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Properties of cells responding to visual stimuli in the rat ventral lateral geniculate nucleus
EXPERIMENTAL
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NEUROLOGY
66, 721-736 (1979)
of Ceils Responding to Visual Stimuli Ventral Lateral Geniculate Nucleus
I. SUMITOMO, M. SUGITANI,~. Depurtment
of Neurophysiology. Medicul
FUKUDA, AND K. IWAMA'
Instiiute of Higher Nervous Activity, School, Kita-ku, Osaka 530, Japan Received
May
in the Rat
Osaka
University
IS, 1979
Single-unit recordings were made of the ventral lateral geniculate nucleus (LGv) in the albino rat anesthetized with urethane. Visual receptive field properties as well as the characteristics of responses elicited by electrical stimuli to the optic tract and to the visual cortex were examined. Compared with the relay cells of the dorsal lateral geniculate nucleus (LGd), LGv cells were characterized by the following properties. (i) They responded to visual cortex stimuli orthodromically as well as to optic tract shocks. (ii) The postexcitatory inhibition they showed after single optic tract or visual cortex stimuli was only short-lasting, at most 100 ms. (iii) Conduction velocities of the optic nerve afferent fibers were mostly in the range of slow fibers, 2 to 10 m/s. (iv) The receptive fields were essentially homogeneous in type; about 90% of the sample of 53 cells were On-tonic. (v) Receptive field sizes were substantially large, from 6.3 to 45.6” (mean, 22.3”). (vi) On-tonic cells revealed a regular maintained discharge whose level changed monotonically as a function of the luminous intensity of the stimulating light. The functional implications of these findings were compared with those of the relay cells in the LGd.
INTRODUCTION The ventral lateral geniculate nucleus (LGv) of various mammals is distinguished from the dorsal lateral geniculate nucleus (LGd) with respect to fiber connections as well as cytoarchitecture. The LGd receives afferent impulses primarily from the retina and sends efferent impulses to the visual cortex (VC), thus functioning as a principal relay to the cerebrum. In contrast to this, the input-output relationship of the LGv is relatively complex. Receiving a major input from the retina (14- 16,19,20,23,27,28, Abbreviations: LGv, LGd-ventral, dorsal lateral geniculate nucleus, PSTHperistimulus time histogram, OT-optic tract, ON-optic nerve, VC-visual cortex. 1 The authors wish to thank Miss K. Takuwa for her secretarial help. 721 0014-4886/79/120721-16$02.00/O Copyright 0 1979 by Academic Press, Inc. All rights of reproduction in any form reserved.
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33,36), it projects to the pretectum (7,17,32,42), superior colliculus (7,32, 42), suprachiasmatic nucleus (7, 17, 32, 42), zona incerta (7, 32, 42), and pontine nuclei (7, 17, 32). From these complex interconnections, the LGv has been suggested to function as a center of visuomotor integration (17,42). Although the LGd has long been a subject of physiological studies in various mammals including the rat, only a few studies have been made of the LGv. As far as analyses of single units are concerned, the available data are those obtained from the rabbit (27) and cat (22,36). Though the rat LGv may be agood target of physiological studies because of its well-developed structure, no single-unit analysis has so far been attempted. Thus the objective of the present paper was, first, to characterize LGv cells of the rat on the basis of responses to electrical stimulation of the optic tract (OT) and the VC and, second, to clarify the visual properties of these cells. We attempted to determine how the physiological properties of LGv cells differ from those of the relay cells (P-cells) of the LGd (12). This will aid us in understanding the significance of the differentiation of the rat lateral geniculate nucleus (LGN) into the dorsal and ventral parts. Some of the results were reported previously in abstract form (13). METHODS General Preparation. Albino rats, weighing 250 to 300 g, were anesthetized with urethane (i.p., 1.2 g/kg) and fixed to a stereotaxic apparatus so as to fit the Fifkova and MarSala coordinates (8). One percent procaine was administered at all pressure points and surgical wounds. The animals were immobilized with gallamine triethiodide (i.p., 40 mg/kg) and respiration was maintained artificially through a tracheal cannula. Additional small amounts of urethane and gallamine triethiodide were applied as required. Electrical Stimulation. To activate LGN cells, single electrical shocks were applied to the OT and VC. For each of the stimulating sites, a bipolar electrode insulated except at the tip was introduced stereotaxically. Adequate placement of these electrodes was ascertained by recording characteristic responses to single-flash stimuli. When the contralateral optic nerve (ON) was to be stimulated, a U-shape bipolar electrode of silver wire was hooked under the nerve just behind the eyeball. Electrical shocks were of rectangular pulses 0.01 to 0.1 ms in duration with intensities less than 50 V. Visual Stimulation. Visual stimuli of diffuse light or light spots were projected onto a tangent screen (100 cm high and 118 cm wide). To define the boundaries of the receptive fields, a small spot of 1 to 2” or a large spot of 5 to lo” was turned on and off or moved across the field. The pupil of the
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right eye was dilated by a topical application of 1% atropine sulfate. The cornea was protected with a contact lens with zero power. The tangent screen was placed vertically at an angle of 32” to the midsagittal plane of the animal and 30 cm distant from the eye. As described in detail previously (12), on the tangent screen so placed, the area centralis was at about 60 from the zero vertical axis and about 20” above the zero horizontal axis. Here, the zero vertical and zero horizontal axes were taken as the intersections with the tangent screen of the animal’s midsagittal plane and of the horizontal plane passing through the eye, respectively. The visual field covered by the screen extended 60” in the nasal, 60” in the temporal, 40” in the upward, and 50” in the downward directions from the estimated projection of the area centralis. The luminous intensities of the light spots varied from 20 to 200 cd/m2. Background illumination was kept at about 3 cd/m2. Recordings. Unitary activities of the LGN cells were recorded extracellularly with glass pipet microelectrodes filled with 2 M NaCl or 3 M KCI. They were amplified conventionally and photographed from the screen of an oscilloscope. Responses to electrical or photic stimuli were processed by means of an on-line electronic computer (DAB-5101, Nihon Koden Kogyo) to make peristimulus time histograms (PSTHs). For responses to electrical stimulations, 50 trials were assembled in one PSTH using 256 bins 2 ms in width. For responses to photic stimuli, unit activities during 10 trials were added usually with an analysis time covering 12.8 s (bin width, 50 ms; number of bins, 256), but in occasional cases a shorter analysis time was used (bin width, 20 ms; number of bins, 128). In some experiments microelectrodes filled with 3 M KC1 saturated with fast green FCF dye were used. Through these electrodes negative currents of 10 to 20 PA were passed for about 10 min to produce dye-marking. The marked sites were verified histologically in the 70-Km-thick tissue sections fixed with 10% Formalin and stained with Calbol-thionine. RESULTS Zdentijication of LGv Cells. While advancing a microelectrode vertically through the LGN, we first encountered activities of P-cells in the LGd. As reported previously, P-cells were characterized by antidromic responses to single VC stimuli and orthdromic responses to OT stimuli, and by a series of late discharges following the initial excitation in both OT- and VC-induced responses (2,3,9,11,29,39,40). Sample records of a P-cell are presented in Fig. 1A. The upper right records in A-I and A-II show initial spike discharges elicited by single OT and VC stimuli, respectively. As is characteristic of antidromic invasion, the spike activated by VC
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FIG. 1. Comparisons of LGv cells and P-cells in response properties to electrical shocks (A and B) and in recording depths (C). A-responses of a P-cell to optic tract (OT) (I) and visual cortex (VC) (II) shocks. B-responses of a LGv cell to OT (I) and VC (II) shocks. Records in the upper right of each peristimulus time histogram (PSTH) are superimposed traces of the initial spike response; the arrow in A-II indicates a notch on the positively going stroke of the spike, characteristic of antidromic activation. The time calibration for each superimposed trace was 2 ms. Note a significant fluctuation of the latency in the superimposed traces in B-II. In the PSTHs electrical stimuli were applied at the time indicated by S on the abscissa. Note the clear late discharges only in the PSTHs of A-I and A-II. C-distribution of recording depths of 74 ventral lateral geniculate cells (shaded columns) and of 76 P-cells (open columns). Ordinate, depth from the cortical surface; abscissa, number of units. For details, see text.
