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Influence of the cortico-geniculate pathway on response properties of cat lateral geniculate neurons
Brain Research, 208 (1981) 409-415 © Elsevier/North-Holland Biomedical Press
409
Short Communications Influence of the cortico-geniculate pathway on response properties of cat lateral geniculate neurons
E. E. GEISERT, ARNE LANGSETMO and PETER D. SPEAR* Department of Psychology and Neurosciences Training Program, University of Wisconsin, Madison, Wisc. 53706 (U.S.A.) (Accepted October 16th, 1980) Key words: vision - - visual cortex - - lateral geniculate nucleus - - cortico-fugal pathway - - cat
The influence of the cortico-geniculatepathway on identified X and Y lateral geniculate cells was studied by reversibly cooling visual cortical areas 17 and 18. The majority (86.5~) of cells changed their response to visual stimulation when cortex was inactivated, and both X- and Y-cells were modulated by the cortical input. The influence of the visual cortex was complex, with both excitatory and inhibitory actions. Furthermore, the mechanism underlying the basic center-surround receptive field organization was influenced. The A laminae of the dorsal lateral geniculate nucleus receive a massive input from visual cortical areas 17 and 185,6,s,is. Many investigators have attempted to define the functional role of the cortico-geniculate pathway by reversibly inactivating the visual cortex while recording from lateral geniculate neuronsl,9,10,12-15,1L These studies have investigated such properties as spontaneous activity, response to receptive field center stimulation and binocular interactions. However, the cortical influence on the basic center-surround concentric receptive field organization of lateral geniculate cells has not been investigated. In addition, it is not known if the parallel X- and Y-cell pathways of the lateral geniculate2,3, 7 are influenced differently by cortico-fugal projections. These questions were addressed in the present experiments. In addition, in the course of classifying cells as X or Y, we routinely assessed the effects of cortical inactivation on responses to a number of other stimulus conditions not previously tested. The influence of the cortical input on single neurons in the lateral geniculate nucleus was studied by reversibly cooling cortical areas 17 and 18 in 16 adult cats. Details of the surgical preparation for single unit recording are described elsewhere 11. During the recording session, the animal was immobilized with gallamine triethiodide (Flaxedil) and maintained on 75 ~ N20 and 25 ~ 02. The eyes were fitted with contact lenses containing 4 mm pupils, and spectacle lenses were used to focus the retinae on a tangent screen placed 114 cm from the approximate nodal point of each eye. For * To whom correspondence should be addressed.
410 cortical cooling, a silver plate attached to a Peltier device was placed on the dura overlying the dorsal surface of areas 17 and 18 near the posterior bend of the lateral gyrus. The silver plate covered an area 11 mm (anterior-posterior) × 6 mm (medial-lateral), and cooled 4° or more of the central visual field representation in areas 17 and 1816,17. The area cooled was larger than the area contacted by the silver plate because of the temperature gradient around the plate1°, 14. Cortical activity was monitored with a tungsten microelectrode that passed through a hole in the cooling plate and dura. Cortical temperature was monitored with a thermistor in the tip of a 22-gauge needle that was inserted 2 mm below the cortical surface directly under the plate. Tungsten microelectrodes were used to record extracellularly from single neurons in laminae A and A1 of the lateral geniculate nucleus (recording sites were verified histologically). Only cells that had receptive fields within 4 ° of area centralis were studied to insure that the cortical input was inactivated by the cooling. For each cell, control data were collected while cortex was at 38 °C. The visual cortex was then cooled to 14 °C and the lateral geniculate cell was retested. If the response to any of the tests (see below) changed during cooling, the cortex was rewarmed to 38 °C and the tests were given for a third time. Nine different tests were used: (1) spontaneous activity was measured with the tangent screen diffusely illuminated (--1.35 log cd/sq.m); (2) receptive field center size was measured with a small flashing spot; (3) response to receptive field center stimulation was tested with a spot of light (0.17 log cd/sq.m) the size of the receptive field center; (4) response to receptive field surround stimulation was tested with a light annulus that had an inside diameter equal to the receptive field center size and an outside diameter of 7°; (5) interaction between response to receptive field center and surround stimulation was tested by simultaneously stimulating both regions with a 7 ° spot of light; (6) maximum stimulus velocity to which the cell responded on every trial was determined with a moving 3.5 ° spot of opposite contrast to the receptive field center (e.g. a dark spot for an ON-center cell); (7) maximum spatial frequency to which the cell responded on every cycle was measured using drifting high contrast (89.5~o) square-wave gratings ranging