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Visual function in the ventral lateral geniculate nucleus of the cat
EXPERIMENTAL
NEUROLOGY
79,6 11-62 1 ( 1983)
Visual Function in the Ventral Lateral Geniculate Nucleus of the Cat CHARLES P. HUGHES AND DAVID
Y. K. CHI’
Department of ??euroIogy and Neurological Surgery (Neurology), Washington Universiiy School of Medicine. St. Louis City Hospital, 1515 L.ufayette Avenue, St. Louis, Missouri 63104 Received July 20, 1981; revision received September 16, 1982 The visual receptive fields of 293 single units in the ventral lateral geniculate nucleus of the cat were studied. In addition to the wide variety of types described by others, a group of units responding differentially to color was identified that included units responding particularly to blue and others with opponent color properties. Some units with spontaneous firing and witbout definite visual receptive fields were inhibited by stimulation of the optic cbiasm (OX), A study of latency of firing to OX stimulation suggested that these cells were driven by retinal ganglion cells of the W type. Onethird of all units studied were binocularly driven.
INTRODUCTION Although long accepted as an important substructure in the central processing of visual information, the ventral lateral geniculate nucleus (LGN,) has been relatively neglected in contrast to the dorsal lateral geniculate nucleus (LGN,). Although it is closely associated anatomically with the LGN, in every species of mammal studied, the LGN, is derived embryologically from the ventral thalamus, whereas the LGN, is derived from the dorsal thalamus. The retinal projection to the LGN, has been confirmed in many species (2,8,9), the input being binocular with a majority of the fibers coming from the contralateral eye. Though cytoarchitectural parcellations are less clear in the cat (13) than in other species (17), there is a general pattern of large cells Abbreviations: LGN,, LGNd-ventral, dorsal lateral geniculate nucleus; OX-optic cbiasm. I This study was supported by grants from tbe National Eye Institute (EYO-2535) and from the National Institute of Neurological and Communicative Disorders and Stroke (PSO-NS 04513-15-NSPB). Please address correspondence to Dr. Charles P. Hughes, address above. 611 0014-4886/83/03061 l-l 1%03.00/O
Comght 631983 by Academic Pres,Inc. All rights of reproduction in any fom reserved.
612
HUGHES
AND
CHI
receiving retinal input and smaller cells which do not. Projections to the LGN, (1, 6, 7, 11, 14) other than from the retina arise from various subcortical structures and portions of the visual cortex. Although many areas of visual cortex including 17, 18, 19, 21, lateral supra-sylvian, and 7, have been shown by lesion experiments (14) to project to the LGN, retrograde transport studies (11) have shown that the heaviest input comes from areas 17 and 20 with the cell bodies of origin being found in layer V as opposed to layer VI which projects to the LGNd. Physiological studies in the rabbit ( 15) were the first to demonstrate a wide variety of single neuron receptive-field properties. Such studies in the cat ( 10, 20) have shown an even wider group of properties including both concentrically and uniformly organized fields, motion-sensitive fields, and very large fields occupying much of the contralateral visual field. These studies suggested that single units in the LGN, might in some way be involved in the analysis of head and eye position in space. The present study was designed to investigate the receptive field properties of single units of the LGN, more extensively and to examine the nature of the retinal input. MATERIALS AND METHODS Cats weighing between 2 and 4 kg were anesthetized initially with intramuscular ketamine (25 mg/kg) and intravenous sodium thiopental was used for the remainder of the experiment (9 mg/kg every 1 to 2 h). In prolonged monitoring of the animals without paralysis this level of anesthesia was found to maintain coma but to permit the maintenance of reflexes, respiration, and occasional ear twitching. The animals were paralyzed with Flaxedil (5 mg/ kg/h), and maintained on artificial respiration. Extracellular single-unit recordings were made in the usual manner and peristimulus histograms were collected with the computer which also controlled the onset and offset of the stimulus. The eyes were focused on a tangent screen 1 m away with contact lenses and full mydriasis was obtained. Receptive fields were plotted on the screen using the smallest flash stimulus to which the cell would respond and were measured directly in degrees. Ambient light was usually maintained in the mesopic range ( 10 candelas/m*) and the response of all units to light of various wave lengths was surveyed with broad band filters (Kodak, > 600 nm [red], 430 to 460 nm [blue], 520 to 540 nm [green]) matched for luminance with white light as closely as possible with neutral density filters. For stimulation of the optic chiasm (OX) a three-electrode complex was placed at anterior 14 or 15 according to the atlas of Jasper and AjmoneMarsan (12) 2 1 to 23 mm below the cortical surface. Electrolytic lesions (10 to 40 pm) were made at the conclusion of microelectrode penetrations and the locus verified histologically.