stimulation revealed a notch at its positively going stroke (arrow in the inset record of A-II). The first prominent late discharge was present in the PSTHs in A-I and A-II. The latency of the late discharge, measured at the peak in the PSTH, was usually on the order of 200 to 300 ms. During the period between the initial spike discharge and the late discharge, spontaneous activity was completely silenced. The same was also true during the period after the late discharge. These observations for P-cells are consistent with previous reports (2-4, 9, 39, 40). Cells identifiable as P-cells were recorded from within about 5 mm from the cortical surface. Upon further advancement of the microelectrode, we encountered a group of cells with the following properties in common: (i) Single or occasionally double spike responses were elicited at short latencies by OT stimuli, (ii) no antidromic responses were elicited by single VC stimuli, and (iii) no late discharges appeared after OT- or VC-induced early responses. These response properties led us to assume that the cells were in the LGv. Sample responses of an LGv cell are presented in Fig. 1B. This cell responded to OT stimuli with double spikes, as seen in the upper right records of B-I. The initial spike activated from the VC revealed a significant fluctuation in latency as a characteristic of transsynaptic activation (B-II). In the PSTHs made after OT and VC stimulation, only a
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short-lasting suppression of spontaneous discharges appeared without producing any clear late discharges (B-I and B-II). The suppression after the initial response lasted about 30 to 100 ms. Because it has been observed histologically that LGv cells do not project to the VC (42) but receive corticofugal afferents (16,27,36), transsynaptic activation from the VC can be assumed as a criterion for the identification of LGv cells. In Fig. 1C are plotted the depths of recording sites for cells identified as LGv cells (shaded columns) according to the above characteristics, in comparison with the distribution of recording depths of P-cells (open columns). It is clear that the LGv cells identified on the basis of physiologic characteristics are certainly distributed below the distribution of P-cells, with a little overlap around the depth of 5.0 to 5.2 mm from the cortical surface. More direct identification of recording sites for LGv cells was made with microelectrodes filled with fast green dye. The data from a typical experiment are presented in Fig. 2. In this experiment the LGv was explored in one frontal plane along seven vertical tracks spaced 100 pm apart mediolaterally. Exploration was made with the same microelectrode, and for each LGv cell encountered, its coordinates were noted. Finally, for an LGv cell recorded at the deepest point of the most lateral track, the dye was deposited and the spot was delineated as indicated with an arrow in the photomicrograph of Fig. 2A. This dye spot was taken as a reference for plotting the recording sites of all the LGv cells encountered in this experiment onto outlines of the LGN (Fig. 2B). It is clear that the electrophysiologically identified LGv cells were all within the anatomic confines of the LGv. Along the two most medial tracks a number of cells were recorded, but none of them was excited by OT stimuli or was visually responsive. This observation is consistent with the histological finding that retinal afferents terminate exclusively in the lateral division of the LGv (16, 19, 20, 42). Postexcitatory Inhibition. As referred to in the preceding section, LGv cells revealed no late discharges after a single OT or VC stimulus. This is different from the property of P-cells in that with either type of stimulation, almost without exception the initial excitation is followed by a series of late discharges. The late discharge in the P-cells has been interpreted as a postinhibitory rebound excitation; the inhibition preceding the late discharge appears as a lack of spontaneous discharges and a decreased responsiveness to the testing OT stimuli (3, 9, 39, 40). In the following experiment we examined how quickly LGv cells recovered responsiveness after being excited by OT stimuli. Because LGv cells ceased spontaneous discharges only a short time after the initial excitation by OT stimuli, as revealed in PSTHs, we expected that the post-excitatory recovery determined with double OT stimuli would be accomplished relatively quickly.
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A
0.5 mm FIG. 2. Histological identification of recording sites. A-photomicrograph of a frontal section of the lateral geniculate nucleus. Arrow indicates the site of the green spot deposited after recording from a typical ventral lateral geniculate (LGv) cell. B-a diagrammatic presentation of recording sites of LGv cells responding to optic tract (OT) stimuli: Each of the filled circles represents the recording site of one LGv cell. Seven electrode tracks, separated by 100 pm, are indicated with vertical arrows in the diagram. The recording site corresponding to the dye mark in A is indicated by a horizontal arrow. Note that in the two most medial tracks no cells were activated by OT stimuli.
To determine the recovery curve, double stimuli were applied to the OT. The intensity was set for each cell at twice the threshold for triggering the initial spike and the stimulus interval was varied from 2 to 500 ms. The degree of postexcitatory inhibition after the first stimulus was judged by the firing probabilities to the second stimulus. Samples of the recovery curve in the LGv cells are presented in Figs. 3A and B. Of 33 cells tested, 28 (85%) showed a smooth recovery such as shown in Fig. 3A. Unfilled and filled circles represent the most rapidly and slowly recovering cells in this group, respectively. Even in the case of the most slowly recovering cells (filled circles), the responsiveness started to reappear 20 ms after the first stimulus and completely recovered by 40 ms. All cells which revealed
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smooth recovery curves showed a simple and short-lasting silent period in the spontaneous discharges, as exemplified in the PSTHs of Fig. 3D. The minor group, consisting of five cells (15%), showed an oscillatory recovery, as exemplified by the two cells plotted with filled and unfilled circles in Fig. 3B. In these cases the recovery curve consisted of two periods of inhibition, one occurring within 10 ms after the primary excitation and the other appearing from 30 to 100 ms after. Usually the late inhibition was weaker than the earlier one. Cells showing this type of recovery were characterized by a complex PSTH pattern associated with single OT stimuli; as seen in Fig. 3E, the silent periods were interrupted by a short-lasting excitation. Figures 3C and F show examples of the recovery curve and the PSTH of P-cells, respectively. In Fig. 3C, five cells are plotted together, all showing a long-lasting complete inhibition to as much as 100 or 200 ms and a weak inhibition recurring at about 300 ms. It took more than 500 ms to attain complete recovery. Correspondingly, a complete suppression in the PSTH was apparent before and after the late discharge (Fig. 3F). In summary, this series of experiments made it clear that postexcitatory inhibition in LGv cells was far weaker than in P-cells of the LGd. Affeerent Conduction Velocity. Response latencies to single OT stimuli were measured in 125 LGv cells, and their distribution is shown in Fig. 4A. It covers a range from 1.15 to 5.17 ms (mean, 3.06 ms). Of these cells, 98 (78.4%) were activated transsynaptically from the VC as well. The latency D
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FIG. 3. Comparisons of the postexcitatory inhibition between ventral lateral geniculate (LGv) cells (A, B, D, and E) and P-cells (C and F). A-C-postexcitatory recovery curves made by double stimuli applied to the optic tract (OT). Ordinates, response probabilities to the test OT shock; abscissae, conditioning-testing intervals. Two representative LGv cells are plotted for A and B, identified with unfilled and filled circles, and five P-cells are plotted in C. D and E-PSTHs made after single OT stimuli for the LGv cell depicted in A and B with filled circles, respectively. For details. see text.
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FIG. 4. Latency histograms of ventral lateral geniculate (LGv) cells to stimuli of the optic tract (A) and visual cortex (B), and distributions of afferent conduction velocities for LGv cells (C)and P-cells (D). In A and B, 125 and 98 LGv cells were plotted, respectively. In C and D, 74 LGv cells and 79 P-cells were plotted, respectively. Histogram D is reconstructed from the original published previously (38).
histogram for the VC-induced responses is depicted in Fig. 4B. The latency was distributed from 1.20 to 8.45 ms (mean, 3.67 msec). Twenty-seven other cells (21.6%) could not be activated from the VC, probably because placement of the stimulating electrodes was not adequate. In 74 LGv cells the response latencies to stimulation of the ON and OT were both measured, allowing us to calculate conduction velocities of ON fibers driving these cells. Taking the distance from the ON to the OT electrode as 9 mm (10,38), the conduction velocities were calculated as the distance divided by the difference in latencies between the responses to ON and OT stimulation. The range of the conduction velocity turned out to be from 2.0 to 13.0 m/s (mean, 6.0 m/s), as shown in Fig. 4C. The velocity histogram previously reported by Sumitomo et al. (38) for P-cells of the LGd is shown in Fig. 4D. It is clear that except for the two cells at bins of 11 and 13 m/s, most LGv cells were distributed in the range within 10 m/s. By contrast, of 79 P-cells plotted in Fig. 4D, 36 cells (45%) were innervated by ON fibers having velocities faster than 10 m/s. Therefore, we could conclude that the LGv cells are innervated by relatively slow-conducting ON fibers, whereas the LGd cells are innervated by ON fibers having a wide range of velocities. The synaptic delay was measured for the LGv cells by the same method applied previously for the P-cells (38). The mean synaptic delay in 74 LGv cells was 0.64 ms. This value is comparable to the 0.73 ms which was obtained for P-cells (38). Thus LGv cells can be assumed to be innervated monosynaptically by ON fibers as are the P-cells in the LGd.
