Neural integration of movement: role of motor cortex in reaching

The study of the motor cortex in behaving monkeys during the past 20 years has provided important information on the brain mechanisms underlying motor control. With respect to reaching movement in space, a key role of motor cortex in specifying the direction of reaching has been proposed on the basis of results from studies of the activity of cells and cell populations during reaching. These results and ideas are reviewed and discussed in the context of recent findings concerning the spinal mechanisms underlying reaching movements.     

Role of different projection areas of the motor cortex in reorganization of the innate head-forelimb coordination in dogs

Dogs were trained to perform the forelimb tonic flexion in order to lift a cup with meat from a bottom of the foodwell and hold it during eating with the head bent down to the cup. It is known that conditioning of the instrumental reaction is based on reorganization of the innate head-forelimb coordination into the opposite one. In untrained dogs, the forelimb flexion is accompanied by the anticipatory lifting of the head bent down to the foodwell. The following lowering of the head leads to an extension of the flexed forelimb. Tonic forelimb flexion is possible if the head is in the up position. Simultaneous holding of the flexed forelimb and lowered head providing food reinforcement is achieved only by learning. It was shown earlier that the lesion of the motor cortex contralateral to the "working" forelimb led to a prolonged disturbance of the elaborated coordination and reappearance of the innate coordination. In the present work we studied the influence of local lesions of the projection areas in the motor cortex, such as a "working" forelimb area, bilateral representation of the neck, and the medial part of the motor cortex, on the learned instrumental feeding reaction. It was found that only the lesion of the forelimb but not neck projection led to a disturbance of the learned head-forelimb movement coordination.     

Direction of movement is encoded in the human primary motor cortex

The present study investigated how direction of hand movement, which is a well-described parameter in cerebral organization of motor control, is incorporated in the somatotopic representation of the manual effector system in the human primary motor cortex (M1). Using functional magnetic resonance imaging (fMRI) and a manual step-tracking task we found that activation patterns related to movement in different directions were spatially disjoint within the representation area of the hand on M1. Foci of activation related to specific movement directions were segregated within the M1 hand area; activation related to direction 0° (right) was located most laterally/superficially, whereas directions 180° (left) and 270° (down) elicited activation more medially within the hand area. Activation related to direction 90° was located between the other directions. Moreover, by investigating differences between activations related to movement along the horizontal (0°+180°) and vertical (90°+270°) axis, we found that activation related to the horizontal axis was located more anterolaterally/dorsally in M1 than for the vertical axis, supporting that activations related to individual movement directions are direction- and not muscle related. Our results of spatially segregated direction-related activations in M1 are in accordance with findings of recent fMRI studies on neural encoding of direction in human M1. Our results thus provide further evidence for a direct link between direction as an organizational principle in sensorimotor transformation and movement execution coded by effector representations in M1.     

The supplementary motor area is implicated in the coordination between posture and movement in man

The aim of the present experimental series was to investigate the central organization of the coordination between posture and movement in a bimanual load lifting task. The seated subject was instructed to maintain horizontal one forearm (postural arm) which was loaded with a 1 kg weight. The unloading was performed either by the experimenter (imposed unloading) or by a voluntary movement of the other arm (bimanual unloading). With the bimanual unloading, the movement control was accompanied by an anticipatory adjustment of the postural forearm flexors activity, which resulted in the maintenance of the forearm position despite the unloading. No change in the anticipatory postural adjustment was observed in one patient with complete callosal section. It was reduced in 5 patients with lesion of the SMA region, but only when the postural forearm was contralateral to the lesion. It is suggested that the SMA region contralateral to the postural forearm may select the circuits responsible for the phasic postural adjustments which are necessary to ensure postural maintenance, whereas the motor cortex contralateral to the voluntary movement controls both the movement and, via collaterals, the preselected circuits responsible for the associated postural adjustment.     

