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J Neurosci. 2017 Mar 8;37(10):2612-2626. doi: 10.1523/JNEUROSCI.2561-16.2017. Epub 2017 Feb 3.

Nerve-Specific Input Modulation to Spinal Neurons during a Motor Task in the Monkey.

Author information

1
Department of Neurophysiology, National Institute of Neuroscience, Tokyo 187-8502, Japan.
2
Department of Developmental Physiology, National Institute for Physiological Sciences, Okazaki 444-8585, Japan, and.
3
Department of Neurophysiology, National Institute of Neuroscience, Tokyo 187-8502, Japan, seki@ncnp.go.jp.
4
Precursory Research for Embryonic Science and Technology, Japan Science and Technology Agency, Saitama 332-0012, Japan.

Abstract

If not properly regulated, the large amount of reafferent sensory signals generated by our own movement could destabilize the CNS. We investigated how input from peripheral nerves to spinal cord is modulated during behavior. We chronically stimulated the deep radial nerve (DR; proprioceptive, wrist extensors), the median nerve (M; mixed, wrist flexors and palmar skin) and the superficial radial nerve (SR; cutaneous, hand dorsum) while four monkeys performed a delayed wrist flexion-extension task. Spinal neurons putatively receiving direct sensory input were defined based on their evoked response latency following nerve stimulation. We compared the influence of behavior on the evoked response (responsiveness to a specific peripheral input) and firing rate of 128 neuron-nerve pairs based on their source nerve. Firing rate increased during movement regardless of source nerve, whereas evoked response modulation was strikingly nerve-dependent. In SR (n = 47) and M (n = 27) neurons (cutaneous or mixed input), the evoked response was suppressed during wrist flexion and extension. In contrast, in DR neurons (n = 54, pure proprioceptive input), the evoked response was facilitated exclusively during movements corresponding to the contraction of DR spindle-bearing muscles (i.e., wrist extension). Furthermore, modulations of firing rate and evoked response were uncorrelated in SR and M neurons, whereas they tended to be positively comodulated in DR neurons. Our results suggest that proprioceptive and cutaneous inputs to the spinal cord are modulated differently during voluntary movements, suggesting a refined gating mechanism of sensory signals according to behavior.SIGNIFICANCE STATEMENT Voluntary movements produce copious sensory signals, which may overwhelm the CNS if not properly regulated. This regulation is called "gating" and occurs at several levels of the CNS. To evaluate the specificity of sensory gating, we investigated how different sources of somatosensory inputs to the spinal cord were modulated while monkeys performed wrist movements. We recorded activity from spinal neurons that putatively received direct connections from peripheral nerves while stimulating their source nerves, and measured the evoked responses. Whereas cutaneous inputs were suppressed regardless of the type of movement, muscular inputs were specifically facilitated during relevant movements. We conclude that, even at the spinal level, sensory gating is a refined and input-specific process.

KEYWORDS:

nerve stimulation; primates; sensory gating; somatosensory; spinal neurons; voluntary movement

PMID:
28159911
DOI:
10.1523/JNEUROSCI.2561-16.2017
[Indexed for MEDLINE]
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