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Peter L Strick

Publications and source records attributed to Peter L Strick.

18 recordsLinked to original sources
PubMed2006

Skill representation in the primary motor cortex after long-term practice.

The acquisition of motor skills can lead to profound changes in the functional organization of the primary motor cortex (M1). For example, performance of movement sequences after prolonged practice is associated with an expansion of the effector representation in M1. Paradoxically, there is little evidence that the activity of M1 neurons reflects acquired skills, especially sequences of movements. We examined the activity of M1 neurons during skilled movement sequences in macaques trained to successively hit targets on a monitor. The targets appeared either pseudorandomly (Random mode) or in one of two repeating sequences (Repeating mode). With practice, response times for repeating sequences substantially declined and the monkeys performed the task predictively. Highly trained animals retained the acquired skill after long gaps in practice. After >2 yr of training, 40% of M1 neurons were differentially active during the two task modes. Variations in movement kinematics did not fully explain the task-dependent modulation of neuron activity. Differentially active neurons were more strongly influenced by task mode than by kinematics. Our results suggest that practice sculpts the response properties of M1 neurons. M1 may be a site of storage for the internal representation of skilled sequential movements.

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PubMed2006

Rapid and long-lasting plasticity of input-output mapping.

Skilled use of tools requires us to learn an "input-output map" for the device, i.e., how our movements relate to the actions of the device. We used the paradigm of visuo-motor rotation to examine two questions about the plasticity of input-output maps: 1) does extensive practice on one mapping make it difficult to modify and/or to form a new input-output map and 2) once a map has been modified or a new map has been formed, does this map survive a gap in performance? Humans and monkeys made wrist movements to control the position of a cursor on a computer monitor. Humans practiced the task for approximately 1.5 h; monkeys practiced for 3-9 yr. After this practice, we gradually altered the direction of cursor movement relative to wrist movement while subjects moved either to a single target or to four targets. Subjects were unaware of the change in cursor-movement relationship. Despite their prior practice on the task, the humans and the monkeys quickly adjusted their motor output to compensate for the visuo-motor rotation. Monkeys retained the modified input-output map during a 2-wk gap in motor performance. Humans retained the altered map during a gap of >1 yr. Our results show that sensorimotor performance remains flexible despite considerable practice on a specific task, and even relatively short-term exposure to a new input-output mapping leads to a long-lasting change in motor performance.

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PubMed2006

Muscle representation in the macaque motor cortex: an anatomical perspective.

How are the neurons that directly influence the motoneurons of a muscle distributed in the primary motor cortex (M1)? To answer this classical question we used retrograde transneuronal transport of rabies virus from single muscles of macaques. This enabled us to define cortico-motoneuronal (CM) cells that make monosynaptic connections with the motoneurons of the injected muscle. We examined the distribution of CM cells that project to motoneurons of three thumb and finger muscles. We found that the CM cells for these digit muscles are restricted to the caudal portion of M1, which is buried in the central sulcus. Within this region of M1, CM cells for one muscle display a remarkably widespread distribution and fill the entire mediolateral extent of the arm area. In fact, CM cells for digit muscles are found in regions of M1 that are known to contain the shoulder representation. The cortical territories occupied by CM cells for different muscles overlap extensively. Thus, we found no evidence for a focal representation of single muscles in M1. Instead, the overlap and intermingling among the different populations of CM cells may be the neural substrate to create a wide variety of muscle synergies. We found two additional surprising results. First, 15-16% of the CM cells originate from area 3a, a region of primary somatosensory cortex. Second, the size range of CM cells includes both "fast" and "slow" pyramidal tract neurons. These observations are likely to lead to dramatic changes in views about the function of the CM system.

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PubMed2005

The cerebellum communicates with the basal ganglia.

The cerebral cortex is interconnected with two major subcortical structures: the basal ganglia and the cerebellum. How and where cerebellar circuits interact with basal ganglia circuits has been a longstanding question. Using transneuronal transport of rabies virus in macaques, we found that a disynaptic pathway links an output stage of cerebellar processing, the dentate nucleus, with an input stage of basal ganglia processing, the striatum.

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PubMed2005

Frontal lobe inputs to the digit representations of the motor areas on the lateral surface of the hemisphere.

