Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning.

Current evidence indicates that repetitive motor behavior during motor learning paradigms can produce changes in representational organization in motor cortex. In a previous study, we trained adult squirrel monkeys on a repetitive motor task that required the retrieval of food pellets from a small-diameter well. It was found that training produced consistent task-related changes in movement representations in primary motor cortex (M1) in conjunction with the acquisition of a new motor skill. In the present study, we trained adult squirrel monkeys on a similar motor task that required pellet retrievals from a much larger diameter well. This large-well retrieval task was designed to produce repetitive use of a limited set of distal forelimb movements in the absence of motor skill acquisition. Motor activity levels, estimated by the total number of finger flexions performed during training, were matched between the two training groups. This experiment was intended to evaluate whether simple, repetitive motor activity alone is sufficient to produce representational plasticity in cortical motor maps. Detailed analysis of the motor behavior of the monkeys indicates that their retrieval behavior was highly successful and stereotypical throughout the training period, suggesting that no new motor skills were learned during the performance of the large-well retrieval task. Comparisons between pretraining and posttraining maps of M1 movement representations revealed no task-related changes in the cortical area devoted to individual distal forelimb movement representations. We conclude that repetitive motor activity alone does not produce functional reorganization of cortical maps. Instead, we propose that motor skill acquisition, or motor learning, is a prerequisite factor in driving representational plasticity in M1.

Somatosensory and motor representations in cerebral cortex of a primitive mammal (Monodelphis domestica): a window into the early evolution of sensorimotor cortex.

To examine the potential early stages in the evolution of sensorimotor cortex, electrophysiological studies were conducted in the primitive South American marsupial opossum, Monodelphis domestica. Somatosensory maps derived from multiunit microelectrode recordings revealed a complete somatosensory representation of the contralateral body surface within a large region of midrostral cortex (primary somatosensory cortex, or S1). A large proportion ( approximately 51%) of S1 was devoted to representation of the glaborous snout, mystacial vibrissae, lower jaw, and oral cavity (the rostrum). A second representation, the second somatosensory area (or S2), was found adjacent and caudolateral to S1 as a mirror image reversed along the representation of the glabrous snout. A reversal of somatotopic order and an enlargement of receptive fields marked the transition from S1 to S2. Mapping of excitable cortex was conducted by using intracortical microstimulation (ICMS) techniques, as well as low-impedance depth stimulation and bipolar surface stimulation. In all three procedures, electrical stimulation resulted in movements confined strictly to the face. Specifically, at virtually all sites from which movements could be evoked, stimulation resulted in only vibrissae movement. ICMS-evoked vibrissae movements typically occurred at sites within S1 with receptive fields of the mystacial vibrissae, lower jaw, and glaborous snout. Results were similar using low-impedance depth stimulation and bipolar surface stimulation techniques except that the motor response maps were generally larger in area. There was no evidence of a motor representation rostral to S1. Examination of the cytoarchitecture in this cortical region (reminiscent of typical mammalian somatosensory cortex) and the high levels of stimulation needed for vibrissae movement suggest that the parietal neocortex of Monodelphis is representative of a primitive sensorimotor condition. It possesses a complete S1 representation with an incomplete motor component overlapping the S1 representation of the face. It contains no primary motor representation. Completion of the motor representations within S1 (trunk, limbs, tail) as well as the emergence of a primary motor cortex rostral to S1 may have occurred relatively late in mammalian phylogeny.

Sources of movement-related cortical potentials derived from foot, finger, and mouth movements.