Whisker motor cortex ablation and whisker movement patterns

Previous studies, based on qualitative observations, reported that lesions of the whisker motor cortex produce no deficits in whisking behavior. We used high-resolution optoelectronic recording methods to compare the temporal organization and kinematics of whisker movements before and after unilateral lesions of whisker motor cortex in rats. We now report that while the lesion did not abolish whisking, it significantly disrupted whisking kinematics, coordination, and temporal organization. Lesioned animals showed significant increases in the velocity and amplitude of whisker protractions contralateral to the lesions, as well as a reduction in the synchrony of whisker movements on the two sides of the face. There was a marked shift in the distribution of whisking frequencies, with reduction of activity in the 5–7?Hz bandwidth and increased activity at <?2?Hz. Disruptions of the normal whisking pattern were evident on both sides of the face, and the magnitude of these effects was proportional to the extent of the cortical ablation. We suggest that the observed deficits reflect an imbalance in cortical inputs to a brainstem central pattern generator.     

Whisker motor cortex ablation and whisker movement patterns

Previous studies, based on qualitative observations, reported that lesions of the whisker motor cortex produce no deficits in whisking behavior. We used high-resolution optoelectronic recording methods to compare the temporal organization and kinematics of whisker movements before and after unilateral lesions of whisker motor cortex in rats. We now report that while the lesion did not abolish whisking, it significantly disrupted whisking kinematics, coordination, and temporal organization. Lesioned animals showed significant increases in the velocity and amplitude of whisker protractions contralateral to the lesions, as well as a reduction in the synchrony of whisker movements on the two sides of the face. There was a marked shift in the distribution of whisking frequencies, with reduction of activity in the 5-7 Hz bandwidth and increased activity at < 2 Hz. Disruptions of the normal whisking pattern were evident on both sides of the face, and the magnitude of these effects was proportional to the extent of the cortical ablation. We suggest that the observed deficits reflect an imbalance in cortical inputs to a brainstem central pattern generator.     

Disruption of acquired head and paw movement coordination after unilateral lesioning of the motor cortex in dogs (a kinematic analysis)

Dogs were trained to remove a cup with meat to the head bent down to the feeder and hold the limb flexed during eating. At the early stage of learning, the stable innate head-forelimb coordination characteristic for untrained animals was manifest. The forelimb flexion was accompanied by anticipatory lifting of the bent head, and the following bending of the head led to an extension of the flexed forelimb. The opposite coordination, i.e., the lifting and holding of the forelimb when the head is bent down, was achieved only by training. The lesion of the motor cortex contralateral to the working forelimb in the trained dogs led to a prolonged disturbance of the simultaneous holding of the flexed forelimb and the head bent down. The lesion of the motor cortex did not affect the individual movements but disturbed their coordination. In the operated dogs the innate relationships between the head and forelimb movement recovered. The results support the previous finding that the lesion of the motor cortex led to recovery of the innate coordination transformed in the process of learning.     

Anticipatory activity in primary motor cortex codes memorized movement sequences

Movement sequences, defined both by the component movements and by the serial order in which they are produced, are fundamental building blocks of motor behavior. The serial order of sequence production is strongly encoded in medial motor areas. It is not known to what extent sequences are further elaborated or encoded in primary motor cortex. Here, we describe cells in the primary motor cortex of the monkey that show anticipatory activity exclusively related to a specific memorized sequence of upcoming movements. In addition, the injection of muscimol, a GABA agonist, into motor cortex resulted in an increase in the error rate during sequence production, without concomitant effects on nonsequenced motor performance. Our results challenge the role of medial motor areas in the control of well-practiced movement sequences and suggest that motor cortex contains a complete apparatus for the planning and production of this complex behavior.     

A specific function of the motor cortex in the reorganization of coordination in motor learning in animals and humans

The findings suggest that a particular function of MCx in motor learning involves suppression of synergies and co-ordination which interferes with acquisition of new motor patterns. Experimental animal models based on inhibition of certain natural synergies or reflexes in the process of learning new co-ordination have been developed where the MCx is responsible for inhibition of natural motor patterns. Following the MCx lesion the natural synergies dominate again and the learned movement cannot be adequately performed. Similar disturbances occur after combined lesions of the premotor and parietal associative cortex or after lesions of the cerebellar nuclei. However, after the associative cortex or cerebellar lesions the recovery of learned co-ordinations is possible. This suggests the inhibition of inappropriate synergies or co-ordination during motor learning is a specific function of the MCx, the latter taking part in organisation of new co-ordination between posture and movement in humans as well.     