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RESULTS To reach the relatively small LGNV , the LGNd was first located. The LGNV was then localized using the maps of the retinotopic organization of the LGN, prepared by Sanderson (20) and studying those visually responsive units lying just beneath the LGN, between Sanderson’s coronal 6 and 7, 11 to 11.8 mm lateral to the midline. The recordings to be considered here were all from cell bodies or processes of cells in the LGN, rather than from the axons of retinal ganglion cells. This judgment was based on the configuration and time course of the action potentials and, in many instances, the latency after OX stimulation. Many units recorded in the LGNV were studied for an hour or more and during this time irregular changes in the amount of spontaneous firing was noted. This did not seem related to visual stimulation, the level of ambient light, or to the injection of anesthetic drugs. No units showed rhythmic fluctuations in the rate of spontaneous potentials nor were long-term cyclic changes clearIy discernible. Receptive-Field Classes. Two hundred and ninety-three single units in the LGNV were studied and have been divided into five major groups as indicated in Table 1. The properties of units in categories I through III were largely similar to descriptions given by Spear et al. (2 1) and this report will emphasize certain features of the “spontaneous” units and a group not found by him that responded differentially to color. A more detailed analysis of receptive field properties of units encountered in the LGN, revealed considerable differences between the various groupings listed in Table I. Cells whose receptive fields were described as “uniform or concentric large fields” (group I) were distinguished from those with “uniform or concentric small fields” by having a more sluggish firing pattern. These units in group I could be further subdivided into those which were relatively sensitive to movement and those which were not. All these units responded clearly to stationary flashes but 53 of the 138 units in this category also gave a definite response to a moving stimulus over a wide range of speeds. Those which responded to stationary flash or only very slow movement (
614
HUGHES
AND CHI
TABLE 1 Single-Unit Response in the Ventral Lateral Geniculate Nucleus Group
Total units
Histologically verilied
I. Uniform or concentric large fields A. Responds to stationary stimuli primarily Concentric-10 Uniform-75 B. Movement-sensitive-53
138
58
36
28
III. Large receptive fields
33
13
IV. Color-coded units A. Blue responsive- 15 B. Opponent- 13
28
19
58
18
293
166
II. Uniform or concentric small fields Concentric-20 Uniform- 16
V. Spontaneous units Total
Many units in this group responded to stimulation of each eye separately. When a unit of any type in the LGN, responded to one eye only, it was invariably the contralateral one. An example of a unit with nearly equal binocular effect is shown in Fig. 1. When both eyes were stimulated (top histogram) there was a much more pronounced effect than if either eye was stimulated alone. Only stimulation of the contralateral eye produced a significant “off’ response. There was a distinctive group of units (group II) whose receptive fields were small and either concentrically (20 units) or uniformly (16 units) organized. Compared with units in group I, these had a much brisker response, rarely had a significant spontaneous rate of firing, and thus resembled units isolated in the LGNd and retina. For most of these (28 units), it was possible to be certain of their locus anatomically within the LGN, and all bore the characteristic action potential of a cell body as opposed to an axon. It is of interest that none of these showed a binocular effect but responded solely to stimulation of the contralateral eye. Although the receptive fields were all small with a mean size of 2.4”, they were found to 70” from the center of gaze. Most were found within the central 30” of vision, however. Group III (Table 1) contains units whose receptive fields covered the entire contralateral visual field. For both these and units in group I at or near the
VISION IN CAT VENTRAL
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10 API 2s
Binoc”‘o’ L ++ -1 I-. ,, 0+- B Contra l--F---
IPSI
/ m
ON
1 OFF
FIG. 1. A uniforn~ receptive field of a single unit in the ventral lateral geniculate nucleus showing a binocular effect. The receptive field is illustmted on the left showing a region uniformly responding to “on” and to “OR” throughout. Each hktogmm in this and subsequent b represents 16 trials and on the ordinate, 10 AP indicates 10 action potentials in a given bin.
vertical meridian there was a tendency for a small overlap (5 to 10’) into the ipsilateral visual field. These units had a more sluggish response to visual stimulation similar to group I and many had a high rate of spontaneous firing. Diligent searching never disclosed a smaller receptive field. A few of these units had steadily increasing response rates to increasing background illumination and were virtuahy silent in total darkness in a manner similar to the “ambient” cells of Spear et al. (21). Units of group IV (Table 1) were distinguished from those in group I by their differing responses to light of various wavelengths. All were uniformly organized More than one-half (15 units) responded primarily to blue (430 to 460 nm). There was usually a minimal response to red (>600 nm), a much reduced response to green (520 to 540 nm), and the response to blue was as good or much better than that to white light. Figure 2 shows such a unit with a response to blue greater than white and the other colors reduced The response to blue was so dominant in some of these units that the receptive field could be found only by searching with a blue stimulus. The other units in this group showed opponent color responses. All but one of these units responded with “on” to blue light, “off’ to red, and variably
HUGHES AND CHI
616
1OAP
White 2s
Blue
10”
Red
OFF [
ON-1
OFF
FIG.2. A uniform “on” receptive field showing a strong response to blue. The unit responded well to white and to blue, much less to green and minimally to red.
to green. Figure 3 shows such a unit. Although red did respond to “on,” the broader response was to “off.” Only one unit showed an opposite effect with red and green producing an “on” response and blue responding at “off.” A few of each of these -categories of color-responsive units were binocular; latencies to OX stimulation were similar to other LGN, units. The sites of the majority of these units were histologically verified. The final group V of LGN, units in Table 1 consisted of 58 cells that were isolated because of their spontaneous firing but failed to respond clearly to visual stimuli. Although occasionally a diffise flash of light seemed to cause a response, this effect could not be regularly repeated. These units did not vary their rate of firing with changes in the ambient light. Irregular fluctuations in the rate of spontaneous firing did occur, however, a finding noted in all other classes of LGN, units except group II which rarely bred spontaneously. A number of these units did respond to OX stimulation and usually exhibited latenciy characteristic of LGN” units (3 to 6 ms). One unit had a very long latency ‘of 19 ms and a few showed clear inhibition after OX stimulation. These cells would not respond directly to OX stimulation but instead exhibited an inhibition of spontaneous firing rate for 100 to 250 ms afterward.