from 0.16 to 6.5 cycles/°; (8) the presence of linear or non-linear spatial summation was tested with a 6.5 ° diameter bipartite field. The luminance of each half-field was sinusoidally modulated 180° out of phase so that mean luminance remained constant. The stimulus was stepped across the receptive field to find a location at which no response (linear summation) or response doubling (nonlinear summation) occurred4,7; and (9) modal response latency to electrical stimulation of the optic chiasm was determined. Cells were classified as X, Y, or mixed on the basis of tests 2, 6, 8 and 9~,3. X-cells had at least 3 of the following properties: < 1.0° diameter receptive field center; < 160°/see cut-off velocity; linear spatial summation; and > 1.6 msec latency to optic chiasm stimulation. Y-cells had at least 3 of the opposite properties. Mixed cells had 2 X- and 2 Y-cell properties. Visual stimuli were presented with an automated projector system, and responses were evaluated by listening to an audio monitor or by constructing post-stimulus time histograms with an Ortec 4620/4621 time-histogram analyzer. When analyzing the histograms a change in response magnitude or pattern was defined as a 5 0 ~
X-ON-CENTER
X -OFF - CENTER
Y-ON -CENTER
Y - OFF -CENTER
Fig. 1. Summary of the changes observed during cortical cooling for each cell studied. The direction of change is indicated following the schema shown in the legend in the upper left corner of the figure. Five neurons showed no change in response to any test during cortical cooling. Four of these cells were encountered in the same microelectrode penetration as cells that did show a change. Thirtytwo cells demonstrated an increase or a decrease in response to at least one test, and the direction of this change could be different on different tests.
A. X-CELL,ON-CENTER CONTROL
REWARM
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Fig. 2. Responses of 3 neurons are illustrated by poststimulus frequency histograms. For each cell the response to stimulation of the receptive field center is in the top row (1), the response to surround stimulation is in the middle row (2) and the response to simultaneous stimulation of center plus surround is in the bottom row (3). Stimulus conditions are shown schematically to the left. The control condition is the response of the neuron prior to cooling the visual cortex. The cool condition is the response while the cortex was cooled to 14 °C. The rewarm condition is the response following reactivation of the visual cortex by warming it to 38 °C. In A and B the stimulus duration was one second and 32 trials were presented for each histogram. In C the stimulus duration was 3 seconds and each histogram is constructed of 8 trials. The calibration line to the left of each set of histograms represents 100 spikes. See text for a description of the changes during cortical inactivation.
413 increase or decrease in the number of spikes in the response during cooling relative to the control and rewarm conditions. Data were collected from 37 neurons (Fig. 1). Most cells (86.5 ~) showed a change in response to at least one of the tests during cortical cooling. Comparable changes were seen for X-, Y- and mixed cells and for ON and OFF center cells. In addition, the results were similar for cells in laminae A and A1. The most common change observed during cortical cooling was in the response to stimulation of the receptive field center, surround, or both together using spots and annuli (tests 3-5); 62 ~ of the ceils demonstrated a change in response to one or more of these 3 stimulus conditions (Fig. 1). The changes in response to stimulation of the receptive field center varied from neuron to neuron, with some cells becoming more responsive during cortical cooling and others becoming less responsive. In addition, different components of the receptive field center response could be altered independently, and in different directions, for some neurons. Examples of this are shown in Fig. 2. For the cell in Fig. 2A, cortical cooling decreased both the sustained and transient components of the response to light onset in the receptive field center, and increased the after-discharge to light offset (Fig. 2A1, compare cool with control and rewarm conditions). For the cell in Fig. 2C, cortical cooling decreased the sustained component of the response following stimulus offset, but the transient component of the response was unaffected (Fig. 2C1). When the receptive field surround was stimulated with an annulus, cortical cooling again could produce a variety of response changes. Moreover, the effects of cortical cooling on the surround response could be independent of the effects on the receptive field center response (Fig. 1, compare columns 3 and 4). Fig. 2A and B illustrates the results for two cells in which cortical cooling decreased the response to light onset in the receptive field center, but increased the response to light offset in the receptive field surround. When both the center and surround were stimulated together, the effects of cortical cooling often were predictable from the effects seen with stimulation of the center or surround alone. Of the 14 cells in which the cortical cooling had no effect on the response to center or surround stimulation alone, the cooling