Long-latency Responses to a Mechanical Perturbation of the Index Finger Have a Spinal Component

Abstract

In an uncertain external environment, the motor system may need to respond rapidly to an unexpected stimulus. Limb displacement causes muscle stretch; the corrective response has multiple activity bursts, which are suggested to originate from different parts of the neuraxis. The earliest response is so fast, it can only be produced by spinal circuits; this is followed by slower components thought to arise from primary motor cortex (M1) and other supraspinal areas. Spinal cord (SC) contributions to the slower components are rarely considered. To address this, we recorded neural activity in M1 and the cervical SC during a visuomotor tracking task, in which two female macaque monkeys moved their index finger against a resisting motor to track an on-screen target. Following the behavioral trial, an increase in motor torque rapidly returned the finger to its starting position (lever velocity >200°/s). Many cells responded to this passive mechanical perturbation (M1: 148/211 cells, 70%; SC: 67/119 cells, 56%). The neural onset latency was faster for SC compared to M1 cells (21.7±11.2ms vs 25.5±10.7ms respectively, mean ± SD). Using spike triggered averaging, some cells in both regions were identified as likely premotor cells, with monosynaptic connections to motoneurons. Response latencies for these cells were compatible with a contribution to the muscle responses following the perturbation. Comparable fractions of responding neurons in both areas were active up to 100ms after the perturbation, suggesting that both SC circuits and supraspinal centers could contribute to later response components. Significance Statement Following a limb perturbation, multiple reflexes help to restore limb position. Given conduction delays, the earliest part of these reflexes can only arise from spinal circuits. By contrast, long latency reflex components are typically assumed to originate from supraspinal centers. We recorded from both spinal and motor cortical cells in monkeys responding to index finger perturbations. Many spinal interneurons, including those identified as projecting to motoneurons, responded to the perturbation; the timing of responses was compatible with a contribution to both short-and longlatency reflexes. We conclude that spinal circuits also contribute to long latency reflexes in distal and forearm muscles, alongside supraspinal regions such as the motor cortex and brainstem.

Learning to Use Muscles

“…The addition of intermediary circuitry with computational functions of its own provides a basis for distributing sensorimotor control among the various efferent pathways and combining their results in a more useful way than a final common path. Simultaneous neural activity consistent with such integration has been recorded in motor cortex, pontomedullary reticular formation and spinal interneurons of non-human primates performing a finger dexterity task ( Soteropoulos & Baker, 2020 ; Soteropoulos, Williams, & Baker, 2012 ).…”

Convergence of proprioceptive and visual feedback on neurons in primary motor cortex

“…Muscle activity was 6 times larger for the mechanical loads than cursor slides, whereas M1 activity was only 3 times larger for mechanical loads than cursor slides. This suggests that M1 only contributes ∼50% of the total motor output for mechanical loads with the remaining output likely generated by subcortical circuits including brainstem and spinal cord (Mewes and Cheney, 1991; Soteropoulos et al, 2012; Herter et al, 2015; Soteropoulos and Baker, 2020). However, this estimate on the cortical contribution to motor corrections has many assumptions.…”

Spinal stretch reflexes support efficient control of reaching

“…Twenty individuals volunteered to participate in experiment 1 (males = 6, females = 14, age range 19-23) and 12 individuals volunteered to participate in experiment 2 (males = 8, females = 4, age range = [19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36][37][38]. All participants reported being free from neurological and musculoskeletal dysfunction and provided informed written consent before data collection.…”

“…perturbations (33), will be needed to determine if the presynaptic mechanism proposed here exists and whether it is governed by spinal processing that locally determines the arm's orientation or is implemented by supraspinal regions of the nervous system.…”