VISION IN CAT VENTRAL
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BLUE
.‘oApL-
1
617
GENICULATE RED
Luuru.l...*
.
1 ,
,
,
I
c
LA&-“--L. YF-
m
ON
m
m
ON
~
no. 3. A uniform receptive field of a single unit in the LGN” showing an opponent color response. The receptive field was illustrated on the left showing a region uniformly responding to white light throughout.
Retinal Input to the Ventral Lateral Geniculate Nucleus. Single units in the LGN,, were routinely studied to determine whether they were monocularly or binocularly driven. Table 2 indicates those LGN, units whose reTABLE 2 Binocular Input to the Ventral Lateral Geniculate Nucleus
Receptive-field (RF) type
Units with RF centers within 45” of vertical meridian
Units driven bmacularly
Uniform or concentric large fields Stationary responses only Movement-sensitive
62 38
26 11
Uniform or concentric small fields Concentric Uniform
19 11
0 0
Large receptive fields
33
17
Colorunied
22
5
185
59
Total
units
618
HUGHES
AND CHI
MILLISECONDS
FIG. 4. The latency of units in LGNd and LGN, to stimulation of the optic chiasma. The abscissa indicates the latency in milliseconds from the stimulation and the ordinate indicates the number of units at each latency.
ceptive-field centers were located 45” or less from the center of gaze, the approximate range of the cat’s binocular vision. It includes those large receptive fields that covered the entire contralateral visual field. It is seen from Table 2 that about one-third of LGN, units had a demonstrable binocular input with the notable exception of group II. Most of those with binocular input responded predominantly to the contralateral eye, but a few showed an equal effect from either eye. Together with units in the LGN, a number of cells in the LGNd were briefly studied to determine the position of their receptive field and their latency to OX stimulation. A marked difference appeared in the latencies to such stimulation between units in the dorsal and ventral LGN as depicted in Fig. 4: there was nearly a complete separation in latencies. Most of those in the LGNd had latencies less than 3 ms (mean 2. l), whereas in the LGN, all but four units had latencies longer than 3 ms (mean 5.3) and some had latencies as long as 7 to 19 ms. All LGNd units were isolated in layers A and Al, none in the C laminae. Four units in the LGN, including two in the “spontaneous” category, had latencies in excess of 6 ms, suggestive of a multisynaptic pathway and two had particularly long latencies (a motionsensitive unit, 14.2 ms and a “spontaneous” unit, 19.8 ms). Receptive Field Position in the Cat S Visual Field. For those units whose receptive fields did not cover the entire contralateral visual field, there was a relationship between the size of the field and its eccentricity from the center of gaze. The results of this analysis for units whose receptive fields were types I or IV, are given in Fig. 5. There is a general pattern of larger fields farther from the center of gaze but this relationship was far from absolute. It was noted that in this sample there was no difference between monocularly and binocularly driven units. Only units whose receptive-field centers were 45” or less from the center were plotted here.
VISION IN CAT VENTRAL
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ECCENTRICITY
5. Receptive-field size and eccentricity from the center ofgaze. Open circles-monocularly driven units; closed circles-binocularly driven units. FIG.
VisuotopicArrangement within the Nucleus. There was no clear relationship between the receptive-field type and the location of the cell within this small nucleus for those units whose positions were histologicahy verified. However, units isolated near each other usually had the same type of receptive fields and the centers of these fields were usually in the same vicinity within the contralateral visual field. DISCUSSION Our findings co&m those of Spear et al. (21) but emphasize the new finding of color-coded units as well as an inhibitory response to OX stimulation in “spontaneous” units without definite visual receptive fields. Although cats are known to be able to distinguish colors, it has been difficult to identify single units in the central nervous system or retina that responded differentially to light of different wave lengths. Pearlman and Daw (18) found three opponent color cells in the LGNd and Cleland and Levick (4) identified six retinal ganglion cells responding with excitation to blue and inhibition to red. One of their units lacked the red inhibition but exhibited strong excitation to blue light. The LGN”, therefore, may represent a relatively important subcortical structure for color processing in the cat. The study of the latencies with which units in the LGNV responded to OX stimulation shows a sharp contrast with the upper layers of the LGNd. As noted by Spear et ai. (2 I), it is likely that the cells in the LGNV were being driven monosynaptically by retinal W cells as opposed to X and Y cells. The marked variability of receptive field types and generally sluggish 6ring observed here would be consistent with units driven by W cells. Cleland and Levick (3, 4) summarized the many types of “sluggish” or “rarely encountered” receptive fields of cat retinal cells that may be analogous to W cells.
