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Exercise modulates chloride homeostasis after spinal cord injury
Journal article   Open access   Peer reviewed

Exercise modulates chloride homeostasis after spinal cord injury

Marie-Pascale Côté, Sapan Gandhi, Marina Zambrotta and John D Houlé
The Journal of neuroscience, v 34(27), pp 8976-8987
02 Jul 2014
PMID: 24990918
url
https://doi.org/10.1523/JNEUROSCI.0678-14.2014View
Published, Version of Record (VoR) Open

Abstract

Solute Carrier Family 12, Member 2 - genetics Homeostasis Exercise Therapy gamma-Aminobutyric Acid - physiology Cordotomy Brain-Derived Neurotrophic Factor - physiology Symporters - antagonists & inhibitors Female Chlorides - physiology Solute Carrier Family 12, Member 2 - metabolism Indenes - pharmacology Spinal Cord Injuries - metabolism Gene Expression Regulation Rats Random Allocation Nerve Tissue Proteins - genetics Rats, Sprague-Dawley Bumetanide - pharmacology Symporters - metabolism Chloride Channels - metabolism Nerve Tissue Proteins - metabolism Tibial Nerve - physiopathology H-Reflex - drug effects Animals Symporters - genetics Spinal Cord Injuries - rehabilitation Acetates - pharmacology Spinal Cord Injuries - physiopathology
Activity-based therapies are routinely integrated in spinal cord injury (SCI) rehabilitation programs because they result in a reduction of hyperreflexia and spasticity. However, the mechanisms by which exercise regulates activity in spinal pathways to reduce spasticity and improve functional recovery are poorly understood. Persisting alterations in the action of GABA on postsynaptic targets is a signature of CNS injuries, including SCI. The action of GABA depends on the intracellular chloride concentration, which is determined largely by the expression of two cation-chloride cotransporters (CCCs), KCC2 and NKCC1, which serve as chloride exporters and importers, respectively. We hypothesized that the reduction in hyperreflexia with exercise after SCI relies on a return to chloride homeostasis. Sprague Dawley rats received a spinal cord transection at T12 and were assigned to SCI-7d, SCI-14d, SCI-14d+exercise, SCI-28d, SCI-28d+exercise, or SCI-56d groups. During a terminal experiment, H-reflexes were recorded from interosseus muscles after stimulation of the tibial nerve and the low-frequency-dependent depression (FDD) was assessed. We provide evidence that exercise returns spinal excitability and levels of KCC2 and NKCC1 toward normal levels in the lumbar spinal cord. Acutely altering chloride extrusion using the KCC2 blocker DIOA masked the effect of exercise on FDD, whereas blocking NKCC1 with bumetanide returned FDD toward intact levels after SCI. Our results indicate that exercise contributes to reflex recovery and restoration of endogenous inhibition through a return to chloride homeostasis after SCI. This lends support for CCCs as part of a pathway that could be manipulated to improve functional recovery when combined with rehabilitation programs.

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