Abstract

Inhibitory propriospinal neurons with diffuse projections onto upper limb motoneurons have been revealed in humans using peripheral nerve stimulation. This system is supposed to mediate descending inhibition to motoneurons, to prevent unwilling muscle activity. However, the corticospinal control onto inhibitory propriospinal neurons has never been investigated so far in humans. We addressed the question whether inhibitory cervical propriospinal neurons receive corticospinal inputs from primary motor (M1) and ventral premotor areas (PMv) using spatial facilitation method. We have stimulated M1 or PMv using transcranial magnetic stimulation (TMS) and/or median nerve whose afferents are known to activate inhibitory propriospinal neurons. Potential input convergence was evaluated by studying the change in monosynaptic reflexes produced in wrist extensor electromyogram (EMG) after isolated and combined stimuli in 17 healthy subjects. Then, to determine whether PMv controlled propriospinal neurons directly or through PMv‐M1 interaction, we tested the connectivity between PMv and propriospinal neurons after a functional disruption of M1 produced by paired continuous theta burst stimulation (cTBS). TMS over M1 or PMv produced reflex inhibition significantly stronger on combined stimulations, compared to the algebraic sum of effects induced by isolated stimuli. The extra‐inhibition induced by PMv stimulation remained even after cTBS which depressed M1 excitability. The extra‐inhibition suggests the existence of input convergence between peripheral afferents and corticospinal inputs onto inhibitory propriospinal neurons. Our results support the existence of direct descending influence from M1 and PMv onto inhibitory propriospinal neurons in humans, possibly though direct corticospinal or via reticulospinal inputs.

Highlights

  • In humans, the C3–C4 propriospinal system constitutes a complex spinal circuitry, including excitatory interneurons with long intraspinal and diffuse projections to upper limb motoneurons

  • We found evidences for inhibitory propriospinal neurons in humans, as described in cats (Alstermark et al 1984a, b), but this inhibitory system has been investigated to a lesser extent than the excitatory one (Lourenßco et al 2007b; Marchand-Pauvert and Iglesias 2008)

  • In all the 6 subjects, the medianinduced motor evoked potential (MEP) inhibition was observed at interstimulus intervals (ISIs) 7 and 9 ms; in half, MEP inhibition was observed at ISIs 5 ms

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Summary

Introduction

The C3–C4 propriospinal system constitutes a complex spinal circuitry, including excitatory interneurons with long intraspinal and diffuse projections to upper limb motoneurons. The synaptic transmission through excitatory propriospinal neurons is modulated by feedback and feed-forward inhibitory interneurons, all receiving peripheral and descending inputs. This system can integrate sensory feedback and corticospinal inputs from the primary motor cortex (M1) to regulate the motor command en route to the motoneurons and to control the motoneuron activity according to movement conditions (Pierrot-Deseilligny and Burke 2012). This system has been shown to be involved in reachto-grasp and digit movements in primates and humans a 2017 The Authors. The corticospinal control onto the inhibitory propriospinal system has never been investigated in humans

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