Neurons with visual properties in the posterior group of the thalamic nuclei

EXPERIMENTAL NEUROLOGY23,353-365

Neurons

with

Visual of

(1969)

Properties the

Thalamic

in the

Posterior

Group

Nuclei

HISAOSUZUKI

Departmentof

Physiology,

Hirosaki

University

Faculty

of Medicine,

Hirosaki,

of Medicine,

Sendai,

Japan

AND HIROSHIKATO~ Institute

of Brain

Diseases,

Tohoku

Ulziversity

School

Received

November

18,1968

Japan

Unit activities of neurons in the posterior group of the thalamic nuclei (PO) were recorded in response to stimulation of the ipsilateral optic tract. These neurons were found to be situated in the upper half of PO. The response latencies of the neurons to stimulation of the optic tract were distributed a wide range, 1-15 msec, and the scatter of latencies may indicate the presence of a variety of synaptic connections of neurons with the visual pathway. Synaptic transmission was highly dependent on reticular activity. Most of the neurons in PO had large receptive fields which usually showed eccentricities in the visual field. A small light spot illuminated in any part of the receptive field evoked an “on-off” type of response. Introduction

Recently, several workers postulated that the central visual pathway has connections to certain thalamic nuclei other than the lateral geniculate nucleus (LGN). These thalamic nuclei are said to be the pulvinar, the lateral posterior nucleus (LP), and related nuclei. This region of the thalamus, the “pulvinar-posterior system” (the posterior group of the thalamic nuclei; PO), was first denoted as a functional unity by Rose and Woolsey ( 14). Poggio and Mountcastle (13) made a systematic investigation on the neuronal activity of this region, but their attention was mainly directed to the neurons responding to somatic sensory stimulation and no detailed description was given of neurons responding to visual stimuli. There are conflicting anatomical and physiological reports regarding the neural connections of the visual pathways with PO. Altman (1; also cited in 11) described a small number of the optic nerve fibers terminating in a nuclear mass just medial to the LGN, while Bishop and Clare (2) suggested that some optic nerve fibers which go to the thalamic nuclei are exclusively intercalated in layer B of LGN. On the other hand, Calma (4) 1 The authors are indebted to Dr. S. Ochs for his suggestions regarding 353

English.

354

SUZUKI

AND

KATO

postulated that visual inputs activate the thalamic nuclei only after reaching the visual cortex via the geniculostriate pathway, coming back to the thalamus through efferent fibers from cortical neurons. The purpose of the present report is to describe the behavior of PO units which show visual properties. In addition, some information concerning the connections of the visual system with PO will be presented. Methods Thirty-three adult cats were used. They were anesthetized with ether, the trachea was cannulated and anesthesia was maintained during the following surgical procedures. The cat was transferred to a stereotaxic apparatus designed so as not to obstruct the visual field. Usually a craniotomy was made with a dental burr to expose the dura mater overlying the marginal and suprasylvian gyri of both hemispheres. Thus, the electrodes could be arranged as desired. The electrodes for stimulating the optic tract consisted of two 200-p insulated stainless-steel wires, cemented together with a tip separation of 1 mm. They were inserted vertically from the dorsal surface of the cortex to the stereotaxic position F 12, L 5, H -5. After further up-and-down adjustment, the electrodes were fixed to the position in which the visually evoked potential was maximally recorded. Usually such electrodes were inserted into both optic tracts. Stimulation of the mesencephalic reticular formation (F 2, L 3, H -2) was done with similar electrodes, usually inserted into the left reticular formation. For stimulation of the white matter underlying the visual cortex, bipolar electrodes were inserted perpendicularly into the posterior marginal gyri of both hemispheres at a depth of 4 mm. The electrodes consisted of two 200-p stainless-steel insulated wires, 5 mm apart and parallel to the length of the marginal gyri. After all stimulating electrodes were set in position, they were anchored in place to the skull with acrylic resin. Thereafter, the stimulating electrode holder was removed from the stereotaxic apparatus. No hinderance was present over the dorsal surface of the brain so that a manipulator could be used to drive recording microelectrodes placed in any desired position. A dam of acrylic resin was built around the opening in the skull. The dura was cut open, and the opening was covered with a thick disc of 5% agar-Ringer. Melted agar-Ringer was then dripped down to seal this brain surface. The closed calvarium technique prevented the pulsible and respiratory movements of the brain and made it easier to record unit activity for long periods of time ( 18). All wound margin and pressure points were infiltrated with lo/O procaine solution, and ether anesthesia was discontinued. Flaxedil was then administered through an inlying tubing placed in the saphenous vein and artificial

