Corticospinal control from M1 and PMv areas on inhibitory cervical propriospinal neurons in humans

• Published in: Physiological reports 2017-11, Vol.5 (20), p.e13387-n/a
• Main Authors: Giboin, Louis‐Solal, Sangari, Sina, Lackmy‐Vallée, Alexandra, Messé, Arnaud, Pradat‐Diehl, Pascale, Marchand‐Pauvert, Véronique
• Format: Article
• Language: English
• Subjects: Achievement tests; Adult; Beta Rhythm; Central Nervous System; Convergence; Corticospinal tract; Electromyography; Evoked Potentials, Motor; Excitability; Female; Humans; Life Sciences; Magnetic fields; Male; Median nerve; Motor Control; Motor cortex; Motor Cortex - cytology; Motor Cortex - physiology; Motor neurons; Neural Circuits and Systems; Neural Inhibition; Neural networks; Neurobiology; Neurons; Neurons - physiology; Neurons and Cognition; Original Research; Physiology; Premotor cortex; Proprioception; Propriospinal neurons; Pyramidal tracts; Pyramidal Tracts - cytology; Pyramidal Tracts - physiology; Reflex; Reflexes; TMS; Transcranial Magnetic Stimulation; Wrist
• ISSN: 2051-817X; 2051-817X
• DOI: 10.14814/phy2.13387

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. In humans, inhibitory cervical propriospinal neurons have diffuse projections on upper limb motoneurons and may be good candidates to transmit diffuse descending inhibition to prevent unwilling muscle activity. Propriospinal inhibition was enhanced when peripheral nerve stimuli were combined to TMS over M1 or PMv, and inhibition from PMv was unchanged after a reversible functional disruption of M1. M1 and PMv can depress the excitability of spinal motoneurons and avoid muscle activity through inhibitory cervical propriospinal neurons.