Adjustments of posture accompanying voluntary movements. Normal and pathological aspects.
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Biomedical subjects
Publications and source records attributed to J Massion.
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Experiments were performed to examine the responses of cortical neurons in the pericruciate cortex to cutaneous afferent input from the distal forepaw. Ninety-nine cortical neurons responding to electrical stimulation of the forepaw were recorded from four cats. Their response latencies ranged from 6 to 23 ms. The units had cutaneous receptive fields which ranged in size from those restricted to one digit to those extending over the whole forelimb. They were recorded from area 4 and area 3. Intracortical microstimulation at the recording sites activated either the distal or proximal musculature of the forelimb. When the characteristics obtained from each recording site were examined as a group of features, a uniform population emerged which was significantly different from the rest of the sample. These units had the shortest latency responses to distal forepaw electrical stimulation, the shortest duration of evoked discharge, the smallest distal cutaneous receptive fields. Such units were recorded at the border between areas 3 and 4, at sites which on microstimulation resulted in movements of the distal forepaw musculature.
Thalamic nuclei constitute the diencephalic relay system between different afferent systems and the telencephalon. The "motor" thalamus links cerebellar and pallidal afferents with the motor and pre-motor cortical regions. Separation of pallido-thalamo-cortical and cerebello-thalamo-cortical pathways is relatively complete: afferents of pallidal origin are relayed by thalamic nuclei VA, VLo and VLm and are projected onto prefrontal and supplementary motor areas whereas afferents of cerebellar origin are relayed in the VL and VPLo and then projected onto motor areas 4.6 and parietal areas 5 and 7. This report is concerned mainly with the analysis of the motor thalamus as a relay system for afferents of cerebellar origin. The anatomofunctional organization of the cerebello-thalamo-cortical tract possesses a topographic arrangement and also wide convergences and appears able to participate in the realization, through the motor cortex, of motor synergies and of co-ordinating postures and movements. The cerebello-cortical tract apparently plays a different role during learning of a movement and executing an automatized movement. For the latter, it is involved in their onset and in their completion. Its contribution to fine control of temporal parameters of motor commands or control of peripheral afferent messages is not decisive. During learning of a movement the cerebello-cortical tract plays a predominant role. According to Ito, the cerebellum is involved in the process of automatization of a movement, organized initially entirely by the cortex and then becoming progressively subcortical. Plasticity of cerebellar microcircuits could be the basis for these automatization processes expressed through the cerebello-thalamo-cortical tract.
The postural response to an unexpected drop of either hindlimb platform was studied in the freely standing cat. The vertical forces, the forelimb electromyographic (EMG) activities and the movement of the trunk were analysed. A stereotyped diagonal pattern of support was observed. The imposed unloading of one hindlimb was followed by unloading of the diagonally opposite forelimb and loading of the two other limbs. In the ipsilateral loaded forelimb, the force increase is preceded by an activation of the biceps and is concomitant with a triceps coactivation. In the contralateral unloaded forelimb, reciprocal changes of biceps (activation) and triceps (inhibition) were observed and preceded the force decrease. Lateral or vertical displacement or rotation of the vertebral column at the high thoracic level, as evidenced by movie recording, began no earlier than 100 ms after the hindlimb drop and thus followed the EMG changes. Unilateral sensorimotor cortex ablation had no effect on this pattern or on the latencies of forelimb myographic responses. These results suggest that the hindlimb drop triggers stereotyped forelimb EMG responses which are organized centrally and that these responses are not mediated via a sensorimotor cortical loop.
Human subjects sitting in a chair were asked to maintain their right forearm in a horizontal position in half supination. The forearm was loaded with a constant weight of one kilogram. Vertical force at the wrist level, angular position of the elbow and EMG activity of biceps, brachio-radialis and triceps muscles were recorded. Unloading was tested under four different conditions, the first two having been used in a previous study (Hugon et al. 1982): Voluntary unloading by the subject's other hand. An "anticipatory" deactivation of the load bearing forearm flexors is observed preventing the elbow rotation of that arm. Unpredictable passive unloading. This results in an upward forearm rotation which provokes the classical "unloading reflex". Two new conditions were tested in the present paradigm: Imposed unloading predictable in time (tone signal preceding unloading by a fixed interval). Unloading being actively triggered when the subject presses a key. Under the two latter conditions, no anticipatory deactivation of the flexor supporting muscles preceding the onset of unloading as in situation A was observed. During the first 120 ms after the onset of unloading, the forearm rotation was the same as in situation B (unpredictable passive unloading). Thereafter, the rotation was smaller in some subjects, apparently due to an ameliorated reflex action. It is concluded that temporal information concerning the precise time of the unloading or the triggering of the load release by a voluntary movement (key press) was not by itself able to induce the anticipatory deactivation of the forearm flexors that was seen with a coordinated voluntary release of the load by the contralateral arm.
