Locomotor and Reflex Adaptation After Partial Denervation of Ankle Extensors in Chronic Spinal Cats

Abstract

This work investigates the capacity of the spinal cord to generate locomotion after a complete spinal section and its ability to adapt its locomotor pattern after a peripheral nerve lesion. To study this intrinsic adaptive capacity, the left lateral gastrocnemius-soleus (LGS) nerve was sectioned in three cats that expressed a stable locomotion following a complete spinal transection. The electromyograph (EMG) of multiple hindlimb muscles and reflexes, evoked by stimulating the left tibial (Tib) nerve at the ankle, were recorded before and after denervation during treadmill locomotion. Following denervation, the mean amplitude of EMG bursts of multiple hindlimb muscles increased during locomotion, similar to what is found after an identical denervation in otherwise intact cats. Reflex changes were noted in ipsilateral flexors, such as semitendinosus and tibialis anterior, but not in the ipsilateral knee extensor vastus lateralis following denervation. The present results demonstrate that the spinal cord possesses the circuitry necessary to mediate increased EMG activity in multiple hindlimb muscles and also to produce changes in reflex pathways after a muscle denervation. The similarity of changes following LGS denervation in cats with an intact and transected spinal cord suggests that spinal mechanisms play a major role in the locomotor adaptation.

Incomplete spinal cord injury promotes durable functional changes within the spinal locomotor circuitry

“…Changes within the functional connectivity of the CPG following a lesion within the intrinsic circuitry have also been reported in mollusks, explaining recovery of escape behavior without the need for regeneration (Sakurai and Katz 2009). In addition, and in accordance with our results, several studies have previously shown asymmetric changes imprinted in the spinal circuitry that were revealed by a complete SCI Rossignol 2003a, 2003b;Frigon and Rossignol 2008;). …”

Short-Term Motor Compensations to Denervation of Feline Soleus and Lateral Gastrocnemius Result in Preservation of Ankle Mechanical Output during Locomotion

“…This idea is supported by reported changes in gains of proprioceptive feedback [Pearson and Misiaszek, 2000;Frigon and Rossignol, 2008;Donelan et al, 2009] and central drive to intact synergists [Gritsenko et al, 2001;Maas et al, 2010] after peripheral nerve injury. The adaptive locomotor changes must rely on proprioceptive feedback and could be mediated by neural plasticity at both spinal [Frigon and Rossignol, 2008] and supraspinal levels [Lundborg, 2000].…”

“…Studies in animals have demonstrated that within days after peripheral nerve injury there are changes in electromyographic (EMG) activity of intact synergists and movement kinematics. For instance, denervation of selected ankle extensors in the cat -e.g., soleus (SO) and lateral gastrocnemius (LG) -led to an increase in activity of the remaining intact major ankle extensors [Pearson et al, 1999;Prilutsky et al, 2006;Frigon and Rossignol, 2008;Donelan et al, 2009;Maas et al, 2010]. This enhancement in muscle activity is accompanied by a marked increase in the ankle angle yield (i.e.…”

“…ankle dorsiflexion) and a decrease in the knee flexion during stance of level and slope walking [Pearson et al, 1999;Maas et al, 2007;Donelan et al, 2009;Maas et al, 2010]. These immediate changes in motor pattern were suggested to be mediated by proprioceptive afferent signals, modifications of central drive to the muscles and changes in feedback gains [Pearson and Misiaszek, 2000;Gritsenko et al, 2001;Frigon and Rossignol, 2008;Donelan et al, 2009;Maas et al, 2010].…”

Promoting Gait Recovery and Limiting Neuropathic Pain After Spinal Cord Injury

“…4-7 Since the late 1990s, several studies have shown that motor training after spinal cord transection can lead to improvement in performance (training-induced walking recovery 8 ), be very specific (eg, stand vs walk 9,10 ), and involve spinal circuits reorganization. 4,11,12 On the other hand, sustained exposure to nociceptive input is known to result in central sensitization, a phenomenon defined as an amplification of neural signaling within the CNS eliciting pain hypersensitivity , including increased synaptic efficacy in nociceptive neurons in the dorsal horn of the spinal cord. 13 Central sensitization is considered as a form of maladaptive plasticity as it is an important feature in many patients with chronic pain, and especially in “unexplained” chronic pain disorders.…”