Brain Advance Access published online on March 15, 2008
Brain, doi:10.1093/brain/awn050
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Changes in sensory-evoked synaptic activation of motoneurons after spinal cord injury in man
1Department of Biomedical Engineering, 2Centre for Neuroscience, 3Faculty of Rehabilitation Medicine and 4Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada
Correspondence to:
Dr Monica Gorassini, Centre for Neuroscience, 513 Heritage Medical Research Centre, University of Alberta, Edmonton, Alberta, Canada T6G 2S2 E-mail: monica.gorassini{at}ualberta.ca
Following spinal cord injury (SCI), prolonged muscle spasms are readily triggered by brief sensory stimuli. Animal and indirect human studies have shown that a substantial portion of the depolarization of motoneurons during a muscle spasm comes from the activation of persistent inward currents (PICs). The brief (single pulse) sensory stimuli that trigger the PICs and muscle spasms in chronically spinalized animals evoke excitatory post-synaptic potentials (EPSPs) that are broadened to more than 500 ms, the duration of depolarization required to activate a PIC in the motoneuron. Thus, in humans, we investigated if post-synaptic potentials (PSPs) evoked from brief (<20 ms) sensory stimulation are changed after SCI and if they are broadened to 
500 ms to more readily activate motoneuron PICs and muscle spasms. To estimate both the shape and duration of PSPs in human subjects we used peristimulus frequencygrams (PSFs), which are plots of the instantaneous firing frequency of tonically active single motor units that are time-locked to the occurrence of the sensory stimulus. PSFs in response to cutaneomuscular stimulation of the medial arch or toe of the foot, a sensory stimulus that readily triggers muscle spasms, were compared between non-injured control subjects and in spastic subjects with chronic (>1 year), incomplete SCI. In non-injured controls, a single shock or brief (<20 ms) train of cutaneomuscular stimulation produced PSFs consisting of a 300 ms increase in firing rate above baseline with an interposed period of reduced firing. Parallel intracellular experiments in motoneurons of adult rats revealed that a 300 ms EPSP with a fast intervening inhibitory PSP (IPSP) reproduced the PSF recorded in non-injured subjects. In contrast, the same brief sensory stimulation in subjects with chronic SCI produced PSFs of comparatively long duration (1200 ms) with no evidence for IPSP activation, as reflected by a lack of reduced firing rates after the onset of the PSF. Thus, unlike non-injured controls, the motoneurons of subjects with chronic SCI are activated by very long periods of pure depolarization from brief sensory activation. It is likely that these second-long EPSPs securely recruit slowly activating PICs in motoneurons that are known to mediate, in large part, the many seconds-long activation of motoneurons during involuntary muscle spasms.
Key Words: spasticity; motor unit; spinal cord injury; sensory processing; reflexes
Abbreviations: AHP, afterhyperpolarization; CUSUM, cumulative sum; EPSP, excitatory post-synaptic potential; IPSP, inhibitory post-synaptic potential; iSCI, incomplete spinal cord injury; PIC, persistent inward current; PSF, peristimulus frequencygram; PSTH, post-stimulus time histogram; TA, tibialis anterior
Received September 4, 2007. Revised February 20, 2008. Accepted February 25, 2008.
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