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The maintained activity varied from cell to cell in a sample of LGv cells: Some were virtually silent, whereas others discharged at frequencies as high as 30 to 40 spikes per second. However, as a characteristic of most LGv cells, their maintained discharge altered significantly as the background illumination changed. In general, the discharge increased as the luminance was increased, and as long as the luminance was kept constant, the maintained discharge was also steady. Examples of this behavior will be presented in the following section. Visual Receptive Field Properties. A total of 56 LGv cells was subjected to the analysis of visual responses. Except for three cells responding to the ipsilateral eye, all others responded exclusively to the contralateral eye. There were no binocularly driven cells. For 53 LGv cells, receptive field properties were analyzed with the contralateral eye. On the basis of receptive field center properties, LGv cells were classified into four types: On-tonic, On-inhibited, On-Off-inhibited, and movement-sensitive. Forty-seven of 53 LGv cells (88.7%) were of the On-tonic type and the remainder were classified as one of the other three types: four On-inhibited, one On-Off-inhibited, and one movement-sensitive cells. Sample responses of On-tonic, On-inhibited, and On-Off-inhibited types are presented in Fig. 5. The PSTHs were made by averaging responses to flashing of a light spot of a size equal to the receptive field center size. As with the sample presented in Fig. 5A, On-tonic cells showed tonic discharges during activation of the receptive field center by a light spot. In contrast, the On-inhibited type was characterized by a high level of maintained discharges in the absence of light stimulation and by their suppression upon the onset of a light spot (Fig. SB). Because of the apparent lack of Off response, this type of cell was called the On-inhibited type rather than Off-center. As exemplified in Fig. 5C, the On-Offinhibited type had a moderate level of maintained discharges which was phasically suppressed at either On or Off of a centered light spot. MaintainedDischarge.
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FIG. 5. Three receptive field types of ventral lateral geniculate cells. For each peristimulus time histogram (PSTH), 10 consecutive responses to a stationary spot flashed on and off were compiled. Total analysis time was 12.8 s in A and B and 2.56 s in C. The trace below the PSTHs is upward as the luminance of the activated region increases and downward as it decreases.
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We tried to detect any antagonistic or suppressive field surrounding the center by flashing a small light spot outside the center or by flashing a large spot covering both the center and surround regions. Except for four On-tonic cells (7.5%) having incomplete Off-surrounds, notable surround could not be detected in the other 49 LGv cells tested. Such rare occurrence of the receptive field surround was also noted for the P-cells (12). All 10 cells of the On-tonic type tested decreased their maintained discharges in proportion to a decrease in the intensity of light shining on the field center. A typical case is shown in Fig. 6. In the left column, PSTHs at three different intensities of light are presented, with corresponding oscilloscope traces in the right columns (A-II, B-II, and C-II). The spot intensity was decreased from 200 cd/m2 (A) to 67 cd/m* (B) and further to 20 cd/m2 (C). The mean discharge frequencies were 14.6 (A), 8.3 (B), and 4.3 (C) spikes per second, respectively. Receptive Field Size. In 43 LGv cells, receptive field boundaries could be determined by flashing spots of various sizes. The receptive fields were always circular or square with no appreciable surround components. The center size was 6.3 to 45.6” (mean, 22.3’) in diameter, as presented in Fig. 7B. In Fig. 7A are reproduced the data published previously for the P-cells (12). Although the receptive field sizes of P-cells were distributed widely from 2.1 to 41”, more than 90% of the sample were distributed within 15”. By contrast, about 80% of the LGv cells had receptive fields larger than 15”. There was no difference in the field size among the four receptive field types of the LGv cells. Thus, the LGv cells, as a whole, had receptive fields significantly larger than those of P-cells.
FIG. 6. Sample responses of an On-tonic ventral lateral geniculate cell to a centered light stimulus of graded intensities. Luminous intensity of a light spot was decreased from 200 cd/m2 (A) to 20 cd/m* (C). A-I, B-I, and C-I, the PSTHs obtained at the three different intensities of illumination. The trace below the PSTHs indicates the output of the photodiode placed in the center of the receptive fields. A-II, B-II, and C-II, oscilloscope traces of the discharges maintained during the three stimulus conditions. Note the regular discharges at each light intensity.
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RF Size FIG. 7. A comparison of the receptive field (RF) center sizes ofthe ventral lateral geniculate (LGv) cells and P-cells. A-frequency distribution histogram for P-cells (N = 214). B-frequency distribution histogram for LGv cells (N = 53). Mean sizes (*SD) were 7.8 4 5.4” in A and 22.3 4 10.1” in B, respectively. Histogram A is redrawn from the original published previously (12).
Distribution of Receptive Field Positions. To see if there was a tendency for the recorded LGv cells to represent preferentially a particular part of the visual field, all the receptive fields were replotted on the same sheet of paper by taking the area centralis as a reference. We found that the upper temporal field was less frequently represented than the other three quadrants: three cells in the upper temporal field, 14 cells in the lower temporal field, 14 cells in the lower nasal field, and 16 cells in the upper nasal field. This contrasts sharply with a relatively even representation of the visual fields by P-cells of the LGd (12). However, our sample of LGv cells was small and we cannot think of any physiologically significant implications of this finding. DISCUSSION
From the analysis of the responsiveness of visual neurons to electrical stimulation of the optic pathway, several important characteristics
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emerged to distinguish LGv cells from P-cells of the LGd. First, many LGv cells were activated transsynaptically from the VC. Second, postexcitatory inhibition, assessed by lowered responsiveness to testing stimuli or by silencing of spontaneous discharges after single OT shocks, was only short-lasting. Third, LGv cells were innervated by relatively slowconducting ON fibers. The LGv cells were distinguished from P-cells in visual properties as well. First, under a given condition of background illumination many LGv cells showed regular maintained discharges and the activity changed monotonically as the level of illumination was shifted. Second, LGv cells were fairly homogeneous in terms of the receptive field type, that is, a great majority (88.7%) was of the On-tonic type. Third, the size of the receptive field center was significantly larger than that of the P-cells. These visual properties would indicate that cells of the rat LGv are less differentiated from each other than P-cells in the LGd, hence their function would be primitive in nature. Inhibitory Mechanism within the Ventral Lateral Geniculate Nucleus. A prominent feature in the LGv cells is that the postexcitatory inhibition is only poorly developed. This contrasts sharply with P-cells of the LGd. Since the first report by Burke and Sefton (2-4), it has been repeatedly confirmed that P-cells of the LGd undergo a long-lasting postexcitatory inhibition (9,39,40). Burke and Sefton originally assumed that the activity of interneurons within the LGd was responsible for the postexcitatory inhibition. A more recent report by Sumitomo et al. (40), however, presented evidence that the inhibition is caused by perigeniculate reticular neurons (41) located in a restricted region of the thalamic reticular nucleus immediately rostra1 to the LGd. Furthermore, Sumitomo and Iwama (39) succeeded in recording from intrinsic neurons within the rat LGd and suggested that the intrageniculate inhibition ascribable to the action of these intrinsic neurons might be only subtle. In view of these recent advances in the understanding of the inhibitory mechanism within the rat LGd, an apparent lack of long-lasting inhibition in the LGv cells led us to conclude that these cells were free from the inhibition caused by perigeniculate reticular neurons. Retinal Input. In a preceding paper on P-cells of the rat LGd, we pointed out that most P-cells can be likened to either Y- or W-type relay cells of the cat LGd (12). The Y-type relay cells are characterized by the inputs from fast-conducting retinal ganglion cells, phasic responses to centered spots flashed on or off, and a preference for fast-moving light stimuli. By contrast, W-type relay cells have the following properties in common: innervation by slowly conducting retinal afferent fibers and a preference for slowly moving stimuli. In the W-homologous P-cells of the rat LGd, several subgroups were identified: On-tonic, On-Off-phasic, On-inhibited, motion-sensitive, and so on. According to this classification, the LGv cells