also had no effect on the response to simultaneous stimulation of both. Similarly, 11 of the cells that showed changes in response to center or surround stimulation during cortical cooling simply showed additive effects when both were stimulated. For example, the cell in Fig. 2B decreased its response to center stimulation (Fig. 2B1) and increased its response to surround stimulation (Fig. 2B2) during cortical cooling, and both components of the response showed similar changes to center plus surround stimulation during cortical cooling (Fig. 2B3). In contrast to these results, 10 cells showed changes in response to center plus surround stimulation during cooling that were not predictable from the changes in response to either region alone. Two examples are shown in Fig. 2. For the cell in Fig. 2A, cortical cooling increased the OFF response to surround stimulation (Fig. 2A2), but decreased the OFF response to center plus surround stimulation (Fig. 2A3). For the cell in Fig. 2C, cortical cooling had relatively minor effects on the response to stimulation of center (Fig. 2C1) or surround (Fig. 2C~) alone, but it nearly
414 abolished the response to center plus surround stimulation (Fig. 2C3). For these cells, the mechanisms underlying center-surround response antagonism appear to be increased by inactivation of visual cortex. A total of 5 cells showed changes of this sort, while 5 cells showed a decrease in center-surround response antagonism during cortical inactivation. As shown in Fig. 1, other response properties of lateral geniculate neurons were also seen to change when visual cortex was inactivated. Eleven neurons showed a statistically significant (Student's t-test, P < 0.05 in each case) decrease in spontaneous activity (23-100~ change, mean 59~), while 4 cells showed an increase (16-88 ~, mean 60 ~). Four Y-cells altered their response to drifting square wave gratings (test 7). One of these responded to a maximum of 0.44 cycles/° in the control and rewarm conditions and responded to 0.69 cycles/° in the cool condition. The other 3 ceils changed from 0.69 cycles/° to either 0.91 or 1.11 cycles/°. Changes also were seen in responses to tests that we used to classify X and Y cells. Thus, the maximum velocity to which the cells responded (test 6) was altered in some cases; 4 cells showed a decrease (23-66 ~ ) and 3 showed an increase in maximum velocity (17-67~). Six cells showed a slight but reliable increase in the latency of response to optic chiasm stimulation, ranging from 0.2 to 0.5 msec. In each case, the modal response latency returned to exactly the same value during the rewarm condition as during the control condition (care was taken to use the same stimulus parameters during the control, cool and rewarm conditions). Two cells changed their response to the test for linear spatial summation (test 8) during cortical inactivation. Both of these cells became non-responsive to the contrast-reversal stimulus during cortical cooling (although they continued to respond well to other stimuli). Finally, one cell showed a decrease in receptive field center size from 0.9 ° diameter in the control and rewarm conditions to 0.4 ° diameter during cortical cooling. Although changes in response were seen to tests used to classify cells as X or Y, none of the changes were both of sufficient magnitude and in the appropriate direction to produce a change in classification. Four main conclusions can be drawn from these findings. First, the vast majority of lateral geniculate neurons are influenced by visual cortical input. The proportion of cells showing changes during cortical cooling in the present study is higher than that in previous studies of the cat lateral geniculate10,13,14. Undoubtedly, this is due in part to the use of a large number of stimulus tests in the present experiments. It is possible that all of the cells would show cortical influences if additional tests were used. Second, cortical input modulates important response properties of the lateral geniculate neurons. For example, the basic receptive field center and surround response mechanisms, and the strength of their mutual antagonism, can be altered for many cells. Since center-surround response antagonism is thought to be involved in contour enhancement by the visual system, this result suggests that the cortico-geniculate pathway plays a role in the modulation of basic spatial visual processes. Third, the influence of the cortico-geniculate pathway is very complex. Both excitatory and inhibitory influences were observed on the same lateral geniculate neurons, in agreement with previous studies10,14,15. In addition, for a given cell a change in response to one
415 stimulus c o n d i t i o n could occur i n d e p e n d e n t of any changes in response to other stimulus conditions. Finally, the cortico-geniculate pathway has c o m p a r a b l e influences o n all cell types in the lateral geniculate, including n e u r o n s in both the X- a n d Ysystems. We would like to t h a n k Ms. K a t h y Vielhuber a n d Ms. Lynne O h m a n for their excellent technical assistance. This work was supported by U S P H S Postdoctoral Fellowship EY05259 (E.E.G.), U S P H S Research G r a n t s EY01916 a n d EY02545, a n d U S P H S Research Career Development A w a r d EY00089 (P.D.S.).