Movement-related cortical potentials (MRCPs) register brain electrical activity before and during movement execution. In an attempt to delineate the components of MRCPs that reflect common sources to various movements and that are movement-specific, simple self-paced voluntary foot, finger, and mouth movements were studied. MRCPs were recorded in eight healthy volunteers with 30 electrodes placed on the scalp. Data were analyzed using Brain Electric Source Analysis software, and multiple equivalent dipole models were developed to separate spatial and temporal aspects of brain activity related to the execution of voluntary movements. Independent models were separately developed for the grand average data and for the individual subjects' data for each movement type. MRCPs derived from foot movements were accounted for using a 5-dipole model, finger movements using an 8-dipole model, and mouth movements with a 7-dipole model, yielding the grand average residual variances of 3%, 2%, and 6%, respectively. Based on individual models, intersubject variability of dipole locations was less than 10 mm (+/- SD). Overlaying the mean dipole coordinates onto the stereotaxic atlas provided proof that the sensorimotor cortical areas, supplementary motor area, and also cerebellum and thalamus were active in all three movements. Locations of the dipoles in the contralateral sensorimotor area clearly implied well-known medial to lateral somatotopic organization of foot, finger, and mouth movements. Temporal separation of the activity spread over different brain areas was demonstrated by evolution in the moments of dipole source potentials. The authors' models support the view of simultaneous activation of the primary motor cortex and supplementary motor area at the time of movement execution. Multiple equivalent dipole models developed in this study implied the activity originating in corresponding brain areas as previously detected by positron emission tomography or functional magnetic resonance imaging. However, MRCPs provided additional information regarding the temporal evolution of the brain activity related to the execution of voluntary movements. Thus, the concurrent use of MRCPs and other imaging techniques may provide complementary information not easily obtained by the other imaging techniques themselves.

Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct.

Substantial functional reorganization takes place in the motor cortex of adult primates after a focal ischemic infarct, as might occur in stroke. A subtotal lesion confined to a small portion of the representation of one hand was previously shown to result in a further loss of hand territory in the adjacent, undamaged cortex of adult squirrel monkeys. In the present study, retraining of skilled hand use after similar infarcts resulted in prevention of the loss of hand territory adjacent to the infarct. In some instances, the hand representations expanded into regions formerly occupied by representations of the elbow and shoulder. Functional reorganization in the undamaged motor cortex was accompanied by behavioral recovery of skilled hand function. These results suggest that, after local damage to the motor cortex, rehabilitative training can shape subsequent reorganization in the adjacent intact cortex, and that the undamaged motor cortex may play an important role in motor recovery.

Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys.

1. Intracortical microstimulation (ICMS) techniques were used to derive detailed maps of distal forelimb movement representations in primary motor cortex (area 4) of adult squirrel monkeys before and a few months after a focal ischemic infarct. 2. Infarcts caused a marked but transient deficit in use of the contralateral hand, as evidenced by increased use of the ipsilateral hand, and reduced performance on a task requiring skilled digit use. 3. Infarcts resulted in a widespread reduction in the areal extent of digit representations adjacent to the lesion, and apparent increases in adjacent proximal representations. 4. We conclude that substantial functional reorganization occurs in primary motor cortex of adult primates following a focal ischemic infarct, but at least in the absence of postinfarct training, the movements formerly represented in the infarcted zone do not reappear in adjacent cortical regions.

Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys.

This study was undertaken to document plastic changes in the functional topography of primary motor cortex (M1) that are generated in motor skill learning in the normal, intact primate. Intracortical microstimulation mapping techniques were used to derive detailed maps of the representation of movements in the distal forelimb zone of M1 of squirrel monkeys, before and after behavioral training on two different tasks that differentially encouraged specific sets of forelimb movements. After training on a small-object retrieval task, which required skilled use of the digits, their evoked-movement digit representations expanded, whereas their evoked-movement wrist/forearm representational zones contracted. These changes were progressive and reversible. In a second motor skill exercise, a monkey pronated and supinated the forearm in a key (eyebolt)-turning task. In this case, the representation of the forearm expanded, whereas the digit representational zones contracted. These results show that M1 is alterable by use throughout the life of an animal. These studies also revealed that after digit training there was an areal expansion of dual-response representations, that is, cortical sectors over which stimulation produced movements about two or more joints. Movement combinations that were used more frequently after training were selectively magnified in their cortical representations. This close correspondence between changes in behavioral performance and electrophysiologically defined motor representations indicates that a neurophysiological correlate of a motor skill resides in M1 for at least several days after acquisition. The finding that cocontracting muscles in the behavior come to be represented together in the cortex argues that, as in sensory cortices, temporal correlations drive emergent changes in distributed motor cortex representations.

Analysis of lateralized components of feeding behavior in the ring-tailed lemur (Lemur catta).