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are homologous to the W-type cells for the following reasons. First, axonal conduction velocities of retinal afferent fibers are restricted to the slow range (see Fig. 4C). Second, all the four receptive field types (On-tonic, On-inhibited, On-Off-inhibited, and motion-sensitive) were found in the W-homologous P-cells of the rat LGd as well (12). Further, though not studied for all cells, most LGv cells preferred very slow spot movements. It is most impressive that a monotonic change in maintained activity observed in most On-tonic LGv cells was exactly the same as observed in On-tonic W-type ganglion cells of the cat retina. (37). Another important feature for understanding the mode of retinal inputs to the LGv was that the receptive field size was about three times larger in diameter than that of retinal ganglion cells. The average size of the field in the present samples of LGv cells was 22.3”, whereas Brown (1) reported 7.5” for the rat’s retinal ganglion cells. In another study we reported the average size as 7.8” for P-cells in the rat LGd (12). Thus, it appears most conceivable that about three retinal ganglion cell axons converge upon one LGv cell, whereas a one-to-one connection exists between retinal ganglion cell axons and P-cells in the LGd. Comparison with Other Animals. Visual properties of LGv cells were reported for the monkey (6), rabbit (27), and cat (22, 35). In the monkey, DeValois (6) showed that cells of the perigeniculate nucleus, homologue of the LGv of lower mammals, gave prolonged On-responses to presentation of a light stimulus in a manner similar to the rat’s On-tonic LGv cells. In the rabbit LGv, Mathers and Massetti (27) categorized three types of cells: concentric, uniform, and others. Unfortunately, however, they made no special note as to whether or not these cells were On-tonic. A more recent and extensive study was made by Spear et al. (35) for the cat LGv. They identified On-tonic cells which behaved in the same way as reported in the present paper for the rat LGv. However, the sampling frequency of these cells was about 10% of all visually responsive cells, which is significantly smaller than the frequency (88.7%) of the On-tonic cells sampled in the present study. They noted, in addition, that a vast majority of cells with uniform receptive fields (35.3% of visually responsive cells) and with concentric ones (25.2%) showed On-responses. Thus, the LGv in the cat and the rat share a property in common, that is, the predominance of On-center receptive fields. Functional Implications. It has been suggested that the LGv is involved in visuomotor functions (17, 42). Electrophysiological studies for the cat and monkey showed that the LGv cells change activities in association with head and eye movements (5, 26, 31). On the other hand, in behavioral studies of the rat, the LGv was shown to function in brightness discrimination (2 1,25). The present finding that the rat LGv consists mostly of cells carrying luminous information appears to corroborate these
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behavioral studies. Another possible function of the LGv is in relation to the mediation of the pupillary light reflex. Polyak (30) was the first to ascribe mediation of the pupillary light reflex to the perigeniculate nucleus, homologue in the primate of the LGv of lower mammals. More recently Legg (24) provided evidence in the rat that lesions of the LGv resulted in mydriasis and suggested further that the LGv could be the primary relay to the pretectum, which has long been assumed as the center for the pupillary light reflex. The present finding that the rat LGv consists mainly of On-tonic cells with large receptive fields supports Legg’s suggestion (24). Furthermore, in single-unit studies of the rat’s pretectum, Siminoff et al. (34) reported that in the ventral part there were many On-tonic cells with large receptive fields and that these cells changed their maintained discharges depending on the intensity of ambient illumination. From these two findings, it is suggested that the LGv and the ventral pretectum constitute a system for mediating visual information necessary for the pupillary light reflex. During the preparation of this manuscript, a similar work on the rat LGv was published by Hale et al. (18). They reached the same conclusions as ours, in that the LGv cells are essentially free from the postexcitatory inhibition after single OT stimuli and that a great majority of these cells revealed On-tonic properties in their visual responses. REFERENCES 1. BROWN, J. E. 1965. Dendritic fields of retinal ganglion cells of the rat. J. Neurophysiol. 28: 1091-1100. 2. BURKE, W., AND A. J. SEFTON. 1966. Discharge patterns of principal cells and inhibitory intemeurones in lateral geniculate nucleus of rat. J. Physiol. (London) 187: 201-212. 3. BURKE, W., AND A. J. SEFTON. 1966. Recovery of responsiveness of cells of lateral geniculate nucleus of rat. J. Physiol. (London) 18’7: 213-229. 4. BURKE, W., AND A. J. SEFTON. 1966. Inhibitory mechanism in lateral geniculate nucleus of rat. J. Physiol. (London) 187: 231-246. 5. BUTTNER, U., AND A. F. FUCHS. 1973. Influences of saccadic eye movements on unit activity in simian lateral geniculate and pregeniculate. J. Neurophysiol. 36: 127- 141. 6. DEVALOIS, R. L. 1960. Color vision mechanism in the monkey. J. Gen. Physiol. 43: 115-128. 7. EDWARDS, S. B., A. C. ROSENQUIST, AND L. S. PALMER. 1974. An autoradiographic study of ventral lateral geniculate projections in the cat. Bruin Res. 72: 282-287. 8. FIFKOVA, E., AND J. MARSALA. 1967. Stereotaxic atlases for the cat, rabbit and rat. Pages 426-467 in J. BURES, M. PETR.~~~, AND J. ZACHER, Eds., Elecrrophysiological Methods in Biological Research. Academic Press, New York. 9. FUKUDA, Y. 1973. Differentiation of principal cells of the rat lateral geniculate body into two groups; fast and slow cells. Exp. Brain Res. 17: 242-260. 10. FUKUDA, Y. 1977. A three-group classification of rat retinal ganglion cells: histological and physiological studies. Brain Res. 119: 327-344. 11. FUKUDA, Y., AND M. SUGITANI. 1974. Cortical projections oftwo types ofprincipal cells of the rat lateral geniculate body. Bruin Res. 67: 157-161.
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12. FUKUDA, Y., M. SUGITANI, I. SUMITOMO, AND K. IWAMA. 1979. Receptive-field properties of cells in the dorsal part of the albino rat’s lateral geniculate nucleus. Jap. J. Physiol.
29.
13. FUKUDA, Y., I. SUMITOMO, AND M. SUGITANI. 1977. Properties of cells in the ventral part of the rat’s lateral geniculate nucleus. Proc. 27 IUPS Meeting, p. 247. 14. GAREY, S. J., AND T. P. S. POWELL. 1968. The projection ofthe retinain the cat. J. Anat. 102: 189-222. 15. GIOLLI, R. A., AND M. D. GUTHRIE. 1969. The primary optic projections in the rabbit. An experimental degeneration study. J. Comp. Neural. 136: 99-126. 16. GOODMAN, D. C., AND J. A. HOREL. 1966. Sproutingofoptic tract projections in the brain stem of the rat. J. Comp. Neurol. 127: 71-88. 17. GRAYBIEL, A. M. 1974. Visuo-cerebellar and cerebella-visual connections involving the ventral lateral geniculate nucleus. Exp. Brain Res. 20: 303-306. 18. HALE, P. T., AND A. J. SEFTON. 1978. A comparison ofthe visual and electrical response properties of cells in the dorsal and ventral lateral geniculate nuclei. Brain Res. 153: 591-595. 19. HAYHOW, W. R., A. J. SEFTON, AND C. WEBB. 1962. Primary optic centers of the rat in relation to the terminal distribution of the crossed and uncrossed optic nerve fibers. 1. Comp. Neurol. 118: 295-318. 20. HICKEY, R. L., AND P. D. SPEAR. 1976. Retinogeniculate projections in hooded and albino rats: an autoradiographic study. Exp. Brain Res. 24: 523-529. 21. HOREL, 3. A. 1968. Effects of subcortical lesions on brightness discrimination acquired by rats without visual cortex. J. Comp. Physiol. Psychol. 65: 103-109. 22. 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. 23. LATIES, A. M., AND J. M. SPRAGUE. 1966. The projection of optic fibers to the visual centers in the cat. J. Comp. Neural. 127: 35-70. 24. LEGG, C. R. 1975. Effects of subcortical lesions on the pupillary light reflex in the rat. Neurophychologiu.
13: 373-376.
25. LEGG, C. R., AND A. COWEY. 1977. The role of the ventral lateralgeniculate nucleus and posterior thalamus in intensity discrimination in rats. Bruin Res. 123: 261-273. 26. MAGNIN, M., M. JEANNEROD, AND P. T. S. PUTKONEN. 1974. Vestibular and saccadic influences on dorsal and ventral nuclei of the lateral geniculate body. Exp. Brain Res. 21: 1-18. 27. MATHERS, L. H., AND G. G. MASETTI. 1975. Electrophysiological and morphological properties of neurons in the ventral lateral geniculate nucleus of the rabbit. Exp. Neural.
46: 506-520.
