Proprioceptive neuropathy affects normalization of the H-reflex by exercise after spinal cord injury

Abstract

The H-reflex habituates at relatively low frequency (10 Hz) stimulation in the intact spinal cord, but loss of descending inhibition resulting from spinal cord transection reduces this habituation. There is a return towards a normal pattern of low-frequency habituation in the reflex activity with cycling exercise of the affected hind limbs. This implies that repetitive passive stretching of the muscles in spinalized animals and the accompanying stimulation of large (Group I and II) proprioceptive fibers has modulatory effects on spinal cord reflexes after injury. To test this hypothesis, we induced pyridoxine neurotoxicity that preferentially affects large dorsal root ganglia neurons in intact and spinalized rats. Pyridoxine or saline injections were given twice daily (IP) for 6 weeks and half of the spinalized animals were subjected to cycling exercise during that period. After 6 weeks, the tibial nerve was stimulated electrically and recordings of M and H waves were made from interosseous muscles of the hind paw. Results show that pyridoxine treatment completely eliminated the H-reflex in spinal intact animals. In contrast, transection paired with pyridoxine treatment resulted in a reduction of the frequency-dependent habituation of the H-reflex that was not affected by exercise. These results indicate that normal Group I and II afferent input is critical to achieve exercise-based reversal of hyper-reflexia of the H-reflex after spinal cord injury.

Activity-Dependent Increase in Neurotrophic Factors Is Associated with an Enhanced Modulation of Spinal Reflexes after Spinal Cord Injury

“…The feet were secured to the pedals with surgical tape. This custom motor-driven apparatus moved the hindlimbs through a complete range of motion at a rate of 45 rpm, as described previously (Houlé et al, 1999;Ollivier-Lanvin et al, 2010;Skinner et al, 1996). Animals receiving step-training were placed over a motorized treadmill belt (*9-11 cm/sec) with the forelimbs resting on an acrylic glass platform.…”

“…When the spinal cord is intact, the amplitude of the H-reflex decreases considerably with increasing stimulus frequency (Lee et al, 2005;Ollivier-Lanvin et al, 2010;Thompson et al, 1992). Since biological stimuli are usually transmitted as repetitive signals, the mechanism that modulates motor output relative to repetitive input is thought to shape reflex excitability (Koerber and Mendell, 1991).…”

“…Since biological stimuli are usually transmitted as repetitive signals, the mechanism that modulates motor output relative to repetitive input is thought to shape reflex excitability (Koerber and Mendell, 1991). This ability to attenuate the response is impaired after complete or incomplete SCI in animals and humans (Boulenguez et al, 2010;Grey et al, 2008;Ollivier-Lanvin et al, 2010;Thompson et al, 1992). Previous studies have shown that passive exercise (i.e., cycling) helps to recover the frequency-dependent depression of the H-reflex in animals (Reese et al, 2006;Skinner et al, 1996) and humans (Kiser et al, 2005;Phadke et al, 2009) after SCI.…”

Passive cycling in neurorehabilitation after spinal cord injury: A review

“…To verify this hypothesis, pyridoxine neurotoxicity, preferentially affecting large DRG, has been induced in intact and spinalized rats who were subjected to PC exercise. 21 Pyridoxine treatment completely eliminated the H-reflex in intact animals, while transection paired with pyridoxine treatment led to a reduction of the frequency-dependent habituation of the H-reflex that was not affected by exercise. These findings indicate that normal Group I and II afferent input is critical to achieve exercise-based reversal of hyperreflexia after SCI.…”

Gene expression analysis of neurotrophins, Trk receptors, and associated regulatory molecules after contusive spinal cord injury.

“…Additionally, the type and amount of sensory input can influence spontaneous recovery after SCI (Grau, Washburn et al 2004;Ollivier-Lanvin, Keeler et al 2010;Caudle, Brown et al 2011;Grau, Huie et al 2012) and also influence the effectiveness of physical therapy (Bouyer and Rossignol 1998;Bouyer and Rossignol 2003;Gomez-Pinilla, Ying et al 2004;Edgerton, Courtine et al 2008;Frigon and Rossignol 2009;Ollivier-Lanvin, Keeler et al 2010), all of which may involve neurotrophin signaling (Gomez-Pinilla, Hutchinson, Gomez-Pinilla et al 2004;Boyce, Tumolo et al 2007;de Leon 2007;Côté MP 2011;Boyce, Park et al 2012). Further, autonomic dysreflexia (AD), a maladaptive condition frequently observed in patients with cervical or high thoracic SCI, is often triggered by nociceptive sensory input (Maiorov, Fehlings et al 1998;Krassioukov and Fehlings 1999;Garstang and Miller-Smith 2007), and sprouting of central terminals of nociceptive neurons, thought to be NGF-dependent, is a proposed mechanism that contributes to AD (Weaver, Cassam et al 1997;Krenz, Meakin et al 1999;Marsh, Wong et al 2002;Cameron, Smith et al 2006;Ackery, Norenberg et al 2007).…”