which suggest the pm-ganglionic interaction between two stimuli presented in the same RF center region. First, in the outer plexiform layer of the cat’s retina, a kind of neuronal adaptation which spreads laterally within the RF center has been suggested on the basis of the multi-spot experiments. assuming that a horizontal cell exerts an inhibitory influence either presy~pti~lly on the rotor-bills synapses (Bilttner and Grtlsser, 1968)or back on to receptors (Enroth-Cugell and Shapley, 1973). Enroth-Cugell and Shapley suggested such a feed-back gain control ~chanism from the results of a similar experiment to ours except that the two spots were presented concentrically at the center of RF under the scotopic a~p~tion state. The time course of the gain change in their Y-cell is apparently similar in general form to that of our X-cell. They have not reported on Xcell, and it is so far uncertain whether this discrepancy is due to the different stimulus conditions. As shown by Werbhn (1974) with intracellular study of bipolar and horizontal cells in the mudpuppy retina, horizontal cells in the cat’s retina may control the magnitude of the sustained depolarizing (hyperpolarizing) responses of the bipolar cells to the RFcentered stimulus indifferently to X/Y-classification.it is therefore likely that different gain control m~hanisms between X- and Y-cells may be found in the inner plexiform layer. In the inner piexifo~ layer, the dyad synapse, where the bipolar cell terminal makes contacts with two postsynaptic elements, is commonly associated with a reciprocal synapse from the amacrine to bipolar cell (Dowhng and Boycott. 1966; Dubin. 1970). If such a reciprocal synapse works as a negative feedback (Dowling, 1%7), the transmission of the SUStamed response of the bipolar cell to the ganglion cell will be further regulated. Suppose that the reciprocal inhibitory effect of the amacrine cell is not only confined to the dyad complex where the excitatory input caused by a spot of light is tr~nsmitt~. but also extends to the other synaptic sites where the processes of this cefi terminate. Then, another excitatory input which is caused by another spot of Iight in the same RF center region and which has arrived at those synaptic sites may also he subjected to the regulation of the same amacrine ceil. The marked
~~1~~~ ,#&enIn the inter-spike intervals of the sustained response of X-cell (Saito et al., 1971)suggests the above-mentioned feed-back mechanism. From the facts that the inter-spike intervals in the response of Y-cell are very irregular, and that the time course of the suppression in Y-cell is markedly distinguished from that of X-cell as shown in the present study, a quite different inhibitor mechanism may operate in the inner plexiform layer. ln the mudpuppy retina. Werblin and Copenhagen (1974) claim that only the transient on-off ganglion cells are hy~~lariz~ through the lateral inte~ction involving the transient amacrine ceils from the results of intracellular recordings of both cells. The above observation might give some clue to explain the transient nature of the suppressive effect in Y-cell at on and #of CS. In the most recent electron microscopic study of the cat retina, Kolb and Famiglietti (1974) have distinguished two types of amacrine cells. one of which appears to be speciiically involved in the rod system. In this connection, it should be wo~hwhile to note that the cone/rod ratio in the input to X-cells appears to be higher than to Y-cells: X-cells become more sensitive to the spot of red light when an adaptation state is shifted from scotopic to high mesopic levef (Fukada and Saito, unpublished observation). Further analysis comparing the gain-control behaviours of X/ Y-cells at various light conditions may help to reveal the neuronal organization of X/Y receptive fields, Ac~}low~~dge~~~r-The authors are indebted to Mr. Hirokazu Sunayama for his heip in the experiments. REFERENCES
