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The Journal of Neuroscience, March 3, 2004, 24(9):2122-2132; doi:10.1523/JNEUROSCI.4616-03.2004
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Behavioral/Systems/Cognitive
Corticospinal System Development Depends on Motor Experience
John H. Martin,1,3 Michelle Choy,1 Seth Pullman,2 andZhuo Meng1 1Center for Neurobiology and Behavior, Columbia University, 2Department of Neurology, Columbia University, and 3New York State Psychiatric Institute, New York, New York 10032
Early motor experiences have been shown to be important for the development of motor skills in humans and animals. However, little is known about the role of motor experience in motor system development. In this study, we address the question of whether early motor experience is important in shaping the development of the corticospinal (CS) tract. We prevented limb use by the intramuscular injection of botulinum toxin A into selected forelimb muscles to produce muscle paralysis during the period of development of CS connection specificity, which is between postnatal weeks 3 and 7. CS terminations were examined using an anterograde tracer. Preventing normal forelimb use during CS axon development produced defective development of CS terminations at week 8 and in maturity. There were reductions in the topographic distribution of axon terminals, in terminal and preterminal branching, and in varicosity density. This suggests that limb use is needed to refine CS terminals into topographically specific clusters of dense terminal branches and varicosities. To determine correlated effects on motor behavior, cats were tested in a prehension task, to reach and grasp a piece of food from a narrow food well, when the neuromuscular blockade dissipated (by week 10) and in maturity (week 16). Preventing normal limb use also produced a prehension deficit later in development and in maturity, in which there was a loss of the supination component of grasping. This component of prehension in the cat depends on CS projections from the paw representation of rostral motor cortex to the cervical enlargement. Our findings show that motor experiences are necessary for normal development of CS terminations and function.
Key words: motor cortex; corticospinal system; spinal cord; development; postnatal; cat; prehension; botulinum toxin A
Received Oct 13, 2003; revised January 5, 2004; accepted January 6, 2004.
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