1 Baker, F. H. and Malpeli, J. G., Effects of cryogenic blockade of visual cortex on the responses of lateral geniculate neurons in the monkey, Exp. Brain Res., 29 (1977) 433~44. 2 Bullier, J. and Norton, T. T., X and Y relay cells in cat lateral geniculate nucleus: quantitative analysis of receptive-field properties and classification, J. Neurophysiol., 42 (1979) 244-273. 3 Cleland, B. G., Dubin, M. W. and Levick, W. R., Sustained and transient neurons in the cat's retina and lateral geniculate nucleus, J. PhysioL (Lond.), 217 (1971) 473-496. 4 Enroth-Cugell, C. and Robson, J. G., The contrast sensitivity of retinal ganglion cells of the cat, J. Physiol. (Lond.), 187 (1966) 517-552. 5 Gilbert, C. D. and Kelly, J. P., The projection of cells in different layers of the cat's visual cortex, J. camp. Neurol., 163 (1975) 81-105. 6 Guillery, R. W., Patterns of fiber degeneration in the dorsal lateral geniculate nucleus of the cat following lesions in the visual cortex, J. comp. Neurol., 130 (1967) 197-222. 7 Hoffmann, K.-P., Stone, J. and Sherman, S. M., Relay of receptive-field properties in dorsal lateral geniculate nucleus of the cat, J. Neurophysiol., 35 (1972) 518-531. 8 Holl/inder, H.,Autoradiographicevidenceforaprojection from the striate cortex to the dorsal part of the lateral geniculate nucleus in the cat, Brain Research, 41 (1972) 464-466. 9 Hull, E., Corticofugal influences in the macaque lateral geniculate nucleus, Vision Res., 8 (1968) 1285-1298.
10 Kalil, R. E. and Chase, R., Corticofugal influence on activity of lateral geniculate neurons in the cat, J. NeurophysioL, 33 (1970) 459-474. 11 Kratz, K. E., Spear, P. D. and Smith, D. C., Postcritical-period reversal of effects of monocular deprivation on striate cortex ceils in the cat, J. NeurophysioL, 39 (1976) 501-511. 12 Molotchnikoff, S., Richard, D. and Lachapelle, P., Influence of the visual cortex upon receptive field organization of lateral geniculate cells in rabbits, Brain Research, 193 (1980) 383-399. 13 Richard, D., Gioanni, Y., Kitsikis, A. and Buser, P., A study of geniculate unit activity during cryogenic blockade of primary cortex in the cat, Exp. Brain Res., 22 (1975) 235-242. 14 Schmielau, F. and Singer, W., The roleof visual cortex for binocular interactions in the cat lateral geniculate nucleus, Brain Research, 120 (1977) 354-361. 15 Tsumoto, T., Creutzfeldt, O. D. and Legdndy, C. R., Functional organization of the corticofugal system from visual cortex to lateral geniculate nucleus in the cat, Exp. Brain Res., 32 (1978) 345-364. 16 Tusa, R. J., Palmer, L. A. and Rosenquist, A. C., The retino-topic organization of area 17 (striate cortex) in the cat, J. comp. Neurol., 177 (1978) 213-236. 17 Tusa, R. J., Rosenquist, A. C. and Palmer, L. A., Retinotopic organization of areas 17 and 18 in the cat, J. comp. Neurol., 185 (1979) 657-678. 18 Updyke, B. V., The patterns of projection of cortical areas 17, 18 and 19 onto the laminae of the dorsal lateral geniculate nucleus in the cat, J. comp. NeuroL, 163 (1975) 377-395. 19 Vastola, E. F., Steady state effects of visual cortex on geniculate cells, Vision Res., 7 (1967) 599-609.