Boycott B. B. and Wassle H. (1974)The morphological types of ganglion cells of the domestic cat’s retina. J. Physfof., Lmd. 240. 397-419. Biittner U. and Griisser 0.4. (1968) Quanti~tive Untersuchungen der rlumhchen Erregungssummation im rezep tiven Feld retinaler Neurone der Katze. ~vb~r~erjk 4. 8 l-94. CIelandB. G., Dubin M. W. and LevickW. R. (1971) Sustained and transient neurones in the cat’s retina and lateral gem&ate nucleus. J. Physiof., Land. 217, 473496. Cteland B. G., Levick W. R. and Sanderson K. J. (1973) Properties of sustained and transient gangiion cells in the cat retina. J. Physiol.. f&d. 228. ~~80. Creutzfeldt 0. D.. Sakmann B.. Scheich H. and Korn A. (1970) Sensitivity distribution and spatial summation within receptive-field center of retinal on-center ganglion cells and transfer function of the retina. J. ~eI~ropf~y~iof. 33. 654471. Dowling J. E. (1967) The site of visual adaptation. Science, N.X 155. 273-279. Dowhng J. E. and Boycott B. B. (1966) Grg~n~tion of the primate retina: electron microscopy. Proc. R. Sot.. Lottd. B166, 80-111. Dubin M. W. (1970) The inner plexiform layer of the vertebrate retina: a quantitative and com~rative electron microscopic analysis. J. camp. Newof. 14%479-506. Enroth-Cugell C. and Robson J. G. (1966) The contrast sensitivity of retina) ganglion cells of the cut. f. Ph_vsiol.. Lorrtf. t 87. 517-5.52. Enroth-Cugell C. and Shapley R. M. (1973) Adaptation and dynamics of cat retinal ganglion cells. J. Ph.vsio/.. LoiId. 233, 27 l-309.
1410
Research I\iote
Fukada Y. (1971) Receptive field organization of cat optic nerve fibers with special reference to conduction velocity. Vision Rex 11, 209-226. Fukada Y. and Saito H. (1971) The relationship between response characteristics to flicker stimulation and receptive field organization in the cat’s optic nerve fibers. Vision Res. 11, 221-240. Fukuda Y. and Stone J. (1974) Retinal distribution and central projections of Y-, X- and W-cells of the cat’s retina. J. Neurophysiol. 31, 749-772. Hoffmann K.-P., Stone J. and Sherman S. M. (1972) Relay of receptive-field properties in dorsal lateral geniculate nucleus of the cat. J.- Neurophysiol. 35, 518-531. Ikeda H. and Wright M. J. (1972) Retentive field oraanization of “sustain&” and “transient” r&al gangli& cells which subserve different functional roles. J. Physiol.. Land. 227, 769-800.
Kolb H. and Famiglietti E. V. (1974) Rod and cone pathways in the inner plexiform layer of cat retina. Sc~c~ct,. ,y.y: 186. 47-49. Saito H.. Shimahara T. and Fukada Y. (1970) Four types of responses to light and dark spot stimuli in the cat optic nerve. Tohoku J. cxp. Med. 102, 127-133. Saito H.. Shimahara T. and Fukada Y. (1971) Phasic and tonic responses in the cat optic nerve fibers-stimulusresponse relations. Tohoku J. exp. Med. 104, 31F323. Stone J. and Fabian M. (1968) Summing propertres of the cat’s retinal ganglion cell. Vision Res. 8. 1023-1040. Werblin F. S. (1974) Control of retinal sensitivity--II. Lateral interactions at the outer plexiform layer J gem Phrsiol. 63. 62-87. We&n F. S. and Copenhagen D. R. (1974) Control of retinal sensitivity-III: Lateral interactions at the inner plexiform layer. J. gem Phpsiol. 63, 88-1 10.
Grmt Britain
RESEARCH NOTE GAIN
CONTROL
MECHANISMS WITHIN THE RECEPTIVE OF CAT’S RETINAL GANGLION CELLS’ HIDE-AKI
SAITO
Research Group on Auditory and Visual Infomation
FIELD
CENTER
and YOSHIRO FUUDA
Processing, NHK Broadcasting
Science Research Laboratories.
