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The Journal of Neuroscience, March 5, 2008, 28(10):2409-2425; doi:10.1523/JNEUROSCI.3229-07.2008

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Behavioral/Systems/Cognitive
Individual Premotor Drive Pulses, Not Time-Varying Synergies, Are the Units of Adjustment for Limb Trajectories Constructed in Spinal Cord

William J. Kargo^1,2 and Simon F. Giszter¹

¹Department of Neurobiology and Anatomy, Drexel University College of Medicine, Philadelphia, Pennsylvania 19129, and ²Neurocrine Biosciences Inc., San Diego, California 92130

Correspondence should be addressed to Simon F. Giszter, Neurobiology and Anatomy, Drexel University College of Medicine, 2900 Queen Lane, Philadelphia, PA 19129. Email: simon.giszter{at}drexel.edu

Complex actions may arise by combining simple motor primitives. Our studies support individual premotor drive pulses or bursts as execution primitives in spinal cord. Alternatively, the fundamental execution primitives at the segmental level could be time-varying synergies. To distinguish these hypotheses, we examined sensory feedback effects during targeted wiping organized in spinal cord. This behavior comprises three bursts. We tested (1) whether feedback altered the structure of individual premotor drive bursts or primitives, and (2) whether feedback differentially modulated different drive bursts or pulses in the three burst sequence. At least two of the three bursts would need to always be comodulated to support a time-varying synergy. We used selective muscle vibration to control spindle feedback from a single muscle (biceps/iliofibularis). The structures of premotor drive bursts were conserved. However, biceps vibration (1) scaled the amplitudes of two bursts coactivated during the initial phase of wiping independently of one another without altering their phase, and (2) independently phase regulated the third burst but preserved its amplitude. Thus, all three bursts were regulated separately. Durations were unaffected. The independent effects depended on (1) time of vibration during wiping, (2) frequency of vibration, and (3) limb configuration. Because each of the three bursts was independently modulated, these data strongly support execution using individual premotor bursts rather than time-varying synergies at the spinal level of motor organization. Our data show that both sensory feedback and central systems of the spinal cord act in concert to adjust the individual premotor bursts in support of the straight and unimodal wiping trajectory.

Key words: primitive; force-field; spinal cord; time-varying synergy; reflex; proprioceptive feedback; premotor

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Received April 10, 2007; revised Dec. 21, 2007; accepted Dec. 23, 2007.

Correspondence should be addressed to Simon F. Giszter, Neurobiology and Anatomy, Drexel University College of Medicine, 2900 Queen Lane, Philadelphia, PA 19129. Email: simon.giszter{at}drexel.edu

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