620
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CT-II
These included some with larger fields, some that were directional, and some that gave color-coded responses. It is important to note that even the smallest receptive fields in the LGN, (2 to 2.5”) are larger than X cells and most Y cells observed in the cat retina or LGN,. That cells in the LGN, were often binocularly driven, in contrast to those in the LGN,, is not surprising in view of the bilateral retinal input. The LGN, receives fibers from each eye with a strong contralateral predominance. It is of interest, therefore, that few LGN, units had an equal response to both eyes. The vast majority of those that responded to stimulation of either eye, did so much better when the contralateral eye was stimulated, suggesting that individual neurons are connected to retinal ganglion cells with the same general binocular ratio that applies to the retinal input to the LGN, as a whole. Because of its anatomic connections, some investigators (5) have speculated that the LGN, might function in relation to eye movements. Motionsensitive units, however, were not as prominent as might have been expected and only a few showed directional selectivity. Before a careful study of the firing patterns of units in the LGN, in relation to eye movements is available, however, it would be premature to suggest that the LGN, played no part in visuomotor coordination. Its reciprocal connections with the pretectum and superior colliculus still make this a reasonable possibility. The presence of many units with fairly large uniformly organized receptive fields, or even fields that occupied the entire contralateral visual field, suggest strongly that the LGN, must be relaying information regarding general luminance to various structures. Some units here, as Spear et al. (21) also found, responded with steadily increasing firing rates to increasing illumination. One likely target for such information would be the suprachiasmatic nucleus, known to receive both retinal and LGN, input and to be a nucleus possibly involved in visually related neuroendocrine interactions. The most striking anatomic feature of the LGN, is the extent to which its projections overlap those of the retina at a subcortical level. Swanson et al. (22) suggested that this might indicate that the LGN, functions in the same way as does the isthmooptic nucleus in birds which projects efferent fibers to the retina. Physiological studies of this nucleus in birds (16, 19) have indicated that it has a generally excitatory effect on retinal ganglion cell activity. Although there is no evidence from these studies that the LGN, in the cat does not have a similar effect on retinal fibers at various levels, the diverse types of receptive field organizations that have been found in the LGN, suggest a more complex role for this nucleus. REFERENCES 1. BERMAN, 254.
N. 1917. Connections
of the pretectum
in the cat. J, Camp.
Neural.
174: 22~
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2. CAMPBELL, C. B. G. 1972. Evolutionary patterns in mammalian dienoephalic visual nuclei and their fiber comtections. Bruin Behav. Evol. 6: 218-236. 3. CLELAND, B. G., AND W. R. Luvrc~. 1974. Brisk and sluggish concentrically or~animd ganglion cells in the cat’s retina. J. Physiol. (London) 240: 42 1-456. 4. CLEUND, B. G., AND W. R. LEVICK. 1974. Propesties of rarely encmntezed types of ganglion cells in the cat’s retina and an overall class&&ion. J. Physiol. (London) 240: 457492. 5. EDWARDS, S. B., A. C. ROSIZNQUIST,AND L. A. PALMER 1974. An autoradiogmpbic study of ventral lateral geniculate projections in the cat. Bruin Res. 72: 282-287. 6. G~AIUM, J. 1977. An autoradiograpbic study of the effercnt connections of the superior colliculus in the cat. J. Comp. Neural. 173: 629-654. 7. GRAYBIEL, A. M. 1974. Visuo-cerebellar and cerebella-visual connections involving the ventral lateral geniculate nucleus. Exp. Brain Res. #): 303-306. 8. HAYHOW, W. R. 1958. The cytoarcbitecture of tbe lateral geniculate body in tbe cat in relation to the distribution of crowed and uncrossed optic fibers. J. Comp. Neural. 110:
l-64. 9. HOLL.XNDER, H., AND D. SANIDES. 1976. The retinal projection to the ventral part of tbe lateral geniculate nucleus: an experimental study with silver-impregnation methods and axoplasmic protein tracing. Exp. Brain Res. 26: 329-342. 10. HUGHES, C. P., AND S. B. ATER. 1977. Receptive field properties in the ventral lateral geniculate nucleus of the cat. Brain Res. 132: 163-166. I 1. HUGHES, C. P., AND D. Y. K. CHI. 198 I. A&rent projections to tbe ventral lateral nucleus in the cat. Brain Res. 207: 445-448. 12. JASPER,H. H., AND C. AJMONE-MARSAN. 1954. A stereotactic atlas of the diencephalon of the cut. Nat. Res. Council of Canada, Gttawa. 13. JORDAN, H., AND H. HOUNDER. 1972. Tbe structure of the ventral part of the lateral geniculate nucleus. A cyto- and myeloambitectonic study in the cat. J. Comp. Neural. 142: 259-272. 14. KAWAMURA, S., J. M. SPRAGUE, AND K. NIIMI. 1974. Corticofu8al projections from the visual cortices to the thalamus, pmtectum and superior colliculus in the cat. J. Comp. Neural. 158: 339-362. 15. MATHERS, L. H., AND G. G. MAsczm. 1975. Electrophyxiological and morphological properties of neurons in the ventral lateral 8eniculate nucleus of the rabbit. Exp. Neural. 46: 506-520. 16. MILES, F. A. 1972. CentriQal control of tbe avian retina. Iv Effects of reversible cold block of the istbmo-optic tract on tbe receptive field properties of cells in the retina and istbmooptic nucleus. Brain Res. 48: 131-145. 17. NIIMI, K., T. KANASEKI, AND T. TAK~I+XY~O.1963. The comparative anatomy of the ventral nucleus of the lateral geniculate body in mammals. J. Comp. Neural. 121: 313-323. 18. PEARLMN, A. L., AND N. N. DAW. 1970. Opponent color cells in tbe cat lateral geniculate nucleus. Science 167: 84-86. 19. PEARLMAN, A. L., AND C. P. HUGHES. 1976. Functional role of e.fferentsto the avian retina. II Effects of reversible cooling of the istbmo-optic nucleus J. Comp. Neural. 166: 123131. 20. SANDERSON,K. J. 1971. The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in tbe cat J. Comp. Net&. 143: 101-l 18. 21. SPEAR, P. D., D. C. SMITH, AND L. L. WILLIAMS. 1977. Visual nxeptiv&ield properties of single neurons in cat’s ventral lateral geniculate nucleus. J. Neurophysiool. 40: 390-409. 22. SWANSON,L. W., W. M. COWAN, AND E. G. JONES. 1974. An autoradiograpbic study of tbe efferent connections of tbe ventral lateral geniculate nucleus in tbe albino rat and the cat. J. Comp. Neural. 156: 143-164.
