Activity of ventrolateral thalamic neurons related to posture and movement during contact placing responses in the cat

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Brain Research, 61 (1973) 400-406 O Elsevier ScientificPublishing Company, Amsterdam - Printed in The Netherlands

Activity of v e n t r o i ~ l thalamic neurons related to posture and movement during contact placing responses in the cat

JEAN MASSION AND ALLAN M. SMITH Ddpartement de Neurophysiologie gdndrale, Institut de Neurophysiologie et Psychophysiologie, Centre National de la Recherche Scientifique, 13274 Marseille Cedex 2 (France)

(Accepted July 2nd, 1973)

The integration of posture and movement is one of the most important functions of the motor structures of the central nervous system. Martin lz has hypothesized that the neural systems related to posture and movement are somewhat independent of one another and that, in man, the postural adjustments that are particularly related to equilibrium are organized within the basal ganglia. Recent evidence from studies using chronic unit recording, however, suggests that the basal ganglia7, s,9 as well as the cerebellumlS, 16 and the ventrolateral nucleus of the thalamus~,3, 9 may also play an important role in the initiation of movement. Since both the basal ganglia and the cerebellum send a significant number of efferents to the ventrolateral thalamic nucleus (VL), it was decided to undertake a microelectrode exploration of this structure in the awake cat using the contact placing reaction as a simple method for evoking both postural adjustments and movement. Since Bard's 4 original observation that ablation of the pericruciate motor cortex produces deficits in the contact placing response, considerable evidence has accumulated to suggest that this reaction is also impaired by lesions of the VL, and the red nucleus as well as the interposate and dentate nuclei of the cerebellum 1-a,5,6. It would appear, therefore, that the contact placing response depends not only on the motor cortex but also relies on the integrity of the entire cerebello-thalamo-cortical pathway and the rubrospinal tract as well. In the present study the traditional method of eliciting contact placing (in which the animal is held in the arms and with the eyes averted, the dorsal surface of the forelimb is brought in contact with the edge of a flat hard surface such as a table top) was altered to allow standardized placing tests to be administered and to give the animal as much freedom as possible to make postural adjustments. Chronically prepared cats were habituated to standing quietly in a restraining hammock with all 4 feet in contact with a firm supporting surface. The isometric postural pressures exerted by each of the forelimbs was measured by strain gauge force transducers under each limb. To ensure that each animal maintained adequate postural tonus a minimum pressure of 250 g was generally required from each of the forelimbs before a placing response was evoked. The contact placing was elicited by one of two mobile

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sliding plates, hidden from the view of the animal which could be brought into contact with the dorsal surface of the distal part of either forelimb. A photoelectric cell attached to the leading edge indicated the onset and duration of the contact stimulus which lasted up to the moment that contact was broken by the lifting phase of the placing reaction. A potentiometer fixed about the elbow joint indicated the beginning, amplitude and form of the placing movement. Electromyographic recordings were also taken from the biceps and triceps muscles. Testing was conducted randomly on either forelimb to prevent any possible anticipation by the animal. An analysis of several hundred placing reactions in several different animals indicated that the placing reaction tested in this way showed two temporally distinct phases. Within the first hundred milliseconds after the arrival of the contact stimulus the isometric force exerted by the tested limb began to decline to zero and there was a simultaneous increase in force by the contralateral limb. We have called this phase the postural adjustment. Following the postural adjustment, at a somewhat longer and more variable latency (mean ----480 msec), the movement phase began with the first deflection of the potentiometer and the associated activation of the biceps muscle. Flexion of the limb continued until contact was broken and finally an extension movement placed the limb on the upper surface of the mobile plate. Typical examples of the recordings made during the postural adjustment and movement components of the placing reaction are shown in Fig. 1. In each placing reaction the contact stimulus elicited a movement in the stimulated forelimb (phasic limb) and an increase in the contralateral force in the contralateral forelimb (postural limbs). In view of the fact that the VL influences the contralateral limb via connections to the ipsilateral motor cortex, it was possible to consider that in any placing reaction the VL opposite the phasic limb was the phasic VL and that the VL opposite the PLACING Postural

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Fig. 1. Analysis of the modified placing reaction into postural adjustment and movement phases. On the left all the recordings, except for the isometric force of the postural limb, were taken from the limb making the placing reaction. On the right all recordings, except for the isometric force of the limb making the placing movement, were made from the postural limb. Abbreviations: Bi.c, contralateral biceps activity; Bi.i, ipsilateral biceps activity; F.c, contralateral isometric postural force; F.i, ipsilateral isometric postural force; Pot. c, potentiometer on contralateral limb (no movement shown); Pot.i, potentiometer on ipsilateral limb (movement shown); Tri.c, contralateral triceps activity; Tri.i, ipsilateral triceps activity. S: moment of contact of moving plate with paw. Mt: moment of removal of paw from leading edge of plate.