POSTERIOR

THALAMUS

3.55

respiration was started. Supplemental injections of Flaxedil were given at a rate of about 40 mg per hour. During the experimental period, the corneae were instilled with Medrin-P (Santein Pharmacy Co.), and contact lensesapplied to correct for accommodation and for protection. To determine the receptive fields of neurons, a white screen 50 cm high and 50 cm long was placed 40 cm before the cat’s eyes. At this distance, 0.7 cm of the screen subtends about 1 degree at the eye. The screen was evenly illuminated by a tungsten-filament lamp when background illumination was necessary. The brightness of the screen was 0.1-0.3 cd/m2. Various patterns of visual stimuli were projected on to the screen with a luminance l-2 log unit brighter than that of the background. Microelectrodes for unit recording were electrolytically sharpened insect pins insulated with Insul-X and with bare tip diameter of about 1 p. The electrodes were lowered through the agar-Ringer disc and the tip aimed stereotaxically (9) at the position F 6, L 6, H 6 and as well to close by positions. Unit activity of the neurons was fed into a negative-capacitance high-impedance amplifier, then conventionally amplified and displayed on a dual-beam oscilloscope. The reference electrode was a silver plate wrapped in Ringer-soaked cotton placed at the wound margin. The recording sites were marked by electrolytic deposition of iron (5). This was done by applying 5-10 pamps of positive current through the electrode tip for 20-30 sec. After each experiment was finished, the animal was killed with an overdose of Nembutal. The brain was perfused through the common carotids with 300 ml of warm saline, followed by 300 ml of 10% formalin solution containing 2% ferrocyanide. The brain was then removed and hardened in a ferrocyanide-containing solution of formalin, frozen and sectioned coronally at 30 p. The marking location was readily identified as a blue spot 100 p in diameter. The sections having a marked spot were alternatively stained with cresyl violet for cell bodies and with the Spielmeyer method for observation of fibers. The positions found were used to correct the stereotaxic positions originally used. Results Properties in PO. When a microelectrode was gradually lowered through the cortex to a region corresponding to PO, neurons were encountered along the track of the electrode. Thirty of these neurons were found to respond to stimulation of the ipsilateral optic tract (OT) and they were situated in PO as shown by histological examination made afterwards. They were by this means identified as visual cells of PO. The responseof the neurons excited by a single stimulus applied to the ipsilateral OT was an action spike of about 1 msec in duration with a diphasic positive-negative configuration Identification

of Neurons of Visud

356

SUZUKI

AND

KATO

(Fig. 1A). The spike usually arose from a rising phase of a slow positive wave lasting several msec, the spike generated with a response latency of a several msec. As shown in Fig. lA, the unit did not respond with an action spike to all of the stimuli, some only initiated the slow waves. Furthermore, the action potential generated showed a dispersion in its latencies. Visual cells of PO also responded to single shock stimulation of the underlying white matter of the visual cortex. As illustrated in Fig. lB, cortical stimulation induced after a latency of about 3 msec, a slow positive wave of several msec duration accompanied with an action potential. In this particular example, latency play of the action spike was smaller than that in response to optic tract stimulation. However, this was not always the case: In some visual cells of PO, action potential responses to cortical stimulation showed a great dispersion of latencies (Fig. 1D). Generally, the latency of the response to cortical stimulation was shorter than that of the response to OT stimulation.

I..................

,......,................

rnsec

FIG. 1. Responses of visual cells of PO to single OT stimulation (A, C) and to stimulation of optic radiation (B, D). A, B and C, D represent activities from same neurons.