409
Short Communications Influence of the cortico-geniculate pathway on response properties of cat lateral geniculate neurons
E. E. GEISERT, ARNE LANGSETMO and PETER D. SPEAR* Department of Psychology and Neurosciences Training Program, University of Wisconsin, Madison, Wisc. 53706 (U.S.A.) (Accepted October 16th, 1980) Key words: vision - - visual cortex - - lateral geniculate nucleus - - cortico-fugal pathway - - cat
The influence of the cortico-geniculatepathway on identified X and Y lateral geniculate cells was studied by reversibly cooling visual cortical areas 17 and 18. The majority (86.5~) of cells changed their response to visual stimulation when cortex was inactivated, and both X- and Y-cells were modulated by the cortical input. The influence of the visual cortex was complex, with both excitatory and inhibitory actions. Furthermore, the mechanism underlying the basic center-surround receptive field organization was influenced. The A laminae of the dorsal lateral geniculate nucleus receive a massive input from visual cortical areas 17 and 185,6,s,is. Many investigators have attempted to define the functional role of the cortico-geniculate pathway by reversibly inactivating the visual cortex while recording from lateral geniculate neuronsl,9,10,12-15,1L These studies have investigated such properties as spontaneous activity, response to receptive field center stimulation and binocular interactions. However, the cortical influence on the basic center-surround concentric receptive field organization of lateral geniculate cells has not been investigated. In addition, it is not known if the parallel X- and Y-cell pathways of the lateral geniculate2,3, 7 are influenced differently by cortico-fugal projections. These questions were addressed in the present experiments. In addition, in the course of classifying cells as X or Y, we routinely assessed the effects of cortical inactivation on responses to a number of other stimulus conditions not previously tested. The influence of the cortical input on single neurons in the lateral geniculate nucleus was studied by reversibly cooling cortical areas 17 and 18 in 16 adult cats. Details of the surgical preparation for single unit recording are described elsewhere 11. During the recording session, the animal was immobilized with gallamine triethiodide (Flaxedil) and maintained on 75 ~ N20 and 25 ~ 02. The eyes were fitted with contact lenses containing 4 mm pupils, and spectacle lenses were used to focus the retinae on a tangent screen placed 114 cm from the approximate nodal point of each eye. For * To whom correspondence should be addressed.
410 cortical cooling, a silver plate attached to a Peltier device was placed on the dura overlying the dorsal surface of areas 17 and 18 near the posterior bend of the lateral gyrus. The silver plate covered an area 11 mm (anterior-posterior) × 6 mm (medial-lateral), and cooled 4° or more of the central visual field representation in areas 17 and 1816,17. The area cooled was larger than the area contacted by the silver plate because of the temperature gradient around the plate1°, 14. Cortical activity was monitored with a tungsten microelectrode that passed through a hole in the cooling plate and dura. Cortical temperature was monitored with a thermistor in the tip of a 22-gauge needle that was inserted 2 mm below the cortical surface directly under the plate. Tungsten microelectrodes were used to record extracellularly from single neurons in laminae A and A1 of the lateral geniculate nucleus (recording sites were verified histologically). Only cells that had receptive fields within 4 ° of area centralis were studied to insure that the cortical input was inactivated by the cooling. For each cell, control data were collected while cortex was at 38 °C. The visual cortex was then cooled to 14 °C and the lateral geniculate cell was retested. If the response to any of the tests (see below) changed during cooling, the cortex was rewarmed to 38 °C and the tests were given for a third time. Nine different tests were used: (1) spontaneous activity was measured with the tangent screen diffusely illuminated (--1.35 log cd/sq.m); (2) receptive field center size was measured with a small flashing spot; (3) response to receptive field center stimulation was tested with a spot of light (0.17 log cd/sq.m) the size of the receptive field center; (4) response to receptive field surround stimulation was tested with a light annulus that had an inside diameter equal to the receptive field center size and an outside diameter of 7°; (5) interaction between response to receptive field center and surround stimulation was tested by simultaneously stimulating both regions with a 7 ° spot of light; (6) maximum stimulus velocity to which the cell responded on every trial was determined with a moving 3.5 ° spot of opposite contrast to the receptive field center (e.g. a dark spot for an ON-center cell); (7) maximum spatial frequency to which the cell responded on every cycle was measured using drifting high contrast (89.5~o) square-wave gratings ranging from 0.16 to 6.5 cycles/°; (8) the presence of linear or non-linear spatial summation was tested with a 6.5 ° diameter bipartite field. The luminance of each half-field