28. NIIMI, K., T. KANASEKI, AND T. TAKIMOTO. 1963. The comparative anatomy of the ventral nucleus of the lateral geniculate body in mammals. J. Comp. Neural. 121: 313-323. 29. NODA, H., AND IWAMA, K. 1967. Unitary analysis of retinogeniculate response time in rats. Vision Res. 7: 207-215. 30. POLYAK, S. 1957. The pregeniculate gray nucleus and the pupillary reflex pathway. Pages 376-385 in H. KLBVER, Ed., The Vertebrate Visual System. University of Chicago Press, Chicago. 31. PUTKONEN, P. T. S., M. MAGNIN, AND M. JEANNEROD. 1973. Directional responses to head rotation in neurons from the ventral nucleus of the lateral geniculate body. Brain Res. 61: 407-411. 32. RIBAK, C. E., AND A. PETERS. 1975. An autoradiographic study of the projections from the lateral geniculate body of the rat. Brain Res. 92: 341-368.
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33. SANNIDES, D. 1975. The retinal projection to the ventral lateral geniculate nucleus of the cat. Brain Res. 85: 313-316. 34. SIMINOFF, B., H. 0. SCHWASSMANN, AND L. KRUGER. 1967. Unit analysis of the pretectal nuclear group in the rat. J. Camp. Neural. 130: 329-342. 35. SPEAR, P. D., D. C. SMITH, AND L. L. WILLIAMS. 1977. Visual responses of single neurons in the cat’s ventral lateral geniculate nucleus. J. Neurophysiol. 40: 390-409. 36. STERZNER, D. J., D. C. GOODMAN, AND P. L. ROSSETTI. 1973. The synaptic organization of the ventral lateral geniculate nucleus, pars lateralis ofthe albino rat. Anat. Rec. 175: 451.
37. STONE, J., AND Y. FUKUDA. 1974. Properties of cat retinal ganglion cells: a comparison of W-cells with X- and Y-cells. J. Neurophysiol. 37: 722-748. 38. SUMITOMO, I., K. IDE, K. IWAMA, AND T. ARIKUNI. 1969. Conduction velocity of optic nerve fibers innervating lateral geniculate body and superior colliculus in the rat. Exp. Neurol. 39. SUMITOMO,
25: 378-392.
I., AND K. IWAMA. 1977. Some properties of intrinsic neurons of the dorsal lateral geniculate nucleus of the rat. Jap. 1. Physiol. 27: 717-730. 40. SUMITOMO, I., M. NAKAMURA, AND K. IWAMA. 1976. Location and function of the so-called intemeurons of rat lateral geniculate body. Exp. Neural. 51: 1 lo- 123. 41. SUMITOMO, I., M. SUGITANI, AND K. IWAMA. 1977. Disinhibition of perigeniculate reticular neurons following chronic ablation of the visual cortex in rats. Z’ohoku J. Exp.
Med.
122: 321-329.
42. SWANSON, L. W., W. COWAN, AND E. G. JONES. 1974. An autoradiographic study of the efferent connection of the ventral lateral geniculate nucleus in the albino rat and the cat. J. Comp.
Neurol.
156: 143-164.
Properties
NEUROLOGY
66, 721-736 (1979)
of Ceils Responding to Visual Stimuli Ventral Lateral Geniculate Nucleus
I. SUMITOMO, M. SUGITANI,~. Depurtment
of Neurophysiology. Medicul
FUKUDA, AND K. IWAMA'
Instiiute of Higher Nervous Activity, School, Kita-ku, Osaka 530, Japan Received
May
in the Rat
Osaka
University
IS, 1979
Single-unit recordings were made of the ventral lateral geniculate nucleus (LGv) in the albino rat anesthetized with urethane. Visual receptive field properties as well as the characteristics of responses elicited by electrical stimuli to the optic tract and to the visual cortex were examined. Compared with the relay cells of the dorsal lateral geniculate nucleus (LGd), LGv cells were characterized by the following properties. (i) They responded to visual cortex stimuli orthodromically as well as to optic tract shocks. (ii) The postexcitatory inhibition they showed after single optic tract or visual cortex stimuli was only short-lasting, at most 100 ms. (iii) Conduction velocities of the optic nerve afferent fibers were mostly in the range of slow fibers, 2 to 10 m/s. (iv) The receptive fields were essentially homogeneous in type; about 90% of the sample of 53 cells were On-tonic. (v) Receptive field sizes were substantially large, from 6.3 to 45.6” (mean, 22.3”). (vi) On-tonic cells revealed a regular maintained discharge whose level changed monotonically as a function of the luminous intensity of the stimulating light. The functional implications of these findings were compared with those of the relay cells in the LGd.
INTRODUCTION The ventral lateral geniculate nucleus (LGv) of various mammals is distinguished from the dorsal lateral geniculate nucleus (LGd) with respect to fiber connections as well as cytoarchitecture. The LGd receives afferent impulses primarily from the retina and sends efferent impulses to the visual cortex (VC), thus functioning as a principal relay to the cerebrum. In contrast to this, the input-output relationship of the LGv is relatively complex. Receiving a major input from the retina (14- 16,19,20,23,27,28, Abbreviations: LGv, LGd-ventral, dorsal lateral geniculate nucleus, PSTHperistimulus time histogram, OT-optic tract, ON-optic nerve, VC-visual cortex. 1 The authors wish to thank Miss K. Takuwa for her secretarial help. 721 0014-4886/79/120721-16$02.00/O Copyright 0 1979 by Academic Press, Inc. All rights of reproduction in any form reserved.
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33,36), it projects to the pretectum (7,17,32,42), superior colliculus (7,32, 42), suprachiasmatic nucleus (7, 17, 32, 42), zona incerta (7, 32, 42), and pontine nuclei (7, 17, 32). From these complex interconnections, the LGv has been suggested to function as a center of visuomotor integration (17,42). Although the LGd has long been a subject of physiological studies in various mammals including the rat, only a few studies have been made of the LGv. As far as analyses of single units are concerned, the available data are those obtained from the rabbit (27) and cat (22,36). Though the rat LGv may be agood target of physiological studies because of its well-developed structure, no single-unit analysis has so far been attempted. Thus the objective of the present paper was, first, to characterize LGv cells of the rat on the basis of responses to electrical stimulation of the optic tract (OT) and the VC and, second, to clarify the visual properties of these cells. We attempted to determine how the physiological properties of LGv cells differ from those of the relay cells (P-cells) of the LGd (12). This will aid us in understanding the significance of the differentiation of the rat lateral geniculate nucleus (LGN) into the dorsal and ventral parts. Some of the results were reported previously in abstract form (13). METHODS General Preparation. Albino rats, weighing 250 to 300 g, were anesthetized with urethane (i.p., 1.2 g/kg) and fixed to a stereotaxic apparatus so as to fit the Fifkova and MarSala coordinates (8). One percent procaine was administered at all pressure points and surgical wounds. The animals were immobilized with gallamine triethiodide (i.p., 40 mg/kg) and respiration was maintained artificially through a tracheal cannula. Additional small amounts of urethane and gallamine triethiodide were applied as required. Electrical Stimulation. To activate LGN cells, single electrical shocks were applied to the OT and VC. For each of the stimulating sites, a bipolar electrode insulated except at the tip was introduced stereotaxically. Adequate placement of these electrodes was ascertained by recording characteristic responses to single-flash stimuli. When the contralateral optic nerve (ON) was to be stimulated, a U-shape bipolar electrode of silver wire was hooked under the nerve just behind the eyeball. Electrical shocks were of rectangular pulses 0.01 to 0.1 ms in duration with intensities less than 50 V. Visual Stimulation. Visual stimuli of diffuse light or light spots were projected onto a tangent screen (100 cm high and 118 cm wide). To define the boundaries of the receptive fields, a small spot of 1 to 2” or a large spot of 5 to lo” was turned on and off or moved across the field. The pupil of the
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right eye was dilated by a topical application of 1% atropine sulfate. The cornea was protected with a contact lens with zero power. The tangent screen was placed vertically at an angle of 32” to the midsagittal plane of the animal and 30 cm distant from the eye. As described in detail previously (12), on the tangent screen so placed, the area centralis was at about 60 from the zero vertical axis and about 20” above the zero horizontal axis. Here, the zero vertical and zero horizontal axes were taken as the intersections with the tangent screen of the animal’s midsagittal plane and of the horizontal plane passing through the eye, respectively. The visual field covered by the screen extended 60” in the nasal, 60” in the temporal, 40” in the upward, and 50” in the downward directions from the estimated projection of the area centralis. The luminous intensities of the light spots varied from 20 to 200 cd/m2. Background illumination was kept at about 3 cd/m2. Recordings. Unitary activities of the LGN cells were recorded extracellularly with glass pipet microelectrodes filled with 2 M NaCl or 3 M KCI. They were amplified conventionally and photographed from the screen of an oscilloscope. Responses to electrical or photic stimuli were processed by means of an on-line electronic computer (DAB-5101, Nihon Koden Kogyo) to make peristimulus time histograms (PSTHs). For responses to electrical stimulations, 50 trials were assembled in one PSTH using 256 bins 2 ms in width. For responses to photic stimuli, unit activities during 10 trials were added usually with an analysis time covering 12.8 s (bin width, 50 ms; number of bins, 256), but in occasional cases a shorter analysis time was used (bin width, 20 ms; number of bins, 128). In some experiments microelectrodes filled with 3 M KC1 saturated with fast green FCF dye were used. Through these electrodes negative currents of 10 to 20 PA were passed for about 10 min to produce dye-marking. The marked sites were verified histologically in the 70-Km-thick tissue sections fixed with 10% Formalin and stained with Calbol-thionine. RESULTS Zdentijication of LGv Cells. While advancing a microelectrode vertically through the LGN, we first encountered activities of P-cells in the LGd. As reported previously, P-cells were characterized by antidromic responses to single VC stimuli and orthdromic responses to OT stimuli, and by a series of late discharges following the initial excitation in both OT- and VC-induced responses (2,3,9,11,29,39,40). Sample records of a P-cell are presented in Fig. 1A. The upper right records in A-I and A-II show initial spike discharges elicited by single OT and VC stimuli, respectively. As is characteristic of antidromic invasion, the spike activated by VC