NEUROLOGY
79,6 11-62 1 ( 1983)
Visual Function in the Ventral Lateral Geniculate Nucleus of the Cat CHARLES P. HUGHES AND DAVID
Y. K. CHI’
Department of ??euroIogy and Neurological Surgery (Neurology), Washington Universiiy School of Medicine. St. Louis City Hospital, 1515 L.ufayette Avenue, St. Louis, Missouri 63104 Received July 20, 1981; revision received September 16, 1982 The visual receptive fields of 293 single units in the ventral lateral geniculate nucleus of the cat were studied. In addition to the wide variety of types described by others, a group of units responding differentially to color was identified that included units responding particularly to blue and others with opponent color properties. Some units with spontaneous firing and witbout definite visual receptive fields were inhibited by stimulation of the optic cbiasm (OX), A study of latency of firing to OX stimulation suggested that these cells were driven by retinal ganglion cells of the W type. Onethird of all units studied were binocularly driven.
INTRODUCTION Although long accepted as an important substructure in the central processing of visual information, the ventral lateral geniculate nucleus (LGN,) has been relatively neglected in contrast to the dorsal lateral geniculate nucleus (LGN,). Although it is closely associated anatomically with the LGN, in every species of mammal studied, the LGN, is derived embryologically from the ventral thalamus, whereas the LGN, is derived from the dorsal thalamus. The retinal projection to the LGN, has been confirmed in many species (2,8,9), the input being binocular with a majority of the fibers coming from the contralateral eye. Though cytoarchitectural parcellations are less clear in the cat (13) than in other species (17), there is a general pattern of large cells Abbreviations: LGN,, LGNd-ventral, dorsal lateral geniculate nucleus; OX-optic cbiasm. I This study was supported by grants from tbe National Eye Institute (EYO-2535) and from the National Institute of Neurological and Communicative Disorders and Stroke (PSO-NS 04513-15-NSPB). Please address correspondence to Dr. Charles P. Hughes, address above. 611 0014-4886/83/03061 l-l 1%03.00/O
Comght 631983 by Academic Pres,Inc. All rights of reproduction in any fom reserved.
612
HUGHES
AND
CHI
receiving retinal input and smaller cells which do not. Projections to the LGN, (1, 6, 7, 11, 14) other than from the retina arise from various subcortical structures and portions of the visual cortex. Although many areas of visual cortex including 17, 18, 19, 21, lateral supra-sylvian, and 7, have been shown by lesion experiments (14) to project to the LGN, retrograde transport studies (11) have shown that the heaviest input comes from areas 17 and 20 with the cell bodies of origin being found in layer V as opposed to layer VI which projects to the LGNd. Physiological studies in the rabbit ( 15) were the first to demonstrate a wide variety of single neuron receptive-field properties. Such studies in the cat ( 10, 20) have shown an even wider group of properties including both concentrically and uniformly organized fields, motion-sensitive fields, and very large fields occupying much of the contralateral visual field. These studies suggested that single units in the LGN, might in some way be involved in the analysis of head and eye position in space. The present study was designed to investigate the receptive field properties of single units of the LGN, more extensively and to examine the nature of the retinal input. MATERIALS AND METHODS Cats weighing between 2 and 4 kg were anesthetized initially with intramuscular ketamine (25 mg/kg) and intravenous sodium thiopental was used for the remainder of the experiment (9 mg/kg every 1 to 2 h). In prolonged monitoring of the animals without paralysis this level of anesthesia was found to maintain coma but to permit the maintenance of reflexes, respiration, and occasional ear twitching. The animals were paralyzed with Flaxedil (5 mg/ kg/h), and maintained on artificial respiration. Extracellular single-unit recordings were made in the usual manner and peristimulus histograms were collected with the computer which also controlled the onset and offset of the stimulus. The eyes were focused on a tangent screen 1 m away with contact lenses and full mydriasis was obtained. Receptive fields were plotted on the screen using the smallest flash stimulus to which the cell would respond and were measured directly in degrees. Ambient light was usually maintained in the mesopic range ( 10 candelas/m*) and the response of all units to light of various wave lengths was surveyed with broad band filters (Kodak, > 600 nm [red], 430 to 460 nm [blue], 520 to 540 nm [green]) matched for luminance with white light as closely as possible with neutral density filters. For stimulation of the optic chiasm (OX) a three-electrode complex was placed at anterior 14 or 15 according to the atlas of Jasper and AjmoneMarsan (12) 2 1 to 23 mm below the cortical surface. Electrolytic lesions (10 to 40 pm) were made at the conclusion of microelectrode penetrations and the locus verified histologically.