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postural limb was the postural VL. With this organization in mind, the spike discharge of single cells in the ventrolateral nucleus of the thalamus was recorded using tungsten microelectrodes sealed in glass tubes. The tungsten microelectrodes were driven by a stereotaxically implanted screw-type mechanical micromanipulator. Cells within the VL were tested for their reactions to movement by eliciting between 5 and 12 placing responses from the forelimb contralateral to the recording electrode. The reaction of the same VL cells to the adjustments made by the postural limb were tested by eliciting between 5 and 12 placing responses from the limb ipsilateral to the recording electrode. In about half of the cases it was possible to identifiy VL cells electrophysiologically by means of chronically implanted stimulating electrodes. Stimulation of the dentate and posterior interpositus nuclei was used to determine, whenever possible, the afferent cerebellar projections to the cell and antidromic stimulation of the motor cortex was used to establish the destination of its axon. At the end of every microelectrode penetration a small coagulation was made (cathodal current of 30 #A for 15 sec) and the total number of penetrations in any given animal never exceeded 5 in order to determine the location of the recorded neurons in histological sections with a maximum degree of precision. At the end of each experiment the animal was sacrificed and the brain was perfused with formalin. Serial coronal sections through the VL were stained with cresyl violet. A total of 80 cells were tested for reactions to the placing reaction. Slightly less than half the total number of cells tested (N : 39) showed a change of activity. For 38 cells, an increase in discharge frequency was observed. Only one cell showed a clear simple inhibition although a few cells responded with a complex sequence of discharge involving an activation, inhibition and reactivation pattern. In general, the simple increase in discharge frequency apparent in most reactive cells was quite variable in latency of onset and duration. Twenty-two cells reacted only when the contralateral limb was the placing limb (i.e. phasic limb), and an example of such a cell is shown in Fig. 2, on the left. Fourteen cells could be consistently activated regardless of whether the contralateral limb was the placing limb or the postural limb. An example of activation when the contralateral limb was the postural limb is shown in Fig. 2, on the right. Three cells could be activated only when the contralateral limb was the postural limb. Many of the postural and phasic VL cells showed an increase in frequency of discharge before either the movement or the postural adjustment but the increased firing rate often continued into the time period occupied by the movement or the

Fig. 2. Two examples of reactive cell in ventralis lateralis. On the left the spike activity from a VL cell is shown for 10 placing reactions elicited from the limb contralateral to the recording electrode. The recordings have been aligned with the end of the contact stimulus. This cell received afferents from the dentate and posterior interpositus nuclei of the cerebellum and sent its axon to the motor cortex. On the right the spike activity from a VL cell is shown for l0 placing reactions elicited from the limb ipsilateral to the recording electrode. These recordings have been aligned with the arriVal of the contact stimulus. This cell sent its axon to the motor cortex. Abbreviations: VL, spike discharge from a VL cell; Pot, output from the potentiometer indicating movement;S, arrival of the contact stimulus; Mt, termination of the contact stimulus by the movement.

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postural adjustment. A substantial number of the cells showed an increase in discharge frequency that preceded the movement by several hundred milliseconds. The relatively short latency of this response can probably be accounted for by the somatic (i.e. contact) nature of the stimulus initiating the movement and the fact that some postural changes in the moving limb precede the beginning of movement. This would seem to agree with Evarts 11 finding that in the monkey, motor cortex units react with much shorter latency when the conditioned stimulus is applied to the limb making the movement as opposed to a movement initiated by a light stimulus. Since we were unable to show responses to light touch in our cells, we have tended to interpret this early activation as indicating some fairly rapid (less than 40 msec) proprioceptive input to VL. This hypothesis is being subjected to further investigation. There were also a surprising number of cells reacting to the postural adjustment at such long latencies as to suggest that continuous postural adjustment was being made even during the movement. Unlike the pyramidal cells of the precentral gyrus of the monkey 1° the cells in VL did not appear to be strictly locked to a particular phase of the movement such as flexion or extension. A possible explanation for this finding is provided by some recent studies by Rispal-Padel et al. ~3 who have shown that a single VL cell can send branching axons to widely different areas of the motor cortex. This would suggest that the activity of cells in VL might be more easily correlated with complex movements or postural adjustments rather than with simple individual muscle contractions. The distribution on both reactive and non-reactive cells has been plotted on a series of 6 standard drawings of the VL seen in frontal sections (Fig. 3). There is a marked tendency for reactive cells to be found in the lateral portion of the nucleus as compared to non-reactive cells which are located more medially. These data would suggest that the distribution of cells concerned with the motor control of posture and movement in this particular behavioral situation can be almost perfectly superimposed. The somatotopographic organization of the VL in the mediolateral plane is difficult to distinguish and the separation of the cells controlling the various parts of the body shows considerable overlap in the middle of the nucleus. This is supported by both anatomical and electrophysiological evidence 13,14. Nevertheless, the most medial region projects to the part of the motor cortex controlling axial muscles whereas the lateral portion projects to the part of the motor cortex controlling the distal muscles. The fact that cells reactive to movements and postural adjustments were located laterally in VL would suggest that in the present behavioral context the postural adjustments required the participation of the distal musculature to about the same extent as the movement. The behavior of the reactive cells and their anatomical distribution taken together failed to show evidence for spatially separated postural and phasic systems. Not only were the populations of posturat cells and movement cells in the same general area of the nucleus, but the integration of postural and kinetic activity appears to occur at the unitary level within VL and therefore very probably in the motor cortex as well. That is, the same cell could react to the demands both for postural adjustments and for movements, although the pattern of discharge demon-

SHORT COMMUNICATIONS phallic

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Fig. 3. Distribution of reactive cells in ventralis lateralis. Cells reactive when the contralateral limb was the placing limb have been shown with large filled circles and have been indicated on 6 coronal sections under the heading of Phasic VL, whereas cells reactive when the contralateral limb was the postural limb have been shown by large filled circles in 6 coronal sections under the heading Postural VL. The small dots indicate unreactive cells. strated by these cells most frequently differed under these two conditions. The dual control of posture and movement which occurs at the cellular level within the cerebello-thalamocortical pathway implies that posture and movement may well be controlled by the same final efferent pathway and that the cortical access to spinal motor neurons is identical. This does not imply, however, that control of posture and movement cannot be performed separately by other structures. We wish to thank A. Grangetto, R. Haour, R. Massarino and P. Quilici for their skillful technical assistance. A.M.S. gratefully acknowledges the personal support of the Medical Research Council of Canada. J. M. wishes to acknowledge the support of the 'Fondation pour la Recherche m6dicale fran~aise'.

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