Clinical Neurophysiology xxx (2014) xxx–xxx

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Letter to the Editor Reply to ‘‘The effects of functional electrical stimulation on upper extremity function and cortical plasticity in chronic stroke patients’’

I appreciate the very important and developed suggestions by Dr. Cecatto for our article (Cecatto, 2014). The proposals on the reasons why EMG-controlled FES (EMG–FES) could shift the brain hemispheric-dominant perfusion in our study provided our study further development and progress. The motor output and corresponding muscle and joint proprioceptive feedback may be tightly coupled and coordinated with movement by EMG–FES. As Dr. Cecatto proposed, these neural reorganisation mechanisms should be explored. The sensory components of large afferent fibre activation, proprioceptive input and increased cognitive sensory attention are all weighted in the direction of spasticity reduction and are thus helpful in the return of voluntary movement and increased function (Roby-Brami et al., 1997). Nudo et al. suggest that afferent input associated with repetitive movements facilitates improvement of motor function (Nudo et al., 1996). For this reason, motor movement stimulation might be more effective in improving motor control than simple sensory stimulation. This is likely, as electrical stimulation that provokes motor activation is associated with cutaneous, muscle and joint proprioceptive afferent feedback. In another way, the mechanism underlying the EMG-controlled FES therapy is that alternative motor pathways are recruited and activated to assist impaired efferent pathways (Roby-Brami et al., 1997). This explanation is based on the sensory–motor integration theory that stipulates that sensory input from movement of an affected limb directly influences subsequent motor output (Stein, 1988). Iftime-Nielsen et al. reported that neuromuscular stimulation combined with voluntary activation produces more activation of the cerebellum and less activation of secondary somatosensory cortex (S2) than does neuromuscular stimulation alone in normal subjects (Iftime-Nielsen et al., 2012). An increase in somatosensory stimulation applied to a hemiparetic limb can benefit performance in functional tests for patients with chronic stroke (Conforto et al., 2002). This result supports the proposal that electrical sensory stimulation in combination with motor training protocols may enhance the benefits of standard neuro-rehabilitative treatments and may also facilitate motor learning (Wu et al., 2006). The sensory motor integration that occurs during the EMG-controlled FES increased perfusion of the ipsilesional sensory motor cortex (SMC) and resulted in functional improvement in the hemiparetic upper extremity in chronic stroke patients. A 5-month treatment intervention of EMG-controlled FES and motor learning produced cortical reorganisation correlated with functional gains as a shift of the brain perfusion from the contralesional to the ipsilesional hemisphere (Conforto et al., 2002). Fig. 1 shows physiological recovery mechanism schema of hemiparetic stroke. Non-affected-side motor-related area facilitation induces the hemiparesis improvement at acute recovery phase

(Calautti and Baron, 2003). Non-affected-side motor-related area cortex activity decreased at 6 months and 1 year after stroke onset (Ward et al., 2003). Finally, affected-side motor-related area cortex activity increase is important for recovery. The patterns of cortical activity in chronic stroke patients support the view that recovery from a hemiparetic stroke depends on the recruitment of alternative systems even in the affected hemisphere (Calautti et al., 2001). Neuroimaging studies of FES-evoked (FES delivered in the absence of voluntary activation) and FES-assisted (FES delivered to augment voluntary activation) movements have suggested that bilateral secondary S2 activation is related to the application of therapeutic FES (Iftime-Nielsen et al., 2012). From a point of view of this recovery mechanism, the FES increasing the activity of affected-side SMC possibly induces brain reorganisation to recover hemiparetic impairment in chronic stage. I also hypothesise that the Hebbian mechanism in the repeated FES rehabilitation that repeatedly generated synchronous pre- and postsynaptic neural activity along motor and sensory pathways might facilitate synaptic remodelling, leading to neural reorganisation that resulted in motor recovery. I wish that in the future, experimental animal studies can reveal the Hebbian mechanism in FES therapy and the cortical neurons that are changed by FES therapy, which neural circuits are more subject to the FES effects and how the interhemispheric connecting fibres are able to interact with FES therapy as Dr. Cecatto proposed. A suitable neurophysiological investigation with magnetic stimulation may be valuable to study the interhemispheric inhibition with FES treatment and the extent of its contribution to functional recovery after stroke. References Calautti C, Leroy F, Guincestre JY, Baron JC. Dynamics of motor network overactivation after striatocapsular stroke: a longitudinal PET study using a fixed-performance paradigm. Stroke 2001;32:2534–42. Calautti C, Baron JC. Functional neuroimaging studies of motor recovery after stroke in adults: a review. Stroke 2003;34:1553–66. Cecatto RB. The effects of functional electrical stimulation on upper extremity function and cortical plasticity in chronic stroke patients. Clin Neurophysiol 2014 [in this issue]. Conforto AB, Kaelin-Lang A, Cohen LG. Increase in hand muscle strength of stroke patients after somatosensory stimulation. Ann Neurol 2002;51:122–5. Roby-Brami A, Fuchs S, Mokhtari M. Reaching and grasping strategies in hemiparetic patients. Motor Control 1997;1:72–91. Iftime-Nielsen SD, Christensen MS, Vingborg RJ, Sinkjaer T, Roepstorff A, Grey MJ. Interaction of electrical stimulation and voluntary hand movement in SII and the cerebellum during simulated therapeutic functional electrical stimulation in healthy adults. Hum Brain Mapp 2012;33:40–9. Nudo RJ, Wise BM, SiFuentis F, Milliken GW. Neural substrates for the effects of rehabilitative trainings on motor recovery after ischemic infarct. Science 1996;272:1791–4. Stein DG. Brain injury and theories of recovery. In: Goldstein LB, editor. Restorative Neurology: Advances in Pharmacotherapy for Recovery after Stroke. Amonk, NY: Futura Publishing; 1988. p. 1–34. Ward NS, Brown MM, Thompson AJ, Frackowiak RS. Neural correlates of motor recovery after stroke: a longitudinal fMRI study. Brain 2003;126:2476–96. Wu CW, Seo H-J, Cohen LG. Influence of electric somatosensory stimulation on paretic-hand function in chronic stroke. Arch Phys Med Rehabil 2006;87:351–7.

1388-2457/$36.00 Ó 2014 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.clinph.2013.12.106

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Letter to the Editor / Clinical Neurophysiology xxx (2014) xxx–xxx

Fig. 1. Physiological recovery mechanism of hemiparesis. Non-affected side motor related area facilitation induce the hemiparesis improvement at acute recovery phase (Calautti and Baron, 2003). Non-affected side motor related area cortex activity decreased at half and one year after stroke onset (Ward et al., 2003). Finally affected side motor related area cortex activity increase is important for recovery. SMA; supplementary motor area, PM; premotor area, M1; primary motor area.



Yukihiro Hara Nippon Medical School, Chiba Hokusoh Hospital, Department of Rehabilitation Medicine, 1715 Kamakari, Inzai-City, Chiba Prefecture 270-1694, Japan ⇑ Tel.: +81 476 99 1111 (O), +81 3 3986 8221 (R); fax: +81 476 99 1917. E-mail address: [email protected] Available online xxxx

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