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RESULTS To reach the relatively small LGNV , the LGNd was first located. The LGNV was then localized using the maps of the retinotopic organization of the LGN, prepared by Sanderson (20) and studying those visually responsive units lying just beneath the LGN, between Sanderson’s coronal 6 and 7, 11 to 11.8 mm lateral to the midline. The recordings to be considered here were all from cell bodies or processes of cells in the LGN, rather than from the axons of retinal ganglion cells. This judgment was based on the configuration and time course of the action potentials and, in many instances, the latency after OX stimulation. Many units recorded in the LGNV were studied for an hour or more and during this time irregular changes in the amount of spontaneous firing was noted. This did not seem related to visual stimulation, the level of ambient light, or to the injection of anesthetic drugs. No units showed rhythmic fluctuations in the rate of spontaneous potentials nor were long-term cyclic changes clearIy discernible. Receptive-Field Classes. Two hundred and ninety-three single units in the LGNV were studied and have been divided into five major groups as indicated in Table 1. The properties of units in categories I through III were largely similar to descriptions given by Spear et al. (2 1) and this report will emphasize certain features of the “spontaneous” units and a group not found by him that responded differentially to color. A more detailed analysis of receptive field properties of units encountered in the LGN, revealed considerable differences between the various groupings listed in Table I. Cells whose receptive fields were described as “uniform or concentric large fields” (group I) were distinguished from those with “uniform or concentric small fields” by having a more sluggish firing pattern. These units in group I could be further subdivided into those which were relatively sensitive to movement and those which were not. All these units responded clearly to stationary flashes but 53 of the 138 units in this category also gave a definite response to a moving stimulus over a wide range of speeds. Those which responded to stationary flash or only very slow movement (
614
HUGHES
AND CHI
TABLE 1 Single-Unit Response in the Ventral Lateral Geniculate Nucleus Group
Total units
Histologically verilied
I. Uniform or concentric large fields A. Responds to stationary stimuli primarily Concentric-10 Uniform-75 B. Movement-sensitive-53
138
58
36
28
III. Large receptive fields
33
13
IV. Color-coded units A. Blue responsive- 15 B. Opponent- 13
28
19
58
18
293
166
II. Uniform or concentric small fields Concentric-20 Uniform- 16
V. Spontaneous units Total
Many units in this group responded to stimulation of each eye separately. When a unit of any type in the LGN, responded to one eye only, it was invariably the contralateral one. An example of a unit with nearly equal binocular effect is shown in Fig. 1. When both eyes were stimulated (top histogram) there was a much more pronounced effect than if either eye was stimulated alone. Only stimulation of the contralateral eye produced a significant “off’ response. There was a distinctive group of units (group II) whose receptive fields were small and either concentrically (20 units) or uniformly (16 units) organized. Compared with units in group I, these had a much brisker response, rarely had a significant spontaneous rate of firing, and thus resembled units isolated in the LGNd and retina. For most of these (28 units), it was possible to be certain of their locus anatomically within the LGN, and all bore the characteristic action potential of a cell body as opposed to an axon. It is of interest that none of these showed a binocular effect but responded solely to stimulation of the contralateral eye. Although the receptive fields were all small with a mean size of 2.4”, they were found to 70” from the center of gaze. Most were found within the central 30” of vision, however. Group III (Table 1) contains units whose receptive fields covered the entire contralateral visual field. For both these and units in group I at or near the
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615
10 API 2s
Binoc”‘o’ L ++ -1 I-. ,, 0+- B Contra l--F---
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1 OFF
FIG. 1. A uniforn~ receptive field of a single unit in the ventral lateral geniculate nucleus showing a binocular effect. The receptive field is illustmted on the left showing a region uniformly responding to “on” and to “OR” throughout. Each hktogmm in this and subsequent b represents 16 trials and on the ordinate, 10 AP indicates 10 action potentials in a given bin.
vertical meridian there was a tendency for a small overlap (5 to 10’) into the ipsilateral visual field. These units had a more sluggish response to visual stimulation similar to group I and many had a high rate of spontaneous firing. Diligent searching never disclosed a smaller receptive field. A few of these units had steadily increasing response rates to increasing background illumination and were virtuahy silent in total darkness in a manner similar to the “ambient” cells of Spear et al. (21). Units of group IV (Table 1) were distinguished from those in group I by their differing responses to light of various wavelengths. All were uniformly organized More than one-half (15 units) responded primarily to blue (430 to 460 nm). There was usually a minimal response to red (>600 nm), a much reduced response to green (520 to 540 nm), and the response to blue was as good or much better than that to white light. Figure 2 shows such a unit with a response to blue greater than white and the other colors reduced The response to blue was so dominant in some of these units that the receptive field could be found only by searching with a blue stimulus. The other units in this group showed opponent color responses. All but one of these units responded with “on” to blue light, “off’ to red, and variably
HUGHES AND CHI
616
1OAP
White 2s
Blue
10”
Red
OFF [
ON-1
OFF
FIG.2. A uniform “on” receptive field showing a strong response to blue. The unit responded well to white and to blue, much less to green and minimally to red.
to green. Figure 3 shows such a unit. Although red did respond to “on,” the broader response was to “off.” Only one unit showed an opposite effect with red and green producing an “on” response and blue responding at “off.” A few of each of these -categories of color-responsive units were binocular; latencies to OX stimulation were similar to other LGN, units. The sites of the majority of these units were histologically verified. The final group V of LGN, units in Table 1 consisted of 58 cells that were isolated because of their spontaneous firing but failed to respond clearly to visual stimuli. Although occasionally a diffise flash of light seemed to cause a response, this effect could not be regularly repeated. These units did not vary their rate of firing with changes in the ambient light. Irregular fluctuations in the rate of spontaneous firing did occur, however, a finding noted in all other classes of LGN, units except group II which rarely bred spontaneously. A number of these units did respond to OX stimulation and usually exhibited latenciy characteristic of LGN” units (3 to 6 ms). One unit had a very long latency ‘of 19 ms and a few showed clear inhibition after OX stimulation. These cells would not respond directly to OX stimulation but instead exhibited an inhibition of spontaneous firing rate for 100 to 250 ms afterward.