I feel my hand moving: a new role of the primary motor cortex in somatic perception of limb movement

The primary motor cortex (MI) is regarded as the site for motor control. Occasional reports that MI neurons react to sensory stimuli have either been ignored or attributed to guidance of voluntary movements. Here, we show that MI activation is necessary for the somatic perception of movement of our limbs. We made use of an illusion: when the wrist tendon of one hand is vibrated, it is perceived as the hand moving. If the vibrated hand has skin contact with the other hand, it is perceived as both hands bending. Using fMRI and TMS, we show that the activation in MI controlling the nonvibrated hand is compulsory for the somatic perception of the hand movement. This novel function of MI contrasts with its traditional role as the executive locus of voluntary limb movement.     

Basal ganglia--possible role in motor coordination and learning.

The basal ganglia, with their inhibitory efferents, control motor outputs either directly by their projections to the midbrain motor regions or indirectly through the thalamic nuclei. Neural mechanisms in the basal ganglia act selectively to remove or enhance the inhibition so that different combinations of motor signals, which may act as neural templates for motor learning, are formed.     

Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination

Single neuronal activity was recorded from the supplementary motor area (SMA-proper and pre-SMA) and primary motor cortex (M1) in two Macaca fascicularis trained to perform a delayed conditional sequence of coordinated bimanual pull and grasp movements. The behavioural paradigm was designed to distinguish neuronal activity associated with bimanual coordination from that related to a comparable motor sequence but executed unimanually (left or right arm only). The bimanual and unimanual trials were instructed in a random order by a visual cue. Following the cue, there was a waiting period until presentation of a "go-signal", signalling the monkey to perform the instructed movement. A total of 143 task-related neurons were recorded from the SMA (SMA-proper, 62; pre-SMA, 81). Most SMA units (87%) were active in both unimanual contralateral and unimanual ipsilateral trials (bilateral neurons), whereas 9% of units were active only in unimanual contralateral trials and 3% were active only in unimanual ipsilateral trials. Forty-eight per cent of SMA task-related units were classified as bimanual, defined as neurons in which the activity observed in bimanual trials could not be predicted from that associated with unimanual trials when comparing the same events related to the same arm. For direct comparison, 527 neurons were recorded from M1 in the same monkeys performing the same tasks. The comparison showed that M1 contains significantly less bilateral neurons (75%) than the SMA, whereas the reverse was observed for contralateral neurons (22% in M1). The proportion of M1 bimanual cells (53%) was not statistically different from that observed in the SMA. The results suggest that both the SMA and M1 may contribute to the control of sequential bimanual coordinated movements. Interlimb coordination may then take place in a distributed network including at least the SMA and M1, but the contribution of other cortical and subcortical areas such as cingulate motor cortex and basal ganglia remains to be investigated.     

Anticipatory postural adjustment in bimanual unloading: role of the motor cortex in motor learning

The role of the motor cortex was investigated during learning unusual postural adjustment. Healthy subjects held their right (postural) forearm in a horizontal position while supporting a 1-kG load via an electromagnet. The postural forearm position was perturbed by the load release triggered by other elbow voluntary movement. Repetition of the imposed unloading test resulted in a progressive reduction of the maximal forearm rotation, accompanied by the anticipatory decrease in m. biceps brachii activity (learning). Control situation consisted of the voluntary forearm loading. Using the transcranial magnetic stimulation we examined changes in the motor evoked potential of the m. biceps brahii at the beginning and at the end of learning. The evoked potential amplitude did not significantly change in process of the decrease of m. biceps brachii activity. At the end of learning, motor evoked potential / baseline electromyogram ratio increased as compared to the beginning of learning and to the control situation. The results highlight the fundamental role of the motor cortex in suppression of synergies which interfere with formation of a new coordination during motor learning.     

