Reorganization of motor modules for standing reactive balance recovery following pyridoxine-induced large-fiber peripheral sensory neuropathy in cats

J Neurophysiol. 2020 Sep 1;124(3):868-882. doi: 10.1152/jn.00739.2019. Epub 2020 Aug 12.

Abstract

Task-level goals such as maintaining standing balance are achieved through coordinated muscle activity. Consistent and individualized groupings of synchronously activated muscles can be estimated from muscle recordings in terms of motor modules or muscle synergies, independent of their temporal activation. The structure of motor modules can change with motor training, neurological disorders, and rehabilitation, but the central and peripheral mechanisms underlying motor module structure remain unclear. To assess the role of peripheral somatosensory input on motor module structure, we evaluated changes in the structure of motor modules for reactive balance recovery following pyridoxine-induced large-fiber peripheral somatosensory neuropathy in previously collected data in four adult cats. Somatosensory fiber loss, quantified by postmortem histology, varied from mild to severe across cats. Reactive balance recovery was assessed using multidirectional translational support-surface perturbations over days to weeks throughout initial impairment and subsequent recovery of balance ability. Motor modules within each cat were quantified by non-negative matrix factorization and compared in structure over time. All cats exhibited changes in the structure of motor modules for reactive balance recovery after somatosensory loss, providing evidence that somatosensory inputs influence motor module structure. The impact of the somatosensory disturbance on the structure of motor modules in well-trained adult cats indicates that somatosensory mechanisms contribute to motor module structure, and therefore may contribute to some of the pathological changes in motor module structure in neurological disorders. These results further suggest that somatosensory nerves could be targeted during rehabilitation to influence pathological motor modules for rehabilitation.NEW & NOTEWORTHY Stable motor modules for reactive balance recovery in well-trained adult cats were disrupted following pyridoxine-induced peripheral somatosensory neuropathy, suggesting somatosensory inputs contribute to motor module structure. Furthermore, the motor module structure continued to change as the animals regained the ability to maintain standing balance, but the modules generally did not recover pre-pyridoxine patterns. These results suggest changes in somatosensory input and subsequent learning may contribute to changes in motor module structure in pathological conditions.

Keywords: electromyography; muscle synergies; sensory loss.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cats
  • Disease Models, Animal
  • Electromyography
  • Muscle, Skeletal / physiology*
  • Nerve Fibers, Myelinated / drug effects
  • Nerve Fibers, Myelinated / pathology*
  • Neurons, Afferent / drug effects
  • Neurons, Afferent / pathology*
  • Peripheral Nervous System Diseases / chemically induced
  • Peripheral Nervous System Diseases / physiopathology*
  • Postural Balance / physiology*
  • Pyridoxine / pharmacology
  • Recovery of Function / physiology*
  • Somatosensory Disorders / chemically induced
  • Somatosensory Disorders / physiopathology*
  • Vitamin B Complex / pharmacology

Substances

  • Vitamin B Complex
  • Pyridoxine