VISION IN CAT VENTRAL
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no. 3. A uniform receptive field of a single unit in the LGN” showing an opponent color response. The receptive field was illustrated on the left showing a region uniformly responding to white light throughout.
Retinal Input to the Ventral Lateral Geniculate Nucleus. Single units in the LGN,, were routinely studied to determine whether they were monocularly or binocularly driven. Table 2 indicates those LGN, units whose reTABLE 2 Binocular Input to the Ventral Lateral Geniculate Nucleus
Receptive-field (RF) type
Units with RF centers within 45” of vertical meridian
Units driven bmacularly
Uniform or concentric large fields Stationary responses only Movement-sensitive
62 38
26 11
Uniform or concentric small fields Concentric Uniform
19 11
0 0
Large receptive fields
33
17
Colorunied
22
5
185
59
Total
units
618
HUGHES
AND CHI
MILLISECONDS
FIG. 4. The latency of units in LGNd and LGN, to stimulation of the optic chiasma. The abscissa indicates the latency in milliseconds from the stimulation and the ordinate indicates the number of units at each latency.
ceptive-field centers were located 45” or less from the center of gaze, the approximate range of the cat’s binocular vision. It includes those large receptive fields that covered the entire contralateral visual field. It is seen from Table 2 that about one-third of LGN, units had a demonstrable binocular input with the notable exception of group II. Most of those with binocular input responded predominantly to the contralateral eye, but a few showed an equal effect from either eye. Together with units in the LGN, a number of cells in the LGNd were briefly studied to determine the position of their receptive field and their latency to OX stimulation. A marked difference appeared in the latencies to such stimulation between units in the dorsal and ventral LGN as depicted in Fig. 4: there was nearly a complete separation in latencies. Most of those in the LGNd had latencies less than 3 ms (mean 2. l), whereas in the LGN, all but four units had latencies longer than 3 ms (mean 5.3) and some had latencies as long as 7 to 19 ms. All LGNd units were isolated in layers A and Al, none in the C laminae. Four units in the LGN, including two in the “spontaneous” category, had latencies in excess of 6 ms, suggestive of a multisynaptic pathway and two had particularly long latencies (a motionsensitive unit, 14.2 ms and a “spontaneous” unit, 19.8 ms). Receptive Field Position in the Cat S Visual Field. For those units whose receptive fields did not cover the entire contralateral visual field, there was a relationship between the size of the field and its eccentricity from the center of gaze. The results of this analysis for units whose receptive fields were types I or IV, are given in Fig. 5. There is a general pattern of larger fields farther from the center of gaze but this relationship was far from absolute. It was noted that in this sample there was no difference between monocularly and binocularly driven units. Only units whose receptive-field centers were 45” or less from the center were plotted here.
VISION IN CAT VENTRAL
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ECCENTRICITY
5. Receptive-field size and eccentricity from the center ofgaze. Open circles-monocularly driven units; closed circles-binocularly driven units. FIG.
VisuotopicArrangement within the Nucleus. There was no clear relationship between the receptive-field type and the location of the cell within this small nucleus for those units whose positions were histologicahy verified. However, units isolated near each other usually had the same type of receptive fields and the centers of these fields were usually in the same vicinity within the contralateral visual field. DISCUSSION Our findings co&m those of Spear et al. (21) but emphasize the new finding of color-coded units as well as an inhibitory response to OX stimulation in “spontaneous” units without definite visual receptive fields. Although cats are known to be able to distinguish colors, it has been difficult to identify single units in the central nervous system or retina that responded differentially to light of different wave lengths. Pearlman and Daw (18) found three opponent color cells in the LGNd and Cleland and Levick (4) identified six retinal ganglion cells responding with excitation to blue and inhibition to red. One of their units lacked the red inhibition but exhibited strong excitation to blue light. The LGN”, therefore, may represent a relatively important subcortical structure for color processing in the cat. The study of the latencies with which units in the LGNV responded to OX stimulation shows a sharp contrast with the upper layers of the LGNd. As noted by Spear et ai. (2 I), it is likely that the cells in the LGNV were being driven monosynaptically by retinal W cells as opposed to X and Y cells. The marked variability of receptive field types and generally sluggish 6ring observed here would be consistent with units driven by W cells. Cleland and Levick (3, 4) summarized the many types of “sluggish” or “rarely encountered” receptive fields of cat retinal cells that may be analogous to W cells.
620
HUGHES
AND
CT-II
These included some with larger fields, some that were directional, and some that gave color-coded responses. It is important to note that even the smallest receptive fields in the LGN, (2 to 2.5”) are larger than X cells and most Y cells observed in the cat retina or LGN,. That cells in the LGN, were often binocularly driven, in contrast to those in the LGN,, is not surprising in view of the bilateral retinal input. The LGN, receives fibers from each eye with a strong contralateral predominance. It is of interest, therefore, that few LGN, units had an equal response to both eyes. The vast majority of those that responded to stimulation of either eye, did so much better when the contralateral eye was stimulated, suggesting that individual neurons are connected to retinal ganglion cells with the same general binocular ratio that applies to the retinal input to the LGN, as a whole. Because of its anatomic connections, some investigators (5) have speculated that the LGN, might function in relation to eye movements. Motionsensitive units, however, were not as prominent as might have been expected and only a few showed directional selectivity. Before a careful study of the firing patterns of units in the LGN, in relation to eye movements is available, however, it would be premature to suggest that the LGN, played no part in visuomotor coordination. Its reciprocal connections with the pretectum and superior colliculus still make this a reasonable possibility. The presence of many units with fairly large uniformly organized receptive fields, or even fields that occupied the entire contralateral visual field, suggest strongly that the LGN, must be relaying information regarding general luminance to various structures. Some units here, as Spear et al. (21) also found, responded with steadily increasing firing rates to increasing illumination. One likely target for such information would be the suprachiasmatic nucleus, known to receive both retinal and LGN, input and to be a nucleus possibly involved in visually related neuroendocrine interactions. The most striking anatomic feature of the LGN, is the extent to which its projections overlap those of the retina at a subcortical level. Swanson et al. (22) suggested that this might indicate that the LGN, functions in the same way as does the isthmooptic nucleus in birds which projects efferent fibers to the retina. Physiological studies of this nucleus in birds (16, 19) have indicated that it has a generally excitatory effect on retinal ganglion cell activity. Although there is no evidence from these studies that the LGN, in the cat does not have a similar effect on retinal fibers at various levels, the diverse types of receptive field organizations that have been found in the LGN, suggest a more complex role for this nucleus. REFERENCES 1. BERMAN, 254.