We examined the frontal lobe connections of the digit representations in the primary motor cortex (M1), the dorsal premotor area (PMd), and the ventral premotor area (PMv) of cebus monkeys. All of these digit representations lie on the lateral surface of the hemisphere. We used intracortical stimulation to identify the digit representations physiologically, and then we injected different tracers into two of the three cortical areas. This approach enabled us to compare the inputs to two digit representations in the same animal. We found that the densest inputs from the premotor areas to the digit representation in M1 originate from the PMd and the PMv. Both of these premotor areas contain a distinct digit representation, and the two digit representations are densely interconnected. Surprisingly, the projections from the digit representation in the supplementary motor area (SMA) to the PMd and PMv are stronger than the SMA projections to M1. The projections from other premotor areas to M1, the PMd, and the PMv are more modest. Of the three digit areas on the lateral surface, only the PMv receives dense input from the prefrontal cortex. Based on these results, we believe that M1, the PMd, and the PMv form a densely interconnected network of cortical areas that is concerned with the generation and control of hand movements. Overall, the laminar origins of neurons that interconnect the three cortical areas are typical of "lateral" interactions. Thus, from an anatomical perspective, this cortical network lacks a clear hierarchical organization.

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PubMed2004

Basal ganglia and cerebellar inputs to 'AIP'.

The anterior intraparietal area (AIP) is a subregion of area 7b in posterior parietal cortex. AIP neurons respond to the sight of objects, as well as to the act of grasping them. We used retrograde transneuronal transport of rabies virus to examine subcortical inputs to AIP in the monkey. Virus transport labeled substantial numbers of neurons in the substantia nigra pars reticulata (SNpr), as well as in the dentate nucleus of the cerebellum. The hotspots of labeled neurons in SNpr and in dentate after AIP injections were separate from those created by virus injections into several other parietal or frontal regions. These observations provide the first evidence that a major output nucleus of the basal ganglia, the SNpr, projects to a region of posterior parietal cortex. In addition, our findings provide further support for the concept that posterior parietal cortex is a target of cerebellar output.

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PubMed2004

Deficits in movements of the wrist ipsilateral to a stroke in hemiparetic subjects.

We examined step-tracking movements of the wrist and associated EMG activity in seven patients (age range, 27-73 yr) and in seven normal subjects that were matched to patients in age, sex, and handedness. All patients exhibited a hemiparesis that resulted from a unilateral cerebrovascular accident (CVA) that included motor areas in the frontal lobe or their efferents. The lesion in three patients was in their dominant hemisphere. The patients were tested 1-48 mo following their CVA. They had great difficulty in performing or were unable to perform step-tracking movements with the contralesional wrist. In addition, the patients displayed striking deficits in wrist movements and muscle activity of the ipsilesional wrist. These movements were >50% slower than those of controls. The initial movement step routinely undershot the target and was only 63% as large as that of controls. The patients made wrist movements with marked directional errors requiring corrective responses. These errors were due largely to inappropriate temporal sequencing of muscle activity. The deficits in movement and muscle activity in the wrist ipsilesional to a CVA were marked, regardless of whether the lesion was in the dominant or nondominant hemisphere. These observations indicate that unilateral lesions can have significant bilateral effects on the generation and control of distal limb movements.

Adult↗
PubMed2004

Macro-architecture of basal ganglia loops with the cerebral cortex: use of rabies virus to reveal multisynaptic circuits.

We have used retrograde transneuronal transport of rabies virus to examine basal ganglia connections with the cerebral cortex. We injected rabies into the primary motor cortex (M1) or into Area 46 of cebus monkeys. A 4-day survival time was long enough to allow transport of rabies from the injection site to 'third-order' neurons in the basal ganglia. After either M1 or Area 46 injections, third-order neurons were found in the external segment of the globus pallidus (GPe), striatum and subthalamic nucleus (STN). In each of these nuclei, the third-order neurons that innervate M1 were spatially separated from those that innervate Area 46. Thus, distinct basal ganglia-thalamocortical circuits innervate M1 and Area 46. Next, we injected a conventional tracer into M1 to define its terminations in the putamen and STN. We found that the regions of the putamen and STN that receive input from M1 are the same as those that contain third-order neurons after M1 injections of virus. On the other hand, virus injections into M1 also labeled a relatively dense group of third-order neurons in a region of the ventral putamen that is not innervated by M1. This region of the putamen is the target of efferents from the amygdala. Thus, the ventral putamen may provide a route for the limbic system to influence motor output. Overall, our results indicate that basal ganglia circuits with the cerebral cortex can be characterized by both open- and closed-loop macro-architectures.