Twenty-one ring-tailed lemurs (Lemur catta) were videotaped during feeding. They had previously been classified as left-, right- or ambipreferent on the basis of the hand used to reach for food. The feeding sequences provided duration-based measures of manipulation, hand and mouth lateralization, and posture during feeding sequences with 2 types of food. Hand preference for reaching and holding was stable over time and across measurement conditions. As a group, the lemurs grasped fruit bimanually more often than chow; however, right- and ambipreferent lemurs spent more time holding food bimanually than did left-preferent ones. Older animals consumed chow more quickly than did younger animals but did not differ in their rate of manipulation. Lemurs had a preference for using one side of the mouth in feeding, but this had no directional relation to preferred hand. Three postural feeding patterns were identified.

Preliminary observations on hand preference for tapping, digit-feeding and food-holding in captive aye-ayes (Daubentonia madagascariensis).

Aye-ayes possess highly adapted hands, using their specialized third digits to investigate potential food sources by tapping and the third or fourth digits to transfer food to the mouth. Observations were conducted on 11 captive aye-ayes (10 wild-caught; 1 captive-bred) following presentation of food or novel objects, and hand use for holding, tapping and digit-feeding was scored. Eight of the individuals showed significant hand preferences for one or more of the 3 measures, although there was no consistent pattern. These preliminary results are compared to those from other lemur species.

Analyses of feeding lateralization in the small-eared bushbaby (Otolemur garnettii): a comparison with the ring-tailed lemur (Lemur catta).

Feeding related lateralization was examined in a population of 23 small-eared bushbabies (Otolemur garnettii). The three measures used to determine lateralization were food reaching, holding, and manipulation. Sex and age differences were found, with adult females showing a strong right bias and adult males a left bias. Juvenile males were weakly lateralized and less consistent across measures than adult animals. The use of standard scores to assess lateralization allowed species comparisons to be made. The results of this study were compared with results from a previous study on lateralization in the ring-tailed lemur (Lemur catta). Species comparisons found sex differences to be a stronger factor in lateralization than species differences.

Handedness as a function of sex and age in a large population of Lemur.

A population of 194 lemurs (Lemur spp.), 116 males and 78 females, from 1 to 30 years of age, was assessed for lateralized hand use in simple food reaching with a minimum of 100 reaches per animal. A hand preference was present in 80% of the population with a bias for use of the left hand that was most characteristic of male lemurs and young lemurs. The results confirm the presence of lateralization in prosimians, and we interpret the sex and age differences in relation to current theories of neural lateralization.

Multiple measures of hand-use lateralization in the ring-tailed lemur (Lemur catta).

Evaluated a free-ranging matriline of 13 ring-tailed lemurs (Lemur catta) from videotaped records for lateralized hand use with 2 tasks and 4 measures: food reaching, feeding posture, duration of food holding, and manipulation of food between mouth and hand while eating. Binomial z scores determined 7 lemurs to be left preferent in reaching, 3 right, and 3 ambipreferent. Ideographic analyses suggested possible sex-linked and early experience twin effects. When compared to right and ambipreferent lemurs, left reach preferent lemurs used the left hand more but bimanuals grasped less in food holding and also engaged in less hand-mouth food manipulation. The tendency to manipulate food was not correlated with bimanual holding but was inversely related to left hand holding and directly related to right hand holding. These patterns are discussed as possible precursors of human bimanual manipulation.

Posturally related variations in the hand preferences of the ruffed lemur (Varecia variegata variegata).

The hand preferences of 5 semi-free-ranging black-and-white ruffed lemurs were assessed by using three distinct testing procedures. Testing conditions varied in the extent to which they required animals to make a whole body postural adjustment prior to making a reach. Minimal bodily adjustment was necessary for free foraging, whereas discrete food presentations on land (DFP-land) and in a moat (DFP-moat) promoted a gross reorientation of the animal's entire body. In the DFP-moat condition 4 animals exhibited exclusive use of the left hand, and only 1 of 515 reaches was made with the right hand. Similarly, all 5 animals showed a pronounced left hand preference in the DFP-land condition. The free-foraging condition revealed a hand preference for only 1 of the 5 subjects, and that preference was weak in comparison with those measured in the other two test conditions. These findings indicate that whole body postural adjustments critically influenced the expression of hand preference and should be taken into consideration in future studies of primate hand preferences.