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Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement

Abstract

During normal voluntary movements, re-afferent sensory input continuously converges on the spinal circuits that are activated by descending motor commands. This time-varying input must either be synergistically combined with the motor commands or be appropriately suppressed to minimize interference. The earliest suppression could be produced by presynaptic inhibition, which effectively reduces synaptic transmission at the initial synapse. Here we report evidence from awake, behaving monkeys that presynaptic inhibition decreases the ability of afferent impulses to affect postsynaptic neurons in a behaviorally dependent manner. Evidence indicates that cutaneous afferent input to spinal cord interneurons is inhibited presynaptically during active wrist movement, and this inhibition is effectively produced by descending commands. Our results further suggest that this presynaptic inhibition has appropriate functional consequences for movement generation and may underlie increases in perceptual thresholds during active movement.

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Figure 1: Experimental design
Figure 2: Suppression of SR-evoked response in a first-order interneuron.
Figure 3: Summary of response modulation and firing rates for all first-order interneurons.
Figure 4: Suppression of SR-evoked response before EMG onset.
Figure 5: Suppression of SR-evoked response before ENG onset.
Figure 6: Excitability testing of SR afferents.
Figure 7: Suppression of muscle activity evoked from site of interneuron recording.

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Acknowledgements

We thank J. Garlid, S. Gilbert, L. Shupe and S. Votaw for technical assistance. This work was supported by National Institutes of Health grants NS 12542, NS36781 and RR00166, and Human Frontiers Science Program grant LT0070/1999-B.

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Correspondence to Kazuhiko Seki.

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Seki, K., Perlmutter, S. & Fetz, E. Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement. Nat Neurosci 6, 1309–1316 (2003). https://doi.org/10.1038/nn1154

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