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PubMed2003

Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate.

We used transneuronal transport of neurotropic viruses to examine the topographic organization of circuits linking the cerebellar cortex with the arm area of the primary motor cortex (M1) and with area 46 in dorsolateral prefrontal cortex of monkeys. Retrograde transneuronal transport of the CVS-11 (challenge virus strain 11) strain of rabies virus in cerebello-thalamocortical pathways revealed that the arm area of M1 receives input from Purkinje cells located primarily in lobules IV-VI of the cerebellar cortex. In contrast, transneuronal transport of rabies from area 46 revealed that it receives input from Purkinje cells located primarily in Crus II of the ansiform lobule. Thus, both M1 and area 46 are the targets of output from the cerebellar cortex. However, the output to each area of the cerebral cortex originates from Purkinje cells in different regions of the cerebellar cortex. Anterograde transneuronal transport of the H129 strain of herpes simplex virus type 1 (HSV1) revealed that neurons in the arm area of M1 project via the pons to granule cells primarily in lobules IV-VI, whereas neurons in area 46 project to granule cells primarily in Crus II. Together, the findings from rabies and HSV1 experiments indicate that the regions of the cerebellar cortex that receive input from M1 are the same as those that project to M1. Similarly, the regions of the cerebellar cortex that receive input from area 46 are the same as those that project to area 46. Thus, our observations suggest that multiple closed-loop circuits represent a fundamental architectural feature of cerebrocerebellar interactions.

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PubMed2003

Sensorimotor transformations in cortical motor areas.

A central problem in motor research has been to understand how sensory signals are transformed to generate a goal-directed movement. This problem has been formulated as a set of coordinate transformations that begins with an extrinsic coordinate frame representing the spatial location of a target and ends with an intrinsic coordinate frame describing muscle activation patterns. Insight into this process of sensorimotor transformation can be gained by examining the coordinate frames of neuronal activity in interconnected regions of the brain. We recorded the activity of neurons in primary motor cortex (M1) and ventral premotor cortex (PMv) in a monkey trained to perform a task which dissociates three major coordinate frames of wrist movement: muscle, wrist joint, and an extrinsic coordinate frame. We found three major types of neurons in M1 and PMv. The first type was termed 'extrinsic-like'. The activity of these neurons appeared to encode the direction of movement in space independent of the patterns of wrist muscle activity or joint movement that produced the movements. The second type was termed 'extrinsic-like with gain modulation'. The activity of these neurons appeared to encode the direction of movement in space, but the magnitude (gain) of neuronal activity depended on the posture of the forearm. The third type was termed 'muscle-like' since their activity co-varied with muscle activity. The great majority of the directionally-tuned neurons in the PMv were classified as 'extrinsic-like' (48/59, 81%). A smaller group was classified as 'extrinsic-like with gain modulation' (7/59, 12%). In M1, the three types of neurons were more equally represented. Our results raise the possibility that cortical processing between M1 and PMv may contribute to a sensorimotor transformation between extrinsic and intrinsic coordinate frames. Recent modeling studies have demonstrated the computational plausibility of such a process.

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PubMed2003

Activation of the supplementary motor area (SMA) during performance of visually guided movements.

The supplementary motor area (SMA) has long been thought to have a special role in the internal generation of complex movements. Yet, a number of recent functional imaging studies indicate that the SMA is activated during the execution of simple movements guided by sensory cues. The extent of participation of the cingulate motor areas in visually guided movements also is unclear. To explore these issues we used the 2-deoxyglucose (2DG) technique to measure functional activation in the motor areas on the medial wall of the hemisphere in monkeys trained to perform visually guided reaching movements to randomly presented targets. This approach enabled us to make precise comparisons between sites of activation and the location of specific premotor areas on the medial wall of the hemisphere. We found that the SMA was strongly activated during reaching to different visual targets. Indeed, its activation was comparable to that of the primary motor cortex (M1). In contrast, none of the cingulate motor areas displayed significantly increased activation specifically related to arm movements. Our results provide further support for the involvement of the SMA in visually guided movements. Furthermore, our observations suggest that during externally guided reaching, SMA activation is tightly coupled to that of M1, but dissociated from that of the cingulate motor areas.

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PubMed2003

An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex.

