Bihemispheric Motor Cortex Transcranial Direct Current Stimulation Improves Force Steadiness in Post-Stroke Hemiparetic Patients: A Randomized Crossover Controlled Trial

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http://journal.frontiersin.org/article/10.3389/fnhum.2016.00426/full?

Rafael A. Montenegro^1,2, Adrian Midgley³, Renato Massaferri^1,2, Wendell Bernardes², Alexandre H. Okano⁴ and Paulo Farinatti^2*

• ¹Graduate Program in Clinical and Experimental Physiopathology, Faculty of Medical Sciences, University of Rio de Janeiro State, Rio de Janeiro, Brazil
• ²Laboratory of Physical Activity and Health Promotion, Institute of Physical Education and Sports, University of Rio de Janeiro State, Rio de Janeiro, Brazil
• ³Department of Sport and Physical Activity, Edge Hill University, Ormskirk, Lancashire, UK
• ⁴Physical Education Department, Federal University of Rio Grande do Norte, Natal, RN, Brazil

Post-stroke patients usually exhibit reduced peak muscular torque (PT) and/or force steadiness during submaximal exercise. Brain stimulation techniques have been proposed to improve neural plasticity and help to restore motor performance in post-stroke patients. The present study compared the effects of bihemispheric motor cortex transcranial direct current stimulation (tDCS) on PT and force steadiness during maximal and submaximal resistance exercise performed by post-stroke patients vs. healthy controls. A double-blind randomized crossover controlled trial (identification number: TCTR20151112001; URL: http://www.clinicaltrials.in.th/) was conducted involving nine healthy and 10 post-stroke hemiparetic individuals who received either tDCS (2 mA) or sham stimulus upon the motor cortex for 20 min. PT and force steadiness (reflected by the coefficient of variation (CV) of muscular torque) were assessed during unilateral knee extension and flexion at maximal and submaximal workloads (1 set of 3 repetitions at 100% PT and 2 sets of 10 repetitions at 50% PT, respectively). No significant change in PT was observed in post-stroke and healthy subjects. Force steadiness during knee extension (~25–35%, P < 0.001) and flexion (~22–33%, P < 0.001) improved after tDCS compared to the sham condition in post-stroke patients, but improved only during knee extension (~13–27%, P < 0.001) in healthy controls. These results suggest that tDCS may improve force steadiness, but not PT in post-stroke hemiparetic patients, which might be relevant in the context of motor rehabilitation programs.

Introduction

Post-stroke patients often exhibit motor sequels (Langhorne et al., 2011) and hemiparesis (Prado-Medeiros et al., 2012) that are associated with increased variability in the application of force during motor tasks (Chow and Stokic, 2011). This condition typically results in low force steadiness (Moritz et al., 2005) and poor movement control (Kornatz et al., 2005) that can negatively impact on the ability to perform activities of daily living (Timmermans et al., 2014). Patients affected by stroke show a relative imbalance in either transcallosal inhibition or inter-hemispheric cerebral excitability, with hypo-excitability of the affected motor cortex concomitant to hyper-excitability of the non-affected motor cortex (Murase et al., 2004; Bolognini et al., 2011). Strategies to help counteract these imbalances and improve neural plasticity should therefore be beneficial for those patients (Bolognini et al., 2011; Simonetta-Moreau, 2014). Previous studies reported that improvements in neuronal plasticity and functional ability could be optimized by combining physical exercise and neurological therapy (Langhorne et al., 2011; Mang et al., 2013; Billinger et al., 2014).

Non-invasive brain stimulation techniques, such as transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS) have been considered as promising tools for restoring motor control and performance in post-stroke patients (Bolognini et al., 2011). Recently, Tanaka et al. (2011) demonstrated that a unilateral anodal tDCS over motor leg cortex slightly enhanced the maximal force production of the paretic leg. Even though there is controversial findings (O’Shea et al., 2014), evidence indicates that bihemispheric motor cortex tDCS seems to be more effective than unilateral tDCS (i.e., anodal or cathodal tDCS) to increase motor-evoked potentials in upper and lower limb contralateral to the affected cortex, thereby improving neuroplasticity (Bolognini et al., 2009; Cha et al., 2014) and to decrease excitability in regions that inhibit those areas (Vines et al., 2008). In addition, studies with post-stroke patients have evaluated the effects of tDCS using relatively restricted motor tasks, as isometric grip strength and hand function (Khedr et al., 2013; Cha et al., 2014). Thus, the effects of tDCS on the performance of tasks demanding submaximal and maximal strength, and force steadiness during exercise involving larger muscle groups of the legs are yet to be determined. This would be useful, since the muscle strength of both lower limbs is related to activities of daily living.

Recent studies with healthy subjects failed to observe changes in motor performance in response to tDCS in both upper (Hendy and Kidgell, 2013) and lower limbs extremities (Montenegro et al., 2015), which may be due to a possible “ceiling effect” when motor neuronal excitability is already optimal. This may help to explain the mixed findings in regards to the effects of tDCS upon cortical excitability in healthy subjects vs. post-stroke patients (Suzuki et al., 2012). In brief, it is feasible to think that the effects of tDCS upon cortical excitability rely on the extent to which the cortical function is preserved (Byblow et al., 2015), but there is a lack of research investigating this possibility. Comparisons between post-stroke patients and healthy controls regarding the effects of tDCS upon strength performance and force steadiness during gross motor tasks would be useful to test this hypothesis. Thus, the purpose of the present study was to investigate whether tDCS applied to the affected motor cortex in post-stroke hemiparetic patients would increase the peak muscular torque (PT) and force steadiness during a gross motor task in comparison with healthy controls. We hypothesized that tDCS would be capable to increase PT and force steadiness in post-stroke patients, but not in healthy subjects with preserved cortical function.