The action potential of most visual cells in PO as obtained in the present experiments generally failed to show an inflexion on its positive rising phase. The inflexion is believed to be generated when excitation spreads from the initial segment of the axon to the soma-dendritic portion of the cell. The presence of an inflexion may, therefore, provides evidence that the unit activity originated from the cell body. Since the inflexion was absent, we should consider the possibility that the action potential may originate from the axon, not from the cell body. However, the following observation may exclude this possibility. The neuron illustrated in Fig. lC, at first showed a low rate of spontaneous discharge, at a frequency below

POSTERIOR

357

THALAMUS

l/set. When the microelectrode was then very carefully advanced, the rate of spontaneous discharge became higher. Simultaneously, the responsiveness of the neuron increased so that most stimuli applied to the optic tract and to the cortex gave rise to action potentials (Fig. lC, D). Moreover, a notch then appeared on the rising phase of action potentials which were generated with unusually long delays (Fig. 1D). These two experimental tindings strongly indicate that the action potentials under consideration originate from the cell body. Figure 2A shows the distribution of latencies in the responses of visual cells of PO to OT stimulation. As shown in this figure, the latencies were widely distributed, ranging from 1.0 msec to 15.2 msec with a peak at 4.0-4.5 msec. In Fig. 2B, the latency distribution of responses of histologically identified LGN neurons to OT stimulation is shown. This distribution is illustrated for comparison with the latency distribution of visual cells of PO. The latencies of identified LGN neurons were distributed within a range of 0.5-3.4 msec, and we have as yet failed to obtain with LGN neurons a latency longer than 4 msec. Distribution of Visual Cells within PO. Figure 3 illustrates electrode mark sites where visual cells of PO were recorded. As indicated by the arrows, the stain spots were irregular-shaped and about 100 p long. In these particular examples, the spots were situated at the lateral border of the pulvinar (left figure) and in the ventral part of the pulvinar (right figure). Visual cells were usually located in the dorsal parts of PO though they were widely scattered in the rostrocaudal plane. This dorsal locality of

o\ 0

4

8

12

msec

16

10

0

msec

4

FIG. 2. Latency distribution of responses of visual cells of PO (A) and of lateral geniculate cells (B) on single OT stimulation. Notice great scattering in response latency in visual cells of PO.

358

SUZUKI

AND

KATO

FIG. 3. Two examples of electrode mark sites where visual cells were recorded. Sites are indicated by arrows.

visual cells of PO is to be contrasted to the somatic sensory cells which are usually found in more ventral portions of the nucleus group (13). In Fig. 4, the positions of 30 identified visual cells of PO were plotted on the stereotaxic maps (9). The positions are scattered considerably, from the F 5 plane to F 8. Visual cells were found to present in the pulvinar, the posterior nucleus and in the lateralis posterior nucleus, but most commonly in the pulvinar. Since penetrations of the electrode were made mainly in the vicinity of the stereotaxic plane F 6, a dense localization of visual cells is seemingly presented in this plane. Despite this biased A-P localization, it can be noted that the visual cells of PO are generally situated in the upper half of the nucleus group. We further examined the possibility that

Frc. 4. Positions of visual cells of PO plotted in stereotaxic maps. Notice cells are situated in upper-half of PO.

POSTERIOR

359

THALAMUS

the latency of visual cells in response to OT stimulus varied with their location in PO, and found that the short latency neurons seem to be distributed near the LGN. Reticular Influence to Visual Cell of PO. Most visual cells of P,O did not respond with action potentials to all stimuli but only to some (Fig. 1A). Furthermore, some cells entirely failed to generate action potentials even when the strength of OT stimulation was five times greater than that required for generating action potentials from LGN neurons. The response of these neurons to OT stimulation was a pure slow wave (Fig. 5A, C). However, the cells became capable of responding with an action

A

.

.

-de-

.

-

.

.

FIG. 5. Reticular stimulation volley. A and C give control reticular stimulation. Reticular stimuli.

.

.

.

.

--.1......-.--s..-.-

msec

facilitates responses of visual cells of PO to OT responses. B and D give responses conditioned by stimuli were applied 100 msec earlier than test OT

spike to OT stimulation, when a co&ditioning stimulus was applied to the midbrain reticular formation 100 msec earlier than the test OT stimulus (Fig. 5B, D). In some visual cells of the PO, this increased responsivenesswas not accompanied with an augmentation of the positive slow wave (Fig. 5A, B) . Since the positive slow wave is considered to be the synaptic potential, this would imply an excitability change withaut alteration of the synaptic potential. This phenomena, however, may be accounted for by supposing that the synaptic sites on which endings from the visual path are located are more distally placed on the dendrites and that unit activity of the cell is recorded near to these synapses.In this case, electrotonic spread of the synaptic potential would be necessary in order for it to reach the trigger zone at the initial segment of the axon for spike generation. If some facilitatoty event occurs along the electrontonic path when stimulating the reticular formation, an action potential will be generated without augmenta-