Setagaya-ku, Tokyo 157.Japan (Receiued
18 November
1974; in recisedform
1 Prhrunry 1975)
In the previous studies (Fukada, 1971; Fukada and Saito, 1971X the cat’s retinal ganglion cells have been classified into Type-I and Type-II, independently of
light (5’ dia) were presented on a tangent screen which was placed 1.37m in front of the cat’s eyes and illuminated at 59 cd/m2 by distant fluorescent tubes. The
on- or off-center subdivision, on the basis of the receptive field proper&s and the axonal conduction velocities. Since then, accumulated data by us (&to, Shimahara and F&da, 1970, 1971)and others (Cleland, Dubin and Levi& 1971; Hoflinann, Stone and Sherman, 1972; Ikeda and Wright, 1972; Cleland, Levick and San&son, 1973)suggest that our Type-I cells correspond to Y-cells of Enroth-Cugell and Robson (1966)and Type-II to X-&Is. In this paper, X/Y terminology will be used because of its familiarity. It was observed that the response of on-center Xcell to a flashing spot of light presented at the center of the receptive field (RF) was gradually suppressed with successive stimulation. The suppression of the response was aIso observed even when the preceding spots had been presented at a little diierent position of the center region. By contrast, the response of Ycell remained constant for the repetitive stimulation (Fukada, 1971).From these observations, some kind of inhibition is suggested to develop in the neuronal network which organizes the RF of Xcell with successive stimulation, and to spread over the RF center region. An inhibitory mechanism in Y-cell, if any, may be different. In the present study, the inhibitory processes caused by a flashing spot itself in the on-center fields of X- and Y-cells were investigated by two-spot experiment: Response to the RF-centered spot (test spot, TS) was measured when an additional spot (conditioning spot, CS) was presented in the same RF center region. Experiments were conducted on 13 adult cats anaesthetized with nitrous oxide and immobilized with gallamine triethiodide. Extracellular spikes were
TS was presented at the center of the RF (the most sensitive part of the center region) and CS was located 15’ eccentric to TS. The CS was still well within the center region of the RF. In some experiments, the positions of TS and CS were interchanged with essentially the same results. The CS was presented once every 12 set and lasted for 3 sec. The TS was flashed for 100 or 200 msec with a variable delay relative to the onset or the cessation of CS. The luminance of the spots of light, which were maximally available at 3.9 x ld and 6.8 x 103 cd/m2 for TS and CS respectively, were adjusted with neutral density filters so that an algebraic sum of the responses to TS and CS was well within the dynamic range of the cell’s response. To focus the spot stimuli on the retina and to keep high image quality, a contact lens (usually, + 10 D) with 4mm aperture was used. The magnitude of the test response (TR) was measured as follows. First, the averaged PST-histograms were obtained from 20 consecutive responses to TS alone, CS alone and to combined stimuli of TS and CS, respectively. They were expressed as the number of impulses for each bin (bin width was usually 20 msec). The maintained discharge rate averaged for 1 set prior to the presentation of TS alone was ’ expressed also in impulses/bin. The unconditioned TR was defined by a total number of impulses which were elicited by TS alone and exceeded the maintained discharge rate. When TS was combined with CS. the conditioned TR was obtained in the same way except that the maintained discharge rate was substituted by
recorded from the optic tract with tungsten microelectrodes. Spikes were fed to a Schmitt trigger circuit
PST-histograms
to CS alone.
Forty on-center cells were classitied as either X (20) or Y (20) depending on the two criteria. One criterion is the difference in the tonic (X) or phasic (Y) response profile of the cell to a long-lasting spot stimulus. The
1A preliminary report of this work was presented at XXVIICPS SatelliteSymposiumon Visionheld in Sydney.
other is the difference in the fine structure of the impulse train of the initial transient response to the stimulus onset; Y-cells have a clear discontinuity in their discharge rate between the initial burst and SUCceeding discharges whereas Xcells do not show such discontinuity (Saito et al.. 1970, 1971).It is worth noting that this difference in the initial transient part of response was so marked that it proved to be a good criterion for X/Y-classiication. For both types of cells, TR was suppressed by CS
October 1974.
