Abstract
Coordinated movement requires patterned activation of muscles. In this study, we examined differences in selective activation of primate upper limb muscles by cortical and subcortical regions. Five macaque monkeys were trained to perform a reach and grasp task, and electromyogram (EMG) was recorded from 10 to 24 muscles while weak single-pulse stimuli were delivered through microelectrodes inserted in the motor cortex (M1), reticular formation (RF), or cervical spinal cord (SC). Stimulus intensity was adjusted to a level just above threshold. Stimulus-evoked effects were assessed from averages of rectified EMG. M1, RF, and SC activated 1.5 ± 0.9, 1.9 ± 0.8, and 2.5 ± 1.6 muscles per site (means ± SD); only M1 and SC differed significantly. In between recording sessions, natural muscle activity in the home cage was recorded using a miniature data logger. A novel analysis assessed how well natural activity could be reconstructed by stimulus-evoked responses. This provided two measures: normalized vector length L, reflecting how closely aligned natural and stimulus-evoked activity were, and normalized residual R, measuring the fraction of natural activity not reachable using stimulus-evoked patterns. Average values for M1, RF, and SC were L = 119.1 ± 9.6, 105.9 ± 6.2, and 109.3 ± 8.4% and R = 50.3 ± 4.9, 56.4 ± 3.5, and 51.5 ± 4.8%, respectively. RF was significantly different from M1 and SC on both measurements. RF is thus able to generate an approximation to the motor output with less activation than required by M1 and SC, but M1 and SC are more precise in reaching the exact activation pattern required. Cortical, brainstem, and spinal centers likely play distinct roles, as they cooperate to generate voluntary movements.NEW & NOTEWORTHY Brainstem reticular formation, primary motor cortex, and cervical spinal cord intermediate zone can all activate primate upper limb muscles. However, brainstem output is more efficient but less precise in producing natural patterns of motor output than motor cortex or spinal cord. We suggest that gross muscle synergies from the reticular formation are sculpted and refined by motor cortex and spinal circuits to reach the finely fractionated output characteristic of dexterous primate upper limb movements.
Highlights
Controlling movement requires that a large number of muscles are activated in the correct pattern
Overduin et al (2012) showed that stimulation of the motor cortex in macaque monkeys produced muscle activations well represented by a small number of synergies, suggesting that synergies had a basis in the underlying neural representation
Previous work has examined the outputs from different motor structures using responses to either stimulation or post-spike facilitation in spike-triggered averages of rectified EMG
Summary
Controlling movement requires that a large number of muscles are activated in the correct pattern The complexity of this problem has led to suggestions that the nervous system uses dimensional reduction, controlling a small number of functional synergies rather than every muscle independently (Saltiel et al 2001). Different versions of this idea defined either spatial (a set of muscles, activated in fixed ratios) or spatiotemporal (time-varying templates of muscle coactivations) synergies (Overduin et al 2015). Overduin et al (2012) showed that stimulation of the motor cortex in macaque monkeys produced muscle activations well represented by a small number of synergies, suggesting that synergies had a basis in the underlying neural representation
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