N. 1917. Connections
of the pretectum
in the cat. J, Camp.
Neural.
174: 22~
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2. CAMPBELL, C. B. G. 1972. Evolutionary patterns in mammalian dienoephalic visual nuclei and their fiber comtections. Bruin Behav. Evol. 6: 218-236. 3. CLELAND, B. G., AND W. R. Luvrc~. 1974. Brisk and sluggish concentrically or~animd ganglion cells in the cat’s retina. J. Physiol. (London) 240: 42 1-456. 4. CLEUND, B. G., AND W. R. LEVICK. 1974. Propesties of rarely encmntezed types of ganglion cells in the cat’s retina and an overall class&&ion. J. Physiol. (London) 240: 457492. 5. EDWARDS, S. B., A. C. ROSIZNQUIST,AND L. A. PALMER 1974. An autoradiogmpbic study of ventral lateral geniculate projections in the cat. Bruin Res. 72: 282-287. 6. G~AIUM, J. 1977. An autoradiograpbic study of the effercnt connections of the superior colliculus in the cat. J. Comp. Neural. 173: 629-654. 7. GRAYBIEL, A. M. 1974. Visuo-cerebellar and cerebella-visual connections involving the ventral lateral geniculate nucleus. Exp. Brain Res. #): 303-306. 8. HAYHOW, W. R. 1958. The cytoarcbitecture of tbe lateral geniculate body in tbe cat in relation to the distribution of crowed and uncrossed optic fibers. J. Comp. Neural. 110:
l-64. 9. HOLL.XNDER, H., AND D. SANIDES. 1976. The retinal projection to the ventral part of tbe lateral geniculate nucleus: an experimental study with silver-impregnation methods and axoplasmic protein tracing. Exp. Brain Res. 26: 329-342. 10. HUGHES, C. P., AND S. B. ATER. 1977. Receptive field properties in the ventral lateral geniculate nucleus of the cat. Brain Res. 132: 163-166. I 1. HUGHES, C. P., AND D. Y. K. CHI. 198 I. A&rent projections to tbe ventral lateral nucleus in the cat. Brain Res. 207: 445-448. 12. JASPER,H. H., AND C. AJMONE-MARSAN. 1954. A stereotactic atlas of the diencephalon of the cut. Nat. Res. Council of Canada, Gttawa. 13. JORDAN, H., AND H. HOUNDER. 1972. Tbe structure of the ventral part of the lateral geniculate nucleus. A cyto- and myeloambitectonic study in the cat. J. Comp. Neural. 142: 259-272. 14. KAWAMURA, S., J. M. SPRAGUE, AND K. NIIMI. 1974. Corticofu8al projections from the visual cortices to the thalamus, pmtectum and superior colliculus in the cat. J. Comp. Neural. 158: 339-362. 15. MATHERS, L. H., AND G. G. MAsczm. 1975. Electrophyxiological and morphological properties of neurons in the ventral lateral 8eniculate nucleus of the rabbit. Exp. Neural. 46: 506-520. 16. MILES, F. A. 1972. CentriQal control of tbe avian retina. Iv Effects of reversible cold block of the istbmo-optic tract on tbe receptive field properties of cells in the retina and istbmooptic nucleus. Brain Res. 48: 131-145. 17. NIIMI, K., T. KANASEKI, AND T. TAK~I+XY~O.1963. The comparative anatomy of the ventral nucleus of the lateral geniculate body in mammals. J. Comp. Neural. 121: 313-323. 18. PEARLMN, A. L., AND N. N. DAW. 1970. Opponent color cells in tbe cat lateral geniculate nucleus. Science 167: 84-86. 19. PEARLMAN, A. L., AND C. P. HUGHES. 1976. Functional role of e.fferentsto the avian retina. II Effects of reversible cooling of the istbmo-optic nucleus J. Comp. Neural. 166: 123131. 20. SANDERSON,K. J. 1971. The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in tbe cat J. Comp. Net&. 143: 101-l 18. 21. SPEAR, P. D., D. C. SMITH, AND L. L. WILLIAMS. 1977. Visual nxeptiv&ield properties of single neurons in cat’s ventral lateral geniculate nucleus. J. Neurophysiool. 40: 390-409. 22. SWANSON,L. W., W. M. COWAN, AND E. G. JONES. 1974. An autoradiograpbic study of tbe efferent connections of tbe ventral lateral geniculate nucleus in tbe albino rat and the cat. J. Comp. Neural. 156: 143-164.