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FIG. 1. Comparisons of LGv cells and P-cells in response properties to electrical shocks (A and B) and in recording depths (C). A-responses of a P-cell to optic tract (OT) (I) and visual cortex (VC) (II) shocks. B-responses of a LGv cell to OT (I) and VC (II) shocks. Records in the upper right of each peristimulus time histogram (PSTH) are superimposed traces of the initial spike response; the arrow in A-II indicates a notch on the positively going stroke of the spike, characteristic of antidromic activation. The time calibration for each superimposed trace was 2 ms. Note a significant fluctuation of the latency in the superimposed traces in B-II. In the PSTHs electrical stimuli were applied at the time indicated by S on the abscissa. Note the clear late discharges only in the PSTHs of A-I and A-II. C-distribution of recording depths of 74 ventral lateral geniculate cells (shaded columns) and of 76 P-cells (open columns). Ordinate, depth from the cortical surface; abscissa, number of units. For details, see text.
stimulation revealed a notch at its positively going stroke (arrow in the inset record of A-II). The first prominent late discharge was present in the PSTHs in A-I and A-II. The latency of the late discharge, measured at the peak in the PSTH, was usually on the order of 200 to 300 ms. During the period between the initial spike discharge and the late discharge, spontaneous activity was completely silenced. The same was also true during the period after the late discharge. These observations for P-cells are consistent with previous reports (2-4, 9, 39, 40). Cells identifiable as P-cells were recorded from within about 5 mm from the cortical surface. Upon further advancement of the microelectrode, we encountered a group of cells with the following properties in common: (i) Single or occasionally double spike responses were elicited at short latencies by OT stimuli, (ii) no antidromic responses were elicited by single VC stimuli, and (iii) no late discharges appeared after OT- or VC-induced early responses. These response properties led us to assume that the cells were in the LGv. Sample responses of an LGv cell are presented in Fig. 1B. This cell responded to OT stimuli with double spikes, as seen in the upper right records of B-I. The initial spike activated from the VC revealed a significant fluctuation in latency as a characteristic of transsynaptic activation (B-II). In the PSTHs made after OT and VC stimulation, only a
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short-lasting suppression of spontaneous discharges appeared without producing any clear late discharges (B-I and B-II). The suppression after the initial response lasted about 30 to 100 ms. Because it has been observed histologically that LGv cells do not project to the VC (42) but receive corticofugal afferents (16,27,36), transsynaptic activation from the VC can be assumed as a criterion for the identification of LGv cells. In Fig. 1C are plotted the depths of recording sites for cells identified as LGv cells (shaded columns) according to the above characteristics, in comparison with the distribution of recording depths of P-cells (open columns). It is clear that the LGv cells identified on the basis of physiologic characteristics are certainly distributed below the distribution of P-cells, with a little overlap around the depth of 5.0 to 5.2 mm from the cortical surface. More direct identification of recording sites for LGv cells was made with microelectrodes filled with fast green dye. The data from a typical experiment are presented in Fig. 2. In this experiment the LGv was explored in one frontal plane along seven vertical tracks spaced 100 pm apart mediolaterally. Exploration was made with the same microelectrode, and for each LGv cell encountered, its coordinates were noted. Finally, for an LGv cell recorded at the deepest point of the most lateral track, the dye was deposited and the spot was delineated as indicated with an arrow in the photomicrograph of Fig. 2A. This dye spot was taken as a reference for plotting the recording sites of all the LGv cells encountered in this experiment onto outlines of the LGN (Fig. 2B). It is clear that the electrophysiologically identified LGv cells were all within the anatomic confines of the LGv. Along the two most medial tracks a number of cells were recorded, but none of them was excited by OT stimuli or was visually responsive. This observation is consistent with the histological finding that retinal afferents terminate exclusively in the lateral division of the LGv (16, 19, 20, 42). Postexcitatory Inhibition. As referred to in the preceding section, LGv cells revealed no late discharges after a single OT or VC stimulus. This is different from the property of P-cells in that with either type of stimulation, almost without exception the initial excitation is followed by a series of late discharges. The late discharge in the P-cells has been interpreted as a postinhibitory rebound excitation; the inhibition preceding the late discharge appears as a lack of spontaneous discharges and a decreased responsiveness to the testing OT stimuli (3, 9, 39, 40). In the following experiment we examined how quickly LGv cells recovered responsiveness after being excited by OT stimuli. Because LGv cells ceased spontaneous discharges only a short time after the initial excitation by OT stimuli, as revealed in PSTHs, we expected that the post-excitatory recovery determined with double OT stimuli would be accomplished relatively quickly.
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A
0.5 mm FIG. 2. Histological identification of recording sites. A-photomicrograph of a frontal section of the lateral geniculate nucleus. Arrow indicates the site of the green spot deposited after recording from a typical ventral lateral geniculate (LGv) cell. B-a diagrammatic presentation of recording sites of LGv cells responding to optic tract (OT) stimuli: Each of the filled circles represents the recording site of one LGv cell. Seven electrode tracks, separated by 100 pm, are indicated with vertical arrows in the diagram. The recording site corresponding to the dye mark in A is indicated by a horizontal arrow. Note that in the two most medial tracks no cells were activated by OT stimuli.
To determine the recovery curve, double stimuli were applied to the OT. The intensity was set for each cell at twice the threshold for triggering the initial spike and the stimulus interval was varied from 2 to 500 ms. The degree of postexcitatory inhibition after the first stimulus was judged by the firing probabilities to the second stimulus. Samples of the recovery curve in the LGv cells are presented in Figs. 3A and B. Of 33 cells tested, 28 (85%) showed a smooth recovery such as shown in Fig. 3A. Unfilled and filled circles represent the most rapidly and slowly recovering cells in this group, respectively. Even in the case of the most slowly recovering cells (filled circles), the responsiveness started to reappear 20 ms after the first stimulus and completely recovered by 40 ms. All cells which revealed
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smooth recovery curves showed a simple and short-lasting silent period in the spontaneous discharges, as exemplified in the PSTHs of Fig. 3D. The minor group, consisting of five cells (15%), showed an oscillatory recovery, as exemplified by the two cells plotted with filled and unfilled circles in Fig. 3B. In these cases the recovery curve consisted of two periods of inhibition, one occurring within 10 ms after the primary excitation and the other appearing from 30 to 100 ms after. Usually the late inhibition was weaker than the earlier one. Cells showing this type of recovery were characterized by a complex PSTH pattern associated with single OT stimuli; as seen in Fig. 3E, the silent periods were interrupted by a short-lasting excitation. Figures 3C and F show examples of the recovery curve and the PSTH of P-cells, respectively. In Fig. 3C, five cells are plotted together, all showing a long-lasting complete inhibition to as much as 100 or 200 ms and a weak inhibition recurring at about 300 ms. It took more than 500 ms to attain complete recovery. Correspondingly, a complete suppression in the PSTH was apparent before and after the late discharge (Fig. 3F). In summary, this series of experiments made it clear that postexcitatory inhibition in LGv cells was far weaker than in P-cells of the LGd. Affeerent Conduction Velocity. Response latencies to single OT stimuli were measured in 125 LGv cells, and their distribution is shown in Fig. 4A. It covers a range from 1.15 to 5.17 ms (mean, 3.06 ms). Of these cells, 98 (78.4%) were activated transsynaptically from the VC as well. The latency D
E
FIG. 3. Comparisons of the postexcitatory inhibition between ventral lateral geniculate (LGv) cells (A, B, D, and E) and P-cells (C and F). A-C-postexcitatory recovery curves made by double stimuli applied to the optic tract (OT). Ordinates, response probabilities to the test OT shock; abscissae, conditioning-testing intervals. Two representative LGv cells are plotted for A and B, identified with unfilled and filled circles, and five P-cells are plotted in C. D and E-PSTHs made after single OT stimuli for the LGv cell depicted in A and B with filled circles, respectively. For details. see text.