presentation,
to produce pulses of standard width and amplitude. and those pulses were fed to a mini-computer (TOSBAC-3CHM, Toshiba) to compile the post-stimulus time histograms (PST-histograms). The TS and CS were produced from glow modulator tubes (Sylvania, R1131Q and those spots of
1407
but the time course of the suppression
Research
Note
XON
YON
lYJ.&-
(0)
(e)
i
(f)
I
,
I(h)
Time,
Time.
set
set
Fig. I. Two-spot experiments for a X-cell [(a)-(d)] and for a Y-cell [(e)-(h)]. PST-histograms show examples of response profiles to the test spot (TS. short bar under the histograms) and to the conditioning spot (CS, long bar). (a) and (e): TS was presented 2 set after on of CS. (b) and (f): TS alone. (c) and (8): TS, 2 set after @of CS. TS duration; 200 msec for the X-cell, 100 msec for the Y-cell. CS duration; 3 sec. Vertical calibration; 50 impulses/set. Bin width; 20 msec. (d) and (h): Time courses of the change of the magnitude of the test response (TR) caused by CS presentation for the X-cell and the Y-cell respectively. Abscissa: the time of the onset of TS relative to the onset of Cs (first zero) and to the cessation of CS (second zero). Ordinate: the magnitude of the conditioned TR expressed as a relative unit with respect to that of the unconditioned TR.
is remarkably different between X- and Y-cells as shown in Figs. l(d) (X) and (h) (Y). The TR of X-cell is suppressed progressively after the onset of CS, and within about 200 msec, TR reaches very low steady level. This suppression is maintained as long as CS continues, although a slight recovery can be seen. After the cessation of CS, TR recovers monotonically. In Y-cell, on the other hand, TR is suppressed immediately after the onset of CS, then within about 500 msec it recovers to some level which is still lower than the unconditioned TR. One of the most striking differences from X-cell is seen at the cessation of CS: Y-cell shows another transient suppression which is generally stronger than that observed at the onset of CS. The recovery from this suppression at of was often followed by a rebound. Then, an effect of the CS intensity upon the suppression of TR was studied. Figure 2 shows an example of Y-cell for which the time courses of the suppression are obtained for three CS intensities separated by 0.4 log step. The increase of CS intensity causes a general increase of the amount of TR-suppression: the transient suppressions at the onset and the cessation of CS are strengthened and the level to which TR recovers during CS presentation is also lowered. In X-cell as well, the only effect of increase of CS intensity was to strengthen the suppression. The general characteristics of the time course of the suppression in X/Y cells were respectively kept unchanged when the positions of ‘IS and CS were interchanged: X-cell showed sustained suppression concomitant with CS, while Y-cell showed transient suppressions at 011and ofof CS. As has been described, for both X- and Y-cells, excitatory input by flashing a spot of light in the RF-
(0)
I.9
YON
Time,
+-4,
0j -3
set
-2
-I
0
Fig. 2. Effects of CS intensity upon the time course of TR-suppression in a Y-cell. (a): Time courses of the change of the magnitude of the conditioned TR obtained under three CS intensities separated by 04 log unit as indicated on each curve. Abscissa and ordinate; same as in Fig. 1 except that the time scale of the transient parts after on and oflof CS are expanded. (b): Stimulus-response relations of the same cell to TS (filled circles) and to CS (open circles). Abscissa; intensity of TS and CS in log unit. Zero log unit corresponds 3.9 x IO” and 68 x IO3 cd/m’ for TS and CS respectively. Response magnitudes (impulses/ set) averaged over 100 msec after the stimulus onset for TS alone and CS alone under the same luminance conditions as in (a) are indicated by arrows.