360

SUZUKI

AND

KATO

tion of the synaptic potential. In other words, both reticular and retinal paths may converge on and make synaptic contact with one and the same cell under consideration. In other cells of PO, an increase in their responsiveness was definitively accompanied with an augmentation of the synaptic potential (Fig. 5C, D) . The augmentation of the synaptic potential may be produced by an increase in secretion of the transmitter substance to the postsynaptic membrane. This may occur as the result of an increased efficacy of transmission at any synapses along the paths. Therefore, it may not be necessary that there be direct synaptic contacts of reticular paths to the cells in question. However, the following observation may indicate that some visual cells of PO have direct synaptic contact with the reticular pathway. In Fig. 6A, the cell was excited only once to give a spike when five successive stimuli of equal strength were applied to the optic tract. Some

4D .

.TTTm_..

. . mSec . . . . . . .

FIG. 6. Reticular stimulation facilitates responses of visual cells of PO to OT stimulation (A, B) and to optic radiation stimulation (C, D). A and C are control responses. B and D give responses conditioned by reticular stimulation.

stimuli elicited only small slow waves. When conditioning stimuli were applied to the reticular formation 100 msec earlier, test OT stimuli evoked positive slow waves of large and constant amplitude accompanied by an increased firing of action potentials of the cell in response to OT stimulation (Fig. 6B). This same cell was also able to respond with all-or-none .spikes of small amplitude when stimulation was applied to the optic radiation (Fig. 6C). Latencies of the responseswere 2.7 msec with negligibly small play. When conditioning stimuli were applied to the reticular formation, some stimulation of the optic radiation fibers evoked large action potentials (Fig. 6D). The large spike has a notch on its rising phase and

POSTERIOR

361

THALAMUS

this notch corresponded in amplitude with the smaller-sized spike. Relatively short and invariant latencies of the spikes excited by optic radiation stimulation may indicate that the spikes occur as a result of antidromic invasion of the cell. The small and large action spikes may represent antidromic activation of the initial segment and of the soma-dendritic regions of the cell, respectively. Therefore, stimulation of the reticular formation enhances the responsiveness of the cell, facilitating an invasion of the action potential from the initial segment to the soma-dendritic region. Responses of Visual Cell of PO to Light Stimuli. Most visual cells in the PO responded when light stimulation was applied to an appropriate position in the visual field of either eye. Figure 7 illustrates responses

F -iAL

-

-

-

__,.__,._.

FIG. 7. Responses of visual cells of PO to light illumination (lower record in each column represents response of cell to OT stimulation.

10msec ---- -.- ---

row).

Upper

of three visual cells of PO to optic tract stimulation (upper row) and to illumination with a 4-degree light spot presented to the contralateral eye. As can be seen in the lower row in this figure, the cells responded sluggishly with one or several action potentials at the onset and at the cessation of illumination, thus the responseswere of the on-off type. It was also found that most cells were influenced binocularly, though no systematic observations were made on ocular dominancy. The receptive fields of the cells were mapped with a light spot of l- to

362

SUZUKI

AND

KATO

2-degree diameter. Such a small light spot could serve to define the wholefield boundaries with further testing by means of a large spot to determine a definite pattern of response. In most visual cells of PO (23 cells in 30)) the receptive fields present had a great eccentricity, so that their centers often were more than 30 deg from the visual axis. The diameters of the receptive fields were so large that their full field dimensions were never completely mapped with our apparatus (Fig. 8). Throughout the domain of the receptive field, . . . . .

. .. . ..

B

A

.200

.200

2o”

200

. . . . . . . . . . . . . . FIG.

. . . .

. . . . .

. .‘. . . . . . .. . .

. . . . . .

. . . . . . . . . . . . . . . . . ..*.*e*

. . . . . .

8. Receptive fields of visual

. . . . . .

20° . . . . . . .

. . . . . . .

cells of PO.