was sinusoidally modulated 180° out of phase so that mean luminance remained constant. The stimulus was stepped across the receptive field to find a location at which no response (linear summation) or response doubling (nonlinear summation) occurred4,7; and (9) modal response latency to electrical stimulation of the optic chiasm was determined. Cells were classified as X, Y, or mixed on the basis of tests 2, 6, 8 and 9~,3. X-cells had at least 3 of the following properties: < 1.0° diameter receptive field center; < 160°/see cut-off velocity; linear spatial summation; and > 1.6 msec latency to optic chiasm stimulation. Y-cells had at least 3 of the opposite properties. Mixed cells had 2 X- and 2 Y-cell properties. Visual stimuli were presented with an automated projector system, and responses were evaluated by listening to an audio monitor or by constructing post-stimulus time histograms with an Ortec 4620/4621 time-histogram analyzer. When analyzing the histograms a change in response magnitude or pattern was defined as a 5 0 ~
X-ON-CENTER
X -OFF - CENTER
Y-ON -CENTER
Y - OFF -CENTER
Fig. 1. Summary of the changes observed during cortical cooling for each cell studied. The direction of change is indicated following the schema shown in the legend in the upper left corner of the figure. Five neurons showed no change in response to any test during cortical cooling. Four of these cells were encountered in the same microelectrode penetration as cells that did show a change. Thirtytwo cells demonstrated an increase or a decrease in response to at least one test, and the direction of this change could be different on different tests.
A. X-CELL,ON-CENTER CONTROL
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Fig. 2. Responses of 3 neurons are illustrated by poststimulus frequency histograms. For each cell the response to stimulation of the receptive field center is in the top row (1), the response to surround stimulation is in the middle row (2) and the response to simultaneous stimulation of center plus surround is in the bottom row (3). Stimulus conditions are shown schematically to the left. The control condition is the response of the neuron prior to cooling the visual cortex. The cool condition is the response while the cortex was cooled to 14 °C. The rewarm condition is the response following reactivation of the visual cortex by warming it to 38 °C. In A and B the stimulus duration was one second and 32 trials were presented for each histogram. In C the stimulus duration was 3 seconds and each histogram is constructed of 8 trials. The calibration line to the left of each set of histograms represents 100 spikes. See text for a description of the changes during cortical inactivation.
413 increase or decrease in the number of spikes in the response during cooling relative to the control and rewarm conditions. Data were collected from 37 neurons (Fig. 1). Most cells (86.5 ~) showed a change in response to at least one of the tests during cortical cooling. Comparable changes were seen for X-, Y- and mixed cells and for ON and OFF center cells. In addition, the results were similar for cells in laminae A and A1. The most common change observed during cortical cooling was in the response to stimulation of the receptive field center, surround, or both together using spots and annuli (tests 3-5); 62 ~ of the ceils demonstrated a change in response to one or more of these 3 stimulus conditions (Fig. 1). The changes in response to stimulation of the receptive field center varied from neuron to neuron, with some cells becoming more responsive during cortical cooling and others becoming less responsive. In addition, different components of the receptive field center response could be altered independently, and in different directions, for some neurons. Examples of this are shown in Fig. 2. For the cell in Fig. 2A, cortical cooling decreased both the sustained and transient components of the response to light onset in the receptive field center, and increased the after-discharge to light offset (Fig. 2A1, compare cool with control and rewarm conditions). For the cell in Fig. 2C, cortical cooling decreased the sustained component of the response following stimulus offset, but the transient component of the response was unaffected (Fig. 2C1). When the receptive field surround was stimulated with an annulus, cortical cooling again could produce a variety of response changes. Moreover, the effects of cortical cooling on the surround response could be independent of the effects on the receptive field center response (Fig. 1, compare columns 3 and 4). Fig. 2A and B illustrates the results for two cells in which cortical cooling decreased the response to light onset in the receptive field center, but increased the response to light offset in the receptive field surround. When both the center and surround were stimulated together, the effects of cortical cooling often were predictable from the effects seen with stimulation of the center or surround alone. Of the 14 cells in which the cortical cooling had no effect on the response to center or surround stimulation alone, the cooling also had no effect on the response to simultaneous stimulation of both. Similarly, 11 of the cells that showed