I409
Research Note
center makes the excitatory effect of another spot of light in the same center region smaller than if this second stimulus were presented alone. Intrinsic properties of the ganglion cell membrane (Stone and Fabian. 1968) would account for some of the nonlinearity in the signal summation especially when the TS is presented concomitantly with the onset of CS in Y-cell. But the suppression in response to T’Sinversely correlates to the ongoing firing rate of X cell. If the non-linearity is located in the ganglion cell dendrites as suggested by Creutzfeldt, Sakmann, Scheich and Kom (1970). mo~hologi~l differences between X- and Y-cells claimed in recent studies (Fukuda and Stone, 1974; Boycott and W&ie. 1974)may provide us with some clue to account for the differences in the suppression of X/y-cells. However. the dendritic geometry of the ganglion cell would not be sufficient to explain the marked difference in the time course of suppression of X/y-cells. There is plenty of physiological and anatomical studies which suggest the pm-ganglionic interaction between two stimuli presented in the same RF center region. First, in the outer plexiform layer of the cat’s retina, a kind of neuronal adaptation which spreads laterally within the RF center has been suggested on the basis of the multi-spot experiments. assuming that a horizontal cell exerts an inhibitory influence either presy~pti~lly on the rotor-bills synapses (Bilttner and Grtlsser, 1968)or back on to receptors (Enroth-Cugell and Shapley, 1973). Enroth-Cugell and Shapley suggested such a feed-back gain control ~chanism from the results of a similar experiment to ours except that the two spots were presented concentrically at the center of RF under the scotopic a~p~tion state. The time course of the gain change in their Y-cell is apparently similar in general form to that of our X-cell. They have not reported on Xcell, and it is so far uncertain whether this discrepancy is due to the different stimulus conditions. As shown by Werbhn (1974) with intracellular study of bipolar and horizontal cells in the mudpuppy retina, horizontal cells in the cat’s retina may control the magnitude of the sustained depolarizing (hyperpolarizing) responses of the bipolar cells to the RFcentered stimulus indifferently to X/Y-classification.it is therefore likely that different gain control m~hanisms between X- and Y-cells may be found in the inner plexiform layer. In the inner piexifo~ layer, the dyad synapse, where the bipolar cell terminal makes contacts with two postsynaptic elements, is commonly associated with a reciprocal synapse from the amacrine to bipolar cell (Dowhng and Boycott. 1966; Dubin. 1970). If such a reciprocal synapse works as a negative feedback (Dowling, 1%7), the transmission of the SUStamed response of the bipolar cell to the ganglion cell will be further regulated. Suppose that the reciprocal inhibitory effect of the amacrine cell is not only confined to the dyad complex where the excitatory input caused by a spot of light is tr~nsmitt~. but also extends to the other synaptic sites where the processes of this cefi terminate. Then, another excitatory input which is caused by another spot of Iight in the same RF center region and which has arrived at those synaptic sites may also he subjected to the regulation of the same amacrine ceil. The marked
~~1~~~ ,#&enIn the inter-spike intervals of the sustained response of X-cell (Saito et al., 1971)suggests the above-mentioned feed-back mechanism. From the facts that the inter-spike intervals in the response of Y-cell are very irregular, and that the time course of the suppression in Y-cell is markedly distinguished from that of X-cell as shown in the present study, a quite different inhibitor mechanism may operate in the inner plexiform layer. ln the mudpuppy retina. Werblin and Copenhagen (1974) claim that only the transient on-off ganglion cells are hy~~lariz~ through the lateral inte~ction involving the transient amacrine ceils from the results of intracellular recordings of both cells. The above observation might give some clue to explain