Time course of functional recovery during the first 3 mo after surgical transection and repair of nerves to the feline soleus and lateral gastrocnemius muscles

Robert J. Gregor, Huub Maas, Margarita A. Bulgakova, Alanna Oliver, Arthur W. English, Boris I. Prilutsky

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Locomotion outcomes after peripheral nerve injury and repair in cats have been described in the literature for the period immediately following the injury (muscle denervation period) and then again for an ensuing period of long-term recovery (at 3 mo and longer) resulting in muscle self-reinnervation. Little is known about the changes in muscle activity and walking mechanics during midrecovery, i.e., the early reinnervation period that takes place between 5 and 10 wk of recovery. Here, we investigated hindlimb mechanics and electromyogram (EMG) activity of ankle extensors in six cats during level and slope walking before and every 2 wk thereafter in a 14-wk period of recovery after the soleus (SO) and lateral gastrocnemius (LG) muscle nerves in one hindlimb were surgically transected and repaired. We found that the continued increase in SO and LG EMG magnitudes and corresponding changes in hindlimb mechanics coincided with the formation of neuromuscular synapses revealed in muscle biopsies. Throughout the recovery period, EMG magnitude of SO and LG during the stance phase and the duration of the stance-related activity were load dependent, similar to those in the intact synergistic medial gastrocnemius and plantaris. These results and the fact that EMG activity of ankle extensors and locomotor mechanics during level and upslope walking recovered 14 wk after nerve transection and repair suggest that loss of the stretch reflex in self-reinnervated muscles may be compensated by the recovered force-dependent feedback in self-reinnervated muscles, by increased central drive, and by increased gain in intermuscular motion-dependent pathways from intact ankle extensors. NEW & NOTEWORTHY This study provides new evidence that the timeline for functional recovery of gait after peripheral nerve injury and repair is consistent with the time required for neuromuscular junctions to form and muscles to reach preoperative tensions. Our findings suggest that a permanent loss of autogenic stretch reflex in self-reinnervated muscles may be compensated by recovered intermuscular force-dependent and oligosynaptic length-dependent feed-back and central drive to regain adequate locomotor output capabilities during level and upslope walking.

Original languageEnglish
Pages (from-to)1166-1185
Number of pages20
JournalJournal of Neurophysiology
Volume119
Issue number3
DOIs
Publication statusPublished - 1 Mar 2018

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Felidae
Skeletal Muscle
Muscles
Electromyography
Mechanics
Walking
Hindlimb
Ankle
Stretch Reflex
Peripheral Nerve Injuries
Cats
Muscle Denervation
Neuromuscular Junction
Locomotion
Gait
Synapses
Biopsy
Wounds and Injuries

Keywords

  • Cat
  • Muscle length and force feedback
  • Muscle self-reinnervation
  • Peripheral nerve injury
  • Proprioceptive feedback
  • Slope walking
  • Spinal reflexes

Cite this

Gregor, Robert J. ; Maas, Huub ; Bulgakova, Margarita A. ; Oliver, Alanna ; English, Arthur W. ; Prilutsky, Boris I. / Time course of functional recovery during the first 3 mo after surgical transection and repair of nerves to the feline soleus and lateral gastrocnemius muscles. In: Journal of Neurophysiology. 2018 ; Vol. 119, No. 3. pp. 1166-1185.
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Time course of functional recovery during the first 3 mo after surgical transection and repair of nerves to the feline soleus and lateral gastrocnemius muscles. / Gregor, Robert J.; Maas, Huub; Bulgakova, Margarita A.; Oliver, Alanna; English, Arthur W.; Prilutsky, Boris I.

In: Journal of Neurophysiology, Vol. 119, No. 3, 01.03.2018, p. 1166-1185.

Research output: Contribution to JournalArticleAcademicpeer-review

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T1 - Time course of functional recovery during the first 3 mo after surgical transection and repair of nerves to the feline soleus and lateral gastrocnemius muscles

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AU - Oliver, Alanna

AU - English, Arthur W.

AU - Prilutsky, Boris I.

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AB - Locomotion outcomes after peripheral nerve injury and repair in cats have been described in the literature for the period immediately following the injury (muscle denervation period) and then again for an ensuing period of long-term recovery (at 3 mo and longer) resulting in muscle self-reinnervation. Little is known about the changes in muscle activity and walking mechanics during midrecovery, i.e., the early reinnervation period that takes place between 5 and 10 wk of recovery. Here, we investigated hindlimb mechanics and electromyogram (EMG) activity of ankle extensors in six cats during level and slope walking before and every 2 wk thereafter in a 14-wk period of recovery after the soleus (SO) and lateral gastrocnemius (LG) muscle nerves in one hindlimb were surgically transected and repaired. We found that the continued increase in SO and LG EMG magnitudes and corresponding changes in hindlimb mechanics coincided with the formation of neuromuscular synapses revealed in muscle biopsies. Throughout the recovery period, EMG magnitude of SO and LG during the stance phase and the duration of the stance-related activity were load dependent, similar to those in the intact synergistic medial gastrocnemius and plantaris. These results and the fact that EMG activity of ankle extensors and locomotor mechanics during level and upslope walking recovered 14 wk after nerve transection and repair suggest that loss of the stretch reflex in self-reinnervated muscles may be compensated by the recovered force-dependent feedback in self-reinnervated muscles, by increased central drive, and by increased gain in intermuscular motion-dependent pathways from intact ankle extensors. NEW & NOTEWORTHY This study provides new evidence that the timeline for functional recovery of gait after peripheral nerve injury and repair is consistent with the time required for neuromuscular junctions to form and muscles to reach preoperative tensions. Our findings suggest that a permanent loss of autogenic stretch reflex in self-reinnervated muscles may be compensated by recovered intermuscular force-dependent and oligosynaptic length-dependent feed-back and central drive to regain adequate locomotor output capabilities during level and upslope walking.

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KW - Slope walking

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