Motor Cortex

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Motor Cortex

Nearly all adult behavior expresses an acquired motor skill. Because mammals have highly evolved motor regions of frontal cortex, including the primary motor cortex, they can acquire skilled motor behaviors involving a wide range of complex and adaptable movements. The remarkable adaptability of mammalian motor behavior suggests a high degree of functional flexibility in the motor cortex. There is now a large body of evidence demonstrating functional plasticity within the motor cortex and that this plasticity represents the neural encoding of motor skill.

Motor Map Plasticity

More than a century ago Fritsch and Hitzig (1870) found that electrical stimulation applied to regions of frontal cortex could evoke movement and Hitzig. The subsequent refinements of intracortical microstimulation (Asanuma and Ward, 1971) have identified two basic principles of organization within the motor cortex. The first is that movements corresponding to body parts over which there is a high degree of control, such as the hand, are multiply represented over a larger area of cortex than those of less dexterous body parts such as the foot. The second is that, although the general location of the map within the cortex is constant, the particular organization of movement representations is dynamic and can change in response to a variety of manipulations (Sanes and Donoghue, 2000).

These two principles of cortical organization also appear to govern the encoding of skilled movement within the motor cortex. Motor-skill training leads to a reorganization of movement representations that expands the representations corresponding to trained movements. For example, squirrel monkeys trained to retrieve a food pellet from successively smaller food wells exhibit an expansion of wrist and digit representations into elbow and shoulder representations (Nudo, Milliken, Jenkins, and Merzenich, 1996). Rats trained to reach outside their cages to retrieve a food pellet show a comparable expansion of wrist and digit representations (Kleim, Barbay, and Nudo, 1998). There is also evidence for a similar reorganization following motor-skill learning in human subjects (Pascuel-Leoni et al., 1995).

Although these experiments show the concurrence of skill learning and map reorganization, they do not reveal whether these changes result from learning or drive the development of skill. A recent experiment examining the motor maps of rats at different times during skilled forelimb training suggests that reorganization occurs after the acquisition of motor skill. Significant expansion of wrist and digit movements requires ten days of skilled reach, training whereas significant improvements in reaching accuracy occurs after three days (Kleim et al., 2000). This temporal discrepancy seems to show that functional reorganization requires sufficient performance of the skilled movements once they have been acquired. Rats trained for three days followed by ten days without training do not exhibit any significant change in the distribution of movement representations (Hogg et al., 2001). However, simple movement repetition alone is not sufficient to drive changes in the motor maps. In one experiment, squirrel monkeys were trained daily to retrieve pellets from a large food well that does not require the development of skilled wrist movements but does involve extensive wrist and digit use; there was no significant map reorganization despite thousands of movement repetitions (Plautz, Milliken, and Nudo, 2000). Similarly, rats housed with running wheels for a month show no significant change in the distribution of forelimb movement representations (Kleim et al., 2002). Thus, motor map reorganization is dependent upon the acquisition and subsequent performance of novel skilled movements but does not occur in response to repetition of existing movements.

Neural Substrates of Motor Map Plasticity

In the microcircuitry of the motor cortex there are extensive recurrent axon collaterals that span several millimeters across the cortex (Huntley and Jones, 1991; Keller, 1993). Intracortical stimulation evokes movement by activating these horizontal afferents (Jankowska, Padel, and Tanaka, 1975). Hence changes in intracortical connectivity might mediate changes in the organization of movement representations. Several experiments have supported this hypothesis by demonstrating activity-dependent changes in synaptic efficacy within the horizontal connections of the motor cortex via differential patterns of electrical stimulation. Long-term potentiation (LTP) of synaptic responses occurs in response to high frequency stimulation (Hess and Donoghue, 1994), whereas lower frequency stimulation leads to long-term depression (LTD) of these same synapses (Hess and Donoghue, 1996). Although these changes are induced through artificial patterns of cortical stimulation, they demonstrate that the horizontal connections within the motor cortex are modifiable in response to differential motor experience.

More direct evidence for the role of horizontal afferent plasticity in motor learning has come from experiments showing that synaptic potentials following stimulation of intracortical afferents were significantly greater in the trained than in the untrained hemisphere (Rioult-Pedotti, Friedman, Hess, and Donoghue, 1998). Further, relative to the untrained hemisphere, LTP was reduced and LTD was enhanced in the trained hemisphere (Rioult-Pedotti, Friedman, Hess, and Donoghue, 2000). These results demonstrate that motor learning increases intracortical synaptic efficacy while maintaining the range within which synapses can be modified.

Changes in the efficacy of intracortical afferents may have an anatomical basis. Huntley (1997) has shown that the pattern of intracortical connections correlates with the functional reorganization that follows peripheral nerve lesions. Further, motor-skill training paradigms that induce motor map changes also cause changes in the morphology of cortical neurons. For example, cortical pyramidal neurons of rats trained on a skilled reaching task have a significantly increased dendritic arbor within the trained versus untrained motor cortex (Withers and Greenough, 1989; Greenough, Larson, and Withers, 1985). Further, rats trained daily to traverse a complex set of obstacles have significantly more synapses per neuron within the motor cortex than rats forced to run a flat, obstacle-free runway (Kleim, Lussnig, Schwarz, and Greenough, 1996). Finally, Kleim et al. (2002b) have shown that increases in synapse number within the rat motor cortex following skilled reach training is confined to those areas of cortex that also underwent reorganization of movement representations.

All of these data suggest that the development of skilled movement is encoded within the motor cortex through changes in the strength of intracortical afferents that may involve increases in synapse numbers. These adaptations of cortical circuitry then show up as changes in the distribution of cortical-movement representations. The coordinated anatomical and physiological plasticity thus represents a neural mechanism by which motor memories (engrams) are represented within the brain.



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Jeffrey A.Kleim