-20”

Dotted

areas

:::::: . . . . . . . . .

. . . . . . . . . .

. . . . . . . . . . . . .

represent

. . . . . . . . . . . . . .

. . . . . . . . . . . . . . field,

response patterns were usually fised, that is of the on-off type. Some cells were difficult to map with a small light spot because they responded too sluggishly and their response declined with repeated stimulation. Furthermore, repeated illumination with a small light spot often evoked various patterns of response. On, off, and on-off types of response were randomly elicited with light stimuli applied to same position of the receptive field. Some visual cells responded only with an illumination with large light spots 20 deg in diameter. The response pattern of this type of cell was very irregular and was statistically identified by means of repeated illumination. Hill (8) also described units in the superior colliculus which responded sluggishly to light stimuli and had large receptive fields similar to these visual cells of PO. Two exceptional cells found in PO had concentrically organized receptive fields consisting of a circular off center with an annular on surround. The diameters of the receptive fields were 9 and 10 deg, respectively. Two other cells were found sensitive to one-directional movement of light-dark edge. Their receptive fields were located at about 30 deg from the visual axis. Short Latency Visual Cells in PO. We found three units in PO which

POSTERIOR

363

THALAMUS

responded to optic tract stimulation with a relatively short and invariant latency. As seen in Fig. 9A, five successive stimuli applied to the optic tract evoked spikes each time with a latency of about 1 msec. The cells showed spontaneous activity of more or less irregularity fluctuating around a mean discharge rate of about lO/sec. The receptive fields had large diameters located with great eccentricity (Fig. 9D). Throughout their domain, the cell responded briskly at the on and off of illumination with a Z-degree diameter light spot (Fig. B) .

A-

A-

........ ........ .. ...**.* . . . . . . . II ...*..*** ..***** I C .... FIG. 9. Short latency visual cell in PO. A, responses to OT stimulation. Time marker, 1 msec. B, responses to small light spot applied to part of receptive field. C, site of recording in stereotaxic map. D, receptive field.

Discussion

The foregoing results show that many neurons located in the upper half of the posterior group of the thalamic nuclei have visual properties. This was verified by the fact that the neurons responded to electric stimulation to the optic tract and also when the eyes were illuminated. The response latencies to OT stimulation were widely distributed with a range of 1-15 msec, and this latency distribution can be accounted for in terms of the variety of synaptic connection made on the cell by the visual pathways. The short-latency cells (Fig. 9) may be activated via a simpler synaptic chain (probably monosynaptic) on OT stimulation, while the long latency cells may be activated via a multisynaptic chain. The short latency cell may

364

SUZUKI

AND

KATO

have a great degree of convergence in their innervation by the visual paths. This inference comes from their larger receptive fields. Such a variety of synaptic organization can not be explained by Calma’s (4) postulate that visual influences to PO are produced solely via a pathway involving the visual cortex. This is easily ruled out because cortical cells in the visual area are usually excited with an action potential have a latency of several msec on stimulation of the optic tract. This follows if the cell in PO is activated with at least the latency of a few msec. This assertion is not relevant to the shorter latency cell having a latency of only 1 msec. According to Bishop and Clare (2). PO cells are intercalated in layer B of the LGN. In this case, PO cells should be only influenced by the contralateral eye. However, the present experiments have revealed that most visual cells of PO are binocularly influenced, a fact incompatible with the hypothesis of Bishop and Clare. Since some visual cefls can be activated antidromically by stimulation of the optic radiation (Fig. 6D), it may be said that some fiber projections are present from PO to the visual cortex. Comparable anatomical data for this proposition has already been provided by means of retrograde cell degeneration (IO. 16). The comples nature of the synaptic organization present in PO described above, indicates that the upper half of the PO of the thalamus may be a visual integrating center, one in which visual impulses go to suecessive cells via a complex synaptic linkage. Temporal and spatial summation may be necessary for a transmission of impulses in PO. This was suggested by the fact that natural stimuli using illumination of the eye is much more effective than electrical stimulation to the optic tract. Furthermore, transmission is closely dependent on reticular activity. We have reported that lateral geniculate neurons receive a facilitatory influence from the reticular formation ( 17 ). In the geniculate neurons, however, an optic tract volley can activate neurons without a reticular volley, and therefore, reticular influence is effective only to change the subliminal state of excitability of the geniculate neuron. In contrast, some PO neurons can fire only with the help of a reticular volley. Hassler (6) also postulated that the pulvinar may be relay station of a secondary visual path to the visual area of the cerebral cortex. Recently, neurons in the LGN were sorted into P and I cells by means of their responses to OT stimulation (3, 7, 12. 15). The P cells responded with short latency action potential, the I cells with long bursts of spikes and with a long latency. The visual cells of PO resemble the I cells with regard to their latency, but they did not show repetitive firing on OT stimulation. In this respect, the I cells differ from the visual cells of PO. Histologically identified LGN cells were activated with spikes having a