Numerical study of coding of the movement direction by a population in the motor cortex

The fundamental statistical aspects of population coding of the movement direction in the motor cortex are studied numerically. The activity of neurons in a population is simulated using pseudorandom numbers so that the directional selectivity of the neurons is similar to that observed experimentally. Accuracy of the coding, which is evaluated by the root-mean-square (rms) error, is analyzed for various population sizes, degrees of variability of neuronal activity, and degrees of nonuniformity of distribution of the preferred directions. The dependence of the rms error on the population size shows a good fit to the inverse square-root law, from which it is estimated that a single population must contain around 10 000 neurons in order to attain the accuracy that allows 1 deg rms error, for example. The coding is studied further for populations with different types of tuning function. The results support the hypothesis proposed by Georgopoulos et al. (1988) except that the tuning function must be tuned in the sense that the average value of the function for movements with components in the preferred direction is larger than for movements away from the preferred direction.     

The innervation of the renal cortex in the dog

Summary Two cytochemical techniques were used at the ultrastructural level to study the distribution of specific axon types to different intrarenal structures in the dog. Using the chromaffin reaction to distinguish catecholaminergic fibres from other axon populations, it was found that the renal cortex of the dog is supplied only by catecholaminergic nerves. Immunostaining for tyrosine hydroxylase (TH) labelled all of the intracortical nerves, and 20% to 25% of these profiles also contained dopa decarboxylase (DDC)-immunoreactivity, indicating they were dopaminergic rather than noradrenergic. Both DDC-positive and DDC-negative axons were seen in close association (80 nm) with blood vessels and juxtaglomerular cells as well as tubular epithelial cells. The distribution of TH- and DDC-immunoreactive nerves in the renal cortex is compatible with existing functional evidence indicating that both dopaminergic and noradrenergic nerves are involved in the regulation of renal blood flow, tubular reabsorption and renin release.     

Enhancement of motor coordination by applying high frequency repetitive TMS on the sensory cortex

The sensory function plays an important role for successful motor performance. We investigated the modulating effects of high frequency repetitive transcranial magnetic stimulation (rTMS) on sensory discrimination and motor coordination. Twenty healthy participants were assigned into two random groups; the real- and sham-rTMS group. Total of 900 rTMS pulses at a frequency of 10 Hz (stimulus intensity of 90% RMT) were given over deltoid representational areas of the somatosensory cortex. Sensory discrimination ability was evaluated using two-point discrimination test. Motor coordination was measured by the latency difference between the synchronized contraction of deltoid and abductor pollicis brevis muscles before and after rTMS. The sensory discrimination was significantly increased only in the deltoid area and the difference in the latency of synchronized contraction of two muscles was significantly shortened after real-rTMS compared sham condition, which had tendency of negative correlation following real-rTMS condition. The results of this study demonstrated rTMS-induced enhancement of sensorimotor integration, which may contribute to develop effective therapeutic strategies for rehabilitation of various sensorimotor disorders in the clinical setting.     

Effect of damage to the parietal associative cortex on the function of acquired motor coordination in dogs

The effect of ablation of the parietal associative cortex on the performance of a complex food instrumental reaction was studied in dogs. The reaction consisted in two movements of the forelimb which were of similar pattern, but differed by their coordination. The first one was the lifting and holding of the paw at a required level for a required time, with the head in natural position (lifted), and the second one was the same movement of the paw with the head bent down for feeding, i.e. a new coordination, for the natural coordination consists in lowering of the forelimb associated with lowering of the head. During two sessions after the lesion, both reactions became irregular (so that the dogs performed only one of two movements or none). In the course of four months, the precision of the first movement was reduced, the amplitude of lifting the paw and duration of holding it were diminished. The new coordination persisted after ablation of the parietal associative cortex, though the holding (fixation) of the paw was less perfect. As was shown before by one of the present authors (M. E. Ioffe), lesion of the sensorimotor cortex resulted in profound disturbance of acquired coordination.