the transient nature of the suppressive effect in Y-cell at on and #of CS. In the most recent electron microscopic study of the cat retina, Kolb and Famiglietti (1974) have distinguished two types of amacrine cells. one of which appears to be speciiically involved in the rod system. In this connection, it should be wo~hwhile to note that the cone/rod ratio in the input to X-cells appears to be higher than to Y-cells: X-cells become more sensitive to the spot of red light when an adaptation state is shifted from scotopic to high mesopic levef (Fukada and Saito, unpublished observation). Further analysis comparing the gain-control behaviours of X/ Y-cells at various light conditions may help to reveal the neuronal organization of X/Y receptive fields, Ac~}low~~dge~~~r-The authors are indebted to Mr. Hirokazu Sunayama for his heip in the experiments. REFERENCES
Boycott B. B. and Wassle H. (1974)The morphological types of ganglion cells of the domestic cat’s retina. J. Physfof., Lmd. 240. 397-419. Biittner U. and Griisser 0.4. (1968) Quanti~tive Untersuchungen der rlumhchen Erregungssummation im rezep tiven Feld retinaler Neurone der Katze. ~vb~r~erjk 4. 8 l-94. CIelandB. G., Dubin M. W. and LevickW. R. (1971) Sustained and transient neurones in the cat’s retina and lateral gem&ate nucleus. J. Physiof., Land. 217, 473496. Cteland B. G., Levick W. R. and Sanderson K. J. (1973) Properties of sustained and transient gangiion cells in the cat retina. J. Physiol.. f&d. 228. ~~80. Creutzfeldt 0. D.. Sakmann B.. Scheich H. and Korn A. (1970) Sensitivity distribution and spatial summation within receptive-field center of retinal on-center ganglion cells and transfer function of the retina. J. ~eI~ropf~y~iof. 33. 654471. Dowling J. E. (1967) The site of visual adaptation. Science, N.X 155. 273-279. Dowhng J. E. and Boycott B. B. (1966) Grg~n~tion of the primate retina: electron microscopy. Proc. R. Sot.. Lottd. B166, 80-111. Dubin M. W. (1970) The inner plexiform layer of the vertebrate retina: a quantitative and com~rative electron microscopic analysis. J. camp. Newof. 14%479-506. Enroth-Cugell C. and Robson J. G. (1966) The contrast sensitivity of retina) ganglion cells of the cut. f. Ph_vsiol.. Lorrtf. t 87. 517-5.52. Enroth-Cugell C. and Shapley R. M. (1973) Adaptation and dynamics of cat retinal ganglion cells. J. Ph.vsio/.. LoiId. 233, 27 l-309.
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Research I\iote
Fukada Y. (1971) Receptive field organization of cat optic nerve fibers with special reference to conduction velocity. Vision Rex 11, 209-226. Fukada Y. and Saito H. (1971) The relationship between response characteristics to flicker stimulation and receptive field organization in the cat’s optic nerve fibers. Vision Res. 11, 221-240. Fukuda Y. and Stone J. (1974) Retinal distribution and central projections of Y-, X- and W-cells of the cat’s retina. J. Neurophysiol. 31, 749-772. Hoffmann K.-P., Stone J. and Sherman S. M. (1972) Relay of receptive-field properties in dorsal lateral geniculate nucleus of the cat. J.- Neurophysiol. 35, 518-531. Ikeda H. and Wright M. J. (1972) Retentive field oraanization of “sustain&” and “transient” r&al gangli& cells which subserve different functional roles. J. Physiol.. Land. 227, 769-800.
Kolb H. and Famiglietti E. V. (1974) Rod and cone pathways in the inner plexiform layer of cat retina. Sc~c~ct,. ,y.y: 186. 47-49. Saito H.. Shimahara T. and Fukada Y. (1970) Four types of responses to light and dark spot stimuli in the cat optic nerve. Tohoku J. cxp. Med. 102, 127-133. Saito H.. Shimahara T. and Fukada Y. (1971) Phasic and tonic responses in the cat optic nerve fibers-stimulusresponse relations. Tohoku J. exp. Med. 104, 31F323. Stone J. and Fabian M. (1968) Summing propertres of the cat’s retinal ganglion cell. Vision Res. 8. 1023-1040. Werblin F. S. (1974) Control of retinal sensitivity--II. Lateral interactions at the outer plexiform layer J gem Phrsiol. 63. 62-87. We&n F. S. and Copenhagen D. R. (1974) Control of retinal sensitivity-III: Lateral interactions at the inner plexiform layer. J. gem Phpsiol. 63, 88-1 10.