Voluntary movements are the source of a perturbation of posture and equilibrium. They are accompanied by postural adjustments which show three main characteristics: they are "anticipatory" with respect to movement and minimize the perturbation of posture and equilibrium due to the movement; they are "adaptable" to the conditions in which the movement is executed, they are influenced by the instructions given to the subject concerning the task to be performed. The central organization of the postural adjustments associated with movement is still largely unknown. The possibility is examined that a "repertoire" of postural adjustments exists; the possible sites of the repertoire are discussed as well as the level at which the parallel or "sequential" control of posture and movement might be organized.
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Normal human subjects, sitting in a chair, were required to maintain stable elbow flexion against loads of 0.5 kg or 1.0 kg. Unloading was affected either 'passively' by the experimenter, or 'actively' with the subject's own contralateral arm. Elbow angle, force exerted by the load, and electromyographic activity (EMG) of biceps and triceps muscles of both arms were recorded and averaged. 'Passive' unloading was followed by a reduction of biceps EMG activity, starting 50--80 ms after weight lift, and by an upward deflection of the forearm. With 'active' unloading, however, a reduction of the biceps EMG activity slightly preceded the onset of unloading (0--30 ms). This reduction of the 'actively' unloading arm occurred at about the same time as the activity of the contralateral unloading arm. In this experiment, the unloaded forearm maintained an almost stable position. Thus, the anticipatory adjustment of elbow posture, observed when unloading was performed by the subject, appears to optimize limb stability during the mechanical perturbation.
The posterior red nucleus (PRN) was studied in two species of primates by the technique of retrograde degeneration of rubrospinal cells following transection of the spinal cord at different levels. The form of the PRN was reconstructed for both a quadruped monkey (baboon) and an anthropoid with erect posture (gibbon). The PRN contains polymorphic cells characterized by their very chromophilic and granular Nissl substance. These neurons vary in diameter from 25 micrometer to 70 micrometer. Some of them give rise to the rubrospinal tract. Baboon: The approximately 1,300 rubrospinal cells in this species are divided into two equal groups, one related to the contralateral forelimb, with axons ending between the second cervical and third thoracic segment, and the other related to the contralateral hindlimb, projecting caudally beyond T3. Following a high cervical lesion, nondegenerated cells of similar description remain throughout the nucleus. A significantly large group of these cells occurs medially and may be the source of fibers ending in the brain stem or cerebellum. Gibbon: In this species, the number of rubrospinal cells controlling the hindlimb is less than half that found in the baboon. This reduction in the gibbon is much greater for medium-sized cells, but is also significant for the giant cells. These results obtained from primates are compared with those reported for the cat. A possible function for the PRN in the control of limb movements is discussed from the viewpoint of phylogeny.
The placing reaction in the standing cat permits the analysis of a movement, the placing movement, together with its postural support. It is provoked by one of two moving plates coming into contact with one forelimb. Each limb rests on a platform equipped with strain gauges which permit changes in force exerted by each limb to be recorded. The placing reaction is characterized by two phases, an early isometric phase lasting until the lift-off of the stimulated limb occurs. It is then that a diagonal postural support on one forelimb and the opposite hindlimb takes place so that the placing movement can take place. Performance of this movement corresponds to the second phase. Four cats underwent an unilateral lesion in sensorimotor cortex. Two animals had a large lesion extending to the pre- and post-cruciate regions and from the midline to the coronal sulcus, including a large part within the depth of that sulcus. Two other cats had a restricted lesion covering mainly the forelimb part of area 4. After extensive cortical lesions, permanent changes in the contralateral placing reaction were observed. The isometric phase increased in duration, without marked changes of the pattern of postural support whereas the movement was prolonged and usually hypermetric. On the contrary, ipsilateral placing with its associated postural support was unmodified. After restricted cortical lesions, only temporary changes were observed. Recuperation was complete within 30 postoperative days. It was concluded that motor cortex on one side controls, as a whole, the contralateral placing movement and its associated postural adjustment, whereas it does not significantly modify the ipsilateral placing and its associated postural responses notwithstanding the use of the contralateral limbs in this adjustment.
A comparative analysis of adjustment of posture for performance of different kinds of local movements (movements elicited by electrical stimulation of the motor cortex; proprioceptive reaction of placing the paw on a support, conditioned lifts of the paw) was made in cats and dogs. The present experimental data were obtained in two laboratories independent of each other. For their quantitative analysis a number of criteria was elaborated which allow to obtain characteristics of the posture at concrete moments and differential characteristics based on the measurement of vertical forces of the limbs support. It was shown that the general characteristics of posture adjustment (the so called diagonal pattern) are identical in cats and dogs and in different kinds of movements; the degree of diagonality, however, depends considerably on the kind of movement. During conditioned movements the diagonality coefficient is higher in dogs than in cats.