POSTERIOR

THALAMUS

365

latency shorter that 4 msec (Fig. 2A). The long latency LGN cells described by others may at least in part have included some of the visual cells of PO. References

J. 1962. Some fiber projections to the superior colliculus in the cat. J. Cow@. Neural. 119 : 77-95. BISHOP, G. H., and M. H. CLARE. 1955. Organization and distribution of fibers in the optic tract of the cat. .I. Comp. Neural. 103 : 269-304. BURKE, W., and A. J. SEFTON. 1967. Discharge patterns of principal cells and interneurones in lateral geniculatc nucleus of rat. J. Physiol. London 187: 201212. CALMA, I. 1965. Activity of the posterior group of thalamic nuclei in the cat. J. Physiol. London 180 : 35&370. GREEN, J. D. 1958. A simple microelectrode for recording from the central nervous system. Nature 182 : 962. HASSLER, R. 1964. Die zentralen Systeme des Sehens, pp. 229-251. In. “Bericht iiber die 66 Zusammenkunft der Deutschen Ophthalmologischen Gesellschaft in Heidelberg.” J. F. Bergmann, Miinchen. HAYASHI, Y., I. SUMITOMO, and K. IWAMA. 1967. Activation of lateral geniculate neurons by electrical stimulation of superior colliculus in cats. Japan. J. Physiol. 17 : 638-651. HILL, R. M. 1966. Receptive field properties of the superior colliculus of the rabbit. Nature 211: 1407-1409. JASPER, H. H., and C. AJMONE-MARSAN. 19.54. “A stereotaxic atlas of the diencephalon of the cat.” The National Research Council of Canada, Ottawa. MAJOROSSY, K., M. R~THELYI, and J. SZENTAGOTHAI. 1965. The large glomerular synapses of the pulvinar. J. Hirnforschmg 7 : 415432. MEIKLE, T. H. JR., and J. M. SPRAGUE. 1964. The neural organization of the visual pathways in the cat. Intern. Rev. Neurobiol. 6: 149-189. NODA, H., and K. IWAMA. 1967. Unitary analysis of retinogeniculate response time in rats. Vi&o% Res. 7 : 20.5-213. POGGIO, G. F., and V. B. MOUNTCASTLE. 1960. A study of the functiondl contributions of the lemniscal and spinothalamic system to somatic sensibility. Central nervous mechanisms in pain. BUZZ. Johns Hopkini Hosp. 106: 266316. ROSE, J. E., and C. N. WOOLSEY. 1958. Cortical connections and functional organization of the thalamic auditory system of the cat, pp. 127-150. In “Biological and Biochemical Bases of Behavior.” H. F. Harlow and C. N. Woolsey [eds.]. University of Wisconsin Press, Madison. SAKAKURA, H. 1968. Spontaneous and evoked unitary activities of’ cat lateral geniculate neurons in sleep and wakefulness. Japan. J. Physiol. 18: 23-42. SPRAGUE, J. M. 1966. Visual, acoustic, and somesthetic deficits in the cat after cortical and midbrain lesions, pp. 397-417. 1% “Thalamus.” D. P. Purpura and M. Yahr teds.]. Columbia University Press, New York. SUZUKI, H., and N. TAIRA. 1961. Effect of reticular stimulation upon synaptic transmission in cat’s lateral geniculate body. Japan. J. Physiol. 11: 641-655. SUZUKI, H., and Y. TUKAHARA. 1963. Recurrent inhibition of the Betz cell.

1. ALTMAN, 2.

3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13,

14.

15. 16.

17. 18.

Japan.

J. Physiol.

13 : 36398. ,