We have used retrograde transneuronal transport of neurotropic viruses to examine the organization of the projections from the dentate nucleus of the cerebellum to "motor" and "nonmotor" areas of the cerebral cortex. To perform this analysis we created an unfolded map of the dentate. Plotting the results from current and prior experiments on this unfolded map revealed important features about the topography of function in the dentate. We found that the projections to the primary motor and premotor areas of the cerebral cortex originated from dorsal portions of the dentate. In contrast, projections to prefrontal and posterior parietal areas of cortex originated from ventral portions of the dentate. Thus the dentate contains anatomically separate and functionally distinct motor and nonmotor domains.

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PubMed2002

Motor areas in the frontal lobe of the primate.

There has been a substantial change in our concepts about the cortical motor areas. It is now clear that the frontal lobe of primates contains at least six premotor areas that project directly to the primary motor cortex (M1). Two premotor areas, the ventral premotor area (PMv) and the dorsal premotor area (PMd), are located on the lateral surface of the hemisphere. Four premotor areas are located on the medial wall of the hemisphere and include the supplementary motor area (SMA) and three cingulate motor areas. Each of these premotor areas has substantial direct projections to the spinal cord. Corticospinal axons from the premotor areas terminate in the intermediate zone of the spinal cord, and some also terminate in the ventral horn around motoneurons. In this respect, the premotor areas are like M1 and appear to have direct connections with spinal motoneurons, particularly those innervating hand muscles. Furthermore, it is possible to evoke movements of the distal and proximal forelimb using intracortical stimulation at relatively low currents in the premotor areas. Thus, the premotor areas appear to have the potential to influence the control of movement not only at the level of M1, but also more directly at the level of the spinal cord. For these reasons, we have suggested that the premotor areas may operate at a hierarchical level comparable to M1. We propose that each premotor area is a functionally distinct efferent system that differentially generates and/or controls specific aspects of motor behavior.

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PubMed2002

Basal-ganglia 'projections' to the prefrontal cortex of the primate.

We used retrograde transneuronal transport of the McIntyre-B strain of herpes simplex virus type 1 to examine the extent and organization of basal-ganglia-thalamocortical projections to five regions of prefrontal cortex in the cebus monkey (Cebus apella): medial and lateral area 9 (9m and 9l), dorsal and ventral area 46 (46d and 46v) and lateral area 12 (12l). All of these prefrontal areas were found to be targets of basal-ganglia output that originated in the internal segment of the globus pallidus (GPi) and/or the pars reticulata of the substantia nigra (SNpr). Approximately one-third of the total volume of these nuclei was directed toward prefrontal cortex, a volume comparable to that directed at the cortical motor areas. The origins of the outputs to different prefrontal areas were topographically organized. Different portions of SNpr (the rostral and caudal thirds) projected to areas 9m and 12l. Similarly, different output nuclei (GPi and SNpr) projected to adjacent portions of the same cytoarchitectonic field (46d and 46v). Furthermore, the outputs to prefrontal areas were segregated from those to motor areas of cortex. Thus, basal-ganglia outputs to prefrontal cortex are both extensive and topographically organized, forming a rich anatomical substrate for basal-ganglia influences on the cognitive operations of the frontal lobe.

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PubMed2002

Motor and nonmotor domains in the monkey dentate.

Our concepts about the organization and functions of the cerebellum have changed substantially in the last 10 years. In recent studies, we used transneuronal virus tracing techniques to demonstrate that the output of the cerebellum of primates projects via the thalamus not only to its classical motor target, the primary motor cortex, but also to "nonmotor" cortical areas in the prefrontal and posterior parietal cortex. We found that dentate neurons projecting to different cortical areas originated from localized regions of the nucleus which we termed "output channels." To compare the locations of the output channels projecting to different cortical targets, we have created an unfolded map of the dentate. This unfolded map revealed that dentate output channels were segregated into spatially separate "motor" and "nonmotor" domains. The output channels in the motor domain exclusively targeted primary motor and premotor areas of the cerebral cortex. These channels were localized in the dorsal portion of the dentate. The output channels in the nonmotor domain projected to prefrontal and posterior parietal cortical areas. The nonmotor domain was confined to the ventral portion of the dentate. In recent studies, we defined a unique molecular marker, monoclonal antibody 8B3, which appears to differentially "recognize" these two domains. Taken together, our results suggest that dentate output is organized according to the functional capabilities of its cortical targets. This organization provides the dentate nucleus with the anatomical substrate to influence not only the control of movement, but also cognitive, higher-order executive and visuospatial functions.

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