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FIG. 4. Latency histograms of ventral lateral geniculate (LGv) cells to stimuli of the optic tract (A) and visual cortex (B), and distributions of afferent conduction velocities for LGv cells (C)and P-cells (D). In A and B, 125 and 98 LGv cells were plotted, respectively. In C and D, 74 LGv cells and 79 P-cells were plotted, respectively. Histogram D is reconstructed from the original published previously (38).
histogram for the VC-induced responses is depicted in Fig. 4B. The latency was distributed from 1.20 to 8.45 ms (mean, 3.67 msec). Twenty-seven other cells (21.6%) could not be activated from the VC, probably because placement of the stimulating electrodes was not adequate. In 74 LGv cells the response latencies to stimulation of the ON and OT were both measured, allowing us to calculate conduction velocities of ON fibers driving these cells. Taking the distance from the ON to the OT electrode as 9 mm (10,38), the conduction velocities were calculated as the distance divided by the difference in latencies between the responses to ON and OT stimulation. The range of the conduction velocity turned out to be from 2.0 to 13.0 m/s (mean, 6.0 m/s), as shown in Fig. 4C. The velocity histogram previously reported by Sumitomo et al. (38) for P-cells of the LGd is shown in Fig. 4D. It is clear that except for the two cells at bins of 11 and 13 m/s, most LGv cells were distributed in the range within 10 m/s. By contrast, of 79 P-cells plotted in Fig. 4D, 36 cells (45%) were innervated by ON fibers having velocities faster than 10 m/s. Therefore, we could conclude that the LGv cells are innervated by relatively slow-conducting ON fibers, whereas the LGd cells are innervated by ON fibers having a wide range of velocities. The synaptic delay was measured for the LGv cells by the same method applied previously for the P-cells (38). The mean synaptic delay in 74 LGv cells was 0.64 ms. This value is comparable to the 0.73 ms which was obtained for P-cells (38). Thus LGv cells can be assumed to be innervated monosynaptically by ON fibers as are the P-cells in the LGd.
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The maintained activity varied from cell to cell in a sample of LGv cells: Some were virtually silent, whereas others discharged at frequencies as high as 30 to 40 spikes per second. However, as a characteristic of most LGv cells, their maintained discharge altered significantly as the background illumination changed. In general, the discharge increased as the luminance was increased, and as long as the luminance was kept constant, the maintained discharge was also steady. Examples of this behavior will be presented in the following section. Visual Receptive Field Properties. A total of 56 LGv cells was subjected to the analysis of visual responses. Except for three cells responding to the ipsilateral eye, all others responded exclusively to the contralateral eye. There were no binocularly driven cells. For 53 LGv cells, receptive field properties were analyzed with the contralateral eye. On the basis of receptive field center properties, LGv cells were classified into four types: On-tonic, On-inhibited, On-Off-inhibited, and movement-sensitive. Forty-seven of 53 LGv cells (88.7%) were of the On-tonic type and the remainder were classified as one of the other three types: four On-inhibited, one On-Off-inhibited, and one movement-sensitive cells. Sample responses of On-tonic, On-inhibited, and On-Off-inhibited types are presented in Fig. 5. The PSTHs were made by averaging responses to flashing of a light spot of a size equal to the receptive field center size. As with the sample presented in Fig. 5A, On-tonic cells showed tonic discharges during activation of the receptive field center by a light spot. In contrast, the On-inhibited type was characterized by a high level of maintained discharges in the absence of light stimulation and by their suppression upon the onset of a light spot (Fig. SB). Because of the apparent lack of Off response, this type of cell was called the On-inhibited type rather than Off-center. As exemplified in Fig. 5C, the On-Offinhibited type had a moderate level of maintained discharges which was phasically suppressed at either On or Off of a centered light spot. MaintainedDischarge.
A
B
ON-tonic
C
ON-inhibited
(I
ON-OFF-inhibited
Y;l I
--I ‘5s
5s
IS
FIG. 5. Three receptive field types of ventral lateral geniculate cells. For each peristimulus time histogram (PSTH), 10 consecutive responses to a stationary spot flashed on and off were compiled. Total analysis time was 12.8 s in A and B and 2.56 s in C. The trace below the PSTHs is upward as the luminance of the activated region increases and downward as it decreases.
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We tried to detect any antagonistic or suppressive field surrounding the center by flashing a small light spot outside the center or by flashing a large spot covering both the center and surround regions. Except for four On-tonic cells (7.5%) having incomplete Off-surrounds, notable surround could not be detected in the other 49 LGv cells tested. Such rare occurrence of the receptive field surround was also noted for the P-cells (12). All 10 cells of the On-tonic type tested decreased their maintained discharges in proportion to a decrease in the intensity of light shining on the field center. A typical case is shown in Fig. 6. In the left column, PSTHs at three different intensities of light are presented, with corresponding oscilloscope traces in the right columns (A-II, B-II, and C-II). The spot intensity was decreased from 200 cd/m2 (A) to 67 cd/m* (B) and further to 20 cd/m2 (C). The mean discharge frequencies were 14.6 (A), 8.3 (B), and 4.3 (C) spikes per second, respectively. Receptive Field Size. In 43 LGv cells, receptive field boundaries could be determined by flashing spots of various sizes. The receptive fields were always circular or square with no appreciable surround components. The center size was 6.3 to 45.6” (mean, 22.3’) in diameter, as presented in Fig. 7B. In Fig. 7A are reproduced the data published previously for the P-cells (12). Although the receptive field sizes of P-cells were distributed widely from 2.1 to 41”, more than 90% of the sample were distributed within 15”. By contrast, about 80% of the LGv cells had receptive fields larger than 15”. There was no difference in the field size among the four receptive field types of the LGv cells. Thus, the LGv cells, as a whole, had receptive fields significantly larger than those of P-cells.
FIG. 6. Sample responses of an On-tonic ventral lateral geniculate cell to a centered light stimulus of graded intensities. Luminous intensity of a light spot was decreased from 200 cd/m2 (A) to 20 cd/m* (C). A-I, B-I, and C-I, the PSTHs obtained at the three different intensities of illumination. The trace below the PSTHs indicates the output of the photodiode placed in the center of the receptive fields. A-II, B-II, and C-II, oscilloscope traces of the discharges maintained during the three stimulus conditions. Note the regular discharges at each light intensity.
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B WV)
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RF Size FIG. 7. A comparison of the receptive field (RF) center sizes ofthe ventral lateral geniculate (LGv) cells and P-cells. A-frequency distribution histogram for P-cells (N = 214). B-frequency distribution histogram for LGv cells (N = 53). Mean sizes (*SD) were 7.8 4 5.4” in A and 22.3 4 10.1” in B, respectively. Histogram A is redrawn from the original published previously (12).