changes in response to center or surround stimulation during cortical cooling simply showed additive effects when both were stimulated. For example, the cell in Fig. 2B decreased its response to center stimulation (Fig. 2B1) and increased its response to surround stimulation (Fig. 2B2) during cortical cooling, and both components of the response showed similar changes to center plus surround stimulation during cortical cooling (Fig. 2B3). In contrast to these results, 10 cells showed changes in response to center plus surround stimulation during cooling that were not predictable from the changes in response to either region alone. Two examples are shown in Fig. 2. For the cell in Fig. 2A, cortical cooling increased the OFF response to surround stimulation (Fig. 2A2), but decreased the OFF response to center plus surround stimulation (Fig. 2A3). For the cell in Fig. 2C, cortical cooling had relatively minor effects on the response to stimulation of center (Fig. 2C1) or surround (Fig. 2C~) alone, but it nearly
414 abolished the response to center plus surround stimulation (Fig. 2C3). For these cells, the mechanisms underlying center-surround response antagonism appear to be increased by inactivation of visual cortex. A total of 5 cells showed changes of this sort, while 5 cells showed a decrease in center-surround response antagonism during cortical inactivation. As shown in Fig. 1, other response properties of lateral geniculate neurons were also seen to change when visual cortex was inactivated. Eleven neurons showed a statistically significant (Student's t-test, P < 0.05 in each case) decrease in spontaneous activity (23-100~ change, mean 59~), while 4 cells showed an increase (16-88 ~, mean 60 ~). Four Y-cells altered their response to drifting square wave gratings (test 7). One of these responded to a maximum of 0.44 cycles/° in the control and rewarm conditions and responded to 0.69 cycles/° in the cool condition. The other 3 ceils changed from 0.69 cycles/° to either 0.91 or 1.11 cycles/°. Changes also were seen in responses to tests that we used to classify X and Y cells. Thus, the maximum velocity to which the cells responded (test 6) was altered in some cases; 4 cells showed a decrease (23-66 ~ ) and 3 showed an increase in maximum velocity (17-67~). Six cells showed a slight but reliable increase in the latency of response to optic chiasm stimulation, ranging from 0.2 to 0.5 msec. In each case, the modal response latency returned to exactly the same value during the rewarm condition as during the control condition (care was taken to use the same stimulus parameters during the control, cool and rewarm conditions). Two cells changed their response to the test for linear spatial summation (test 8) during cortical inactivation. Both of these cells became non-responsive to the contrast-reversal stimulus during cortical cooling (although they continued to respond well to other stimuli). Finally, one cell showed a decrease in receptive field center size from 0.9 ° diameter in the control and rewarm conditions to 0.4 ° diameter during cortical cooling. Although changes in response were seen to tests used to classify cells as X or Y, none of the changes were both of sufficient magnitude and in the appropriate direction to produce a change in classification. Four main conclusions can be drawn from these findings. First, the vast majority of lateral geniculate neurons are influenced by visual cortical input. The proportion of cells showing changes during cortical cooling in the present study is higher than that in previous studies of the cat lateral geniculate10,13,14. Undoubtedly, this is due in part to the use of a large number of stimulus tests in the present experiments. It is possible that all of the cells would show cortical influences if additional tests were used. Second, cortical input modulates important response properties of the lateral geniculate neurons. For example, the basic receptive field center and surround response mechanisms, and the strength of their mutual antagonism, can be altered for many cells. Since center-surround response antagonism is thought to be involved in contour enhancement by the visual system, this result suggests that the cortico-geniculate pathway plays a role in the modulation of basic spatial visual processes. Third, the influence of the cortico-geniculate pathway is very complex. Both excitatory and inhibitory influences were observed on the same lateral geniculate neurons, in agreement with previous studies10,14,15. In addition, for a given cell a change in response to one
415 stimulus c o n d i t i o n could occur i n d e p e n d e n t of any changes in response to other stimulus conditions. Finally, the cortico-geniculate pathway has c o m p a r a b l e influences o n all cell types in the lateral geniculate, including n e u r o n s in both the X- a n d Ysystems. We would like to t h a n k Ms. K a t h y Vielhuber a n d Ms. Lynne O h m a n for their excellent technical assistance. This work was supported by U S P H S Postdoctoral Fellowship EY05259 (E.E.G.), U S P H S Research G r a n t s EY01916 a n d EY02545, a n d U S P H S Research Career Development A w a r d EY00089 (P.D.S.).
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