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The postural adjustment which accompanies single limb movement in the standing cat and dog was analyzed. Four trays equipped with strain gauges were used for measuring the vertical forces exerted by each limb before and during movement performance. Three types of movements were analyzed: flexion movements elicited by motor cortex stimulation, placing movements, conditioned movements of either forelimb or hindlimb (lift-off in cat, flexion with maintained final position in dog). In both cats and dogs the postural adjustment during movement consists of a bipedal stance on two diagonally opposite limbs. Large quantitative differences were observed depending on the type of movement. Cortical stimulation elicited an adjustment where changes of forces exerted by the forelimb a hindlimb were nearly equal. During conditioned fore- and hindlimb lift-off in the cat there was a tendency to use only forelimbs for the postural adjustment associated with forelimb movement and hindlimbs for the adjustments associated with hindlimb movement. For placing in the cat and conditioned movement in the dog, the adjustment was intermediate, that is a predominant contribution of forelimb support with forelimb movements but nevertheless an associated contribution from hindlimbs. The general significance of the results with respect to the mechanism of postural adjustment associated with movement is analyzed.
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By measuring the forces applied by each limb supporting the weight of the standing quadruped (cat), before and during elicitation of the placing reaction, it was possible to examine quantitatively and qualitatively the postural events which preceded and accompanied forelimb displacement. The findings are summarized as follows: 1. Postural adjustment consists of a shift from quadrupedal stance to a tripodal stance to permit withdrawal of weight from one forelimb without loss of equilibrium. The animal's weight is not equally distributed between the three supporting limbs but the majority of the weight is supported by the diagonally opposing limb pair. 2. During the isometric phase of the placing reaction, the animal's projected center of gravity moves contralaterally, across the diagonal line between the contralateral forepaw and the ipsilateral hindpaw, and comes to rest within the triangular zone outlined by the three supporting limbs. 3. The diagonal supporting stance is a maneuver of an anticipatory nature which precedes and accompanies the placing reaction. 4. The force changes exhibited by each limb to bring the animal to the stereotyped diagonal supporting stance illustrated that the way to achieve this is consistent within a given animal, but differs from one animal to another. The pattern in the same animal is generally symmetrical when lifting the right or left forepaw. 5. The data from the cat are compared to observations in other quadrupeds and man.
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The activity of neurons in the ventrolateral nucleus of the thalamus (VL) was analyzed in the cat during placing movements of both the right and left forelimbs. The purpose was to determine if thalamic neuron discharge patterns could be related to movement and/or to postural changes. Placing tests were conducted on animals maintained in a standing position and partially restrained by a hammock. Each of the forelimbs rested on a flat surface containing a strain gauge which allowed the stance forces to be measured. Two mobile plates, one on the left and one on the right, were used to elicit a contact placing reaction. The response was composed of an isometric phase, during which the body weight was shifted from the stimulated limb to the opposite forelimb while the stimulated limb was gently pushed backwards, and a movement phase during which the stimulated paw actually accomplished the placing reaction. (1) About half the recorded neurons (47/86) in the VL region demonstrated a change in activity, generally an increase of discharge frequency, during placing of the right of left forelimb. (2) Almost all the reactive units (45/47) responded to contralateral placing. Two units changed their activity with ipsilateral placing only, whereas 18 units were active during placing of both forelimbs. The discharge pattern of cells activated during ipsilateral placing was considered as related to the isometric postural adjustment of the contralateral limbs. (3) Cells reactive during contralateral tests were located preferentially in the ventrolateral part of VL. Units reactive during ipsilateral tests (postural units) were also clustered in the ventrolateral half of VL which is the zone controlling limb musculature. Some of the 'postural units' were identified as receiving afferents from cerebellar nuclei and projecting to motor cortex. (4) Changes in discharge frequency were observed during either the isometric phase, the movement phase, or both. The same type of patterns were observed during contralateral and ipsilateral placing. About half of the cells responding during the contralateral placing movement did so throughout the entire duration of the movement, and were not specifically related to either the flexion or the extension phase of the placing. (5) The timing of the discharge of VL units with respect to the isometric phase and to the movement phase of the motor sequence varied from cell to cell. No topographic arrangement of neurons with the same pattern of discharge could be found within the nucleus.
1. A cat, restrained in a hammock, stands with its feet on supporting trays each furnished with strain gauges to measure the isometric upthrust. Placing reactions are elicited by contact of the left or right forelimb with a moving tray. The placing movement is preceded and accompanied by a postural adjustment characterized by an increase of the upthrust exerted by the opposite forelimb. 2. After ablation of the motor cortex on one side, the placing movement of the contralateral forelimb is abolished for the first few days after the operation and thereafter is delayed. However, the postural adjustment of the ipsilateral forelimb persists, with the same range of latencies as before the operation. 3. After unilateral motor cortical ablation, the contralateral forelimb still takes part in the postural adjustment associated with the placing movement of the other forelimb. 4. In two cats which had 2 years earlier undergone a total cerebellectomy, the placing movement was lacking or appeared with a long delay, whereas a postural adjustment of the other forelimb could be observed, although reduced. 5. The results indicate that the nervous structures responsible for the movement and for the associated postural adjustment are separate but partially linked.