Distribution of Receptive Field Positions. To see if there was a tendency for the recorded LGv cells to represent preferentially a particular part of the visual field, all the receptive fields were replotted on the same sheet of paper by taking the area centralis as a reference. We found that the upper temporal field was less frequently represented than the other three quadrants: three cells in the upper temporal field, 14 cells in the lower temporal field, 14 cells in the lower nasal field, and 16 cells in the upper nasal field. This contrasts sharply with a relatively even representation of the visual fields by P-cells of the LGd (12). However, our sample of LGv cells was small and we cannot think of any physiologically significant implications of this finding. DISCUSSION
From the analysis of the responsiveness of visual neurons to electrical stimulation of the optic pathway, several important characteristics
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emerged to distinguish LGv cells from P-cells of the LGd. First, many LGv cells were activated transsynaptically from the VC. Second, postexcitatory inhibition, assessed by lowered responsiveness to testing stimuli or by silencing of spontaneous discharges after single OT shocks, was only short-lasting. Third, LGv cells were innervated by relatively slowconducting ON fibers. The LGv cells were distinguished from P-cells in visual properties as well. First, under a given condition of background illumination many LGv cells showed regular maintained discharges and the activity changed monotonically as the level of illumination was shifted. Second, LGv cells were fairly homogeneous in terms of the receptive field type, that is, a great majority (88.7%) was of the On-tonic type. Third, the size of the receptive field center was significantly larger than that of the P-cells. These visual properties would indicate that cells of the rat LGv are less differentiated from each other than P-cells in the LGd, hence their function would be primitive in nature. Inhibitory Mechanism within the Ventral Lateral Geniculate Nucleus. A prominent feature in the LGv cells is that the postexcitatory inhibition is only poorly developed. This contrasts sharply with P-cells of the LGd. Since the first report by Burke and Sefton (2-4), it has been repeatedly confirmed that P-cells of the LGd undergo a long-lasting postexcitatory inhibition (9,39,40). Burke and Sefton originally assumed that the activity of interneurons within the LGd was responsible for the postexcitatory inhibition. A more recent report by Sumitomo et al. (40), however, presented evidence that the inhibition is caused by perigeniculate reticular neurons (41) located in a restricted region of the thalamic reticular nucleus immediately rostra1 to the LGd. Furthermore, Sumitomo and Iwama (39) succeeded in recording from intrinsic neurons within the rat LGd and suggested that the intrageniculate inhibition ascribable to the action of these intrinsic neurons might be only subtle. In view of these recent advances in the understanding of the inhibitory mechanism within the rat LGd, an apparent lack of long-lasting inhibition in the LGv cells led us to conclude that these cells were free from the inhibition caused by perigeniculate reticular neurons. Retinal Input. In a preceding paper on P-cells of the rat LGd, we pointed out that most P-cells can be likened to either Y- or W-type relay cells of the cat LGd (12). The Y-type relay cells are characterized by the inputs from fast-conducting retinal ganglion cells, phasic responses to centered spots flashed on or off, and a preference for fast-moving light stimuli. By contrast, W-type relay cells have the following properties in common: innervation by slowly conducting retinal afferent fibers and a preference for slowly moving stimuli. In the W-homologous P-cells of the rat LGd, several subgroups were identified: On-tonic, On-Off-phasic, On-inhibited, motion-sensitive, and so on. According to this classification, the LGv cells
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are homologous to the W-type cells for the following reasons. First, axonal conduction velocities of retinal afferent fibers are restricted to the slow range (see Fig. 4C). Second, all the four receptive field types (On-tonic, On-inhibited, On-Off-inhibited, and motion-sensitive) were found in the W-homologous P-cells of the rat LGd as well (12). Further, though not studied for all cells, most LGv cells preferred very slow spot movements. It is most impressive that a monotonic change in maintained activity observed in most On-tonic LGv cells was exactly the same as observed in On-tonic W-type ganglion cells of the cat retina. (37). Another important feature for understanding the mode of retinal inputs to the LGv was that the receptive field size was about three times larger in diameter than that of retinal ganglion cells. The average size of the field in the present samples of LGv cells was 22.3”, whereas Brown (1) reported 7.5” for the rat’s retinal ganglion cells. In another study we reported the average size as 7.8” for P-cells in the rat LGd (12). Thus, it appears most conceivable that about three retinal ganglion cell axons converge upon one LGv cell, whereas a one-to-one connection exists between retinal ganglion cell axons and P-cells in the LGd. Comparison with Other Animals. Visual properties of LGv cells were reported for the monkey (6), rabbit (27), and cat (22, 35). In the monkey, DeValois (6) showed that cells of the perigeniculate nucleus, homologue of the LGv of lower mammals, gave prolonged On-responses to presentation of a light stimulus in a manner similar to the rat’s On-tonic LGv cells. In the rabbit LGv, Mathers and Massetti (27) categorized three types of cells: concentric, uniform, and others. Unfortunately, however, they made no special note as to whether or not these cells were On-tonic. A more recent and extensive study was made by Spear et al. (35) for the cat LGv. They identified On-tonic cells which behaved in the same way as reported in the present paper for the rat LGv. However, the sampling frequency of these cells was about 10% of all visually responsive cells, which is significantly smaller than the frequency (88.7%) of the On-tonic cells sampled in the present study. They noted, in addition, that a vast majority of cells with uniform receptive fields (35.3% of visually responsive cells) and with concentric ones (25.2%) showed On-responses. Thus, the LGv in the cat and the rat share a property in common, that is, the predominance of On-center receptive fields. Functional Implications. It has been suggested that the LGv is involved in visuomotor functions (17, 42). Electrophysiological studies for the cat and monkey showed that the LGv cells change activities in association with head and eye movements (5, 26, 31). On the other hand, in behavioral studies of the rat, the LGv was shown to function in brightness discrimination (2 1,25). The present finding that the rat LGv consists mostly of cells carrying luminous information appears to corroborate these
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behavioral studies. Another possible function of the LGv is in relation to the mediation of the pupillary light reflex. Polyak (30) was the first to ascribe mediation of the pupillary light reflex to the perigeniculate nucleus, homologue in the primate of the LGv of lower mammals. More recently Legg (24) provided evidence in the rat that lesions of the LGv resulted in mydriasis and suggested further that the LGv could be the primary relay to the pretectum, which has long been assumed as the center for the pupillary light reflex. The present finding that the rat LGv consists mainly of On-tonic cells with large receptive fields supports Legg’s suggestion (24). Furthermore, in single-unit studies of the rat’s pretectum, Siminoff et al. (34) reported that in the ventral part there were many On-tonic cells with large receptive fields and that these cells changed their maintained discharges depending on the intensity of ambient illumination. From these two findings, it is suggested that the LGv and the ventral pretectum constitute a system for mediating visual information necessary for the pupillary light reflex. During the preparation of this manuscript, a similar work on the rat LGv was published by Hale et al. (18). They reached the same conclusions as ours, in that the LGv cells are essentially free from the postexcitatory inhibition after single OT stimuli and that a great majority of these cells revealed On-tonic properties in their visual responses. REFERENCES 1. BROWN, J. E. 1965. Dendritic fields of retinal ganglion cells of the rat. J. Neurophysiol. 28: 1091-1100. 2. BURKE, W., AND A. J. SEFTON. 1966. Discharge patterns of principal cells and inhibitory intemeurones in lateral geniculate nucleus of rat. J. Physiol. (London) 187: 201-212. 3. BURKE, W., AND A. J. SEFTON. 1966. Recovery of responsiveness of cells of lateral geniculate nucleus of rat. J. Physiol. (London) 18’7: 213-229. 4. BURKE, W., AND A. J. SEFTON. 1966. Inhibitory mechanism in lateral geniculate nucleus of rat. J. Physiol. (London) 187: 231-246. 5. BUTTNER, U., AND A. F. FUCHS. 1973. Influences of saccadic eye movements on unit activity in simian lateral geniculate and pregeniculate. J. Neurophysiol. 36: 127- 141. 6. DEVALOIS, R. L. 1960. Color vision mechanism in the monkey. J. Gen. Physiol. 43: 115-128. 7. EDWARDS, S. B., A. C. ROSENQUIST, AND L. S. PALMER. 1974. An autoradiographic study of ventral lateral geniculate projections in the cat. Bruin Res. 72: 282-287. 8. FIFKOVA, E., AND J. MARSALA. 1967. Stereotaxic atlases for the cat, rabbit and rat. Pages 426-467 in J. BURES, M. PETR.~~~, AND J. ZACHER, Eds., Elecrrophysiological Methods in Biological Research. Academic Press, New York. 9. FUKUDA, Y. 1973. Differentiation of principal cells of the rat lateral geniculate body into two groups; fast and slow cells. Exp. Brain Res. 17: 242-260. 10. FUKUDA, Y. 1977. A three-group classification of rat retinal ganglion cells: histological and physiological studies. Brain Res. 119: 327-344. 11. FUKUDA, Y., AND M. SUGITANI. 1974. Cortical projections oftwo types ofprincipal cells of the rat lateral geniculate body. Bruin Res. 67: 157-161.
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