Improvement of spatial tactile acuity by transcranial direct current stimulation

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Abstract

Objective

Non-invasive brain stimulation such as transcranial direct current stimulation (tDCS) has been successfully used to induce polarity-specific excitability changes in the brain. However, it is still unknown if anodal tDCS (tDCSanodal) applied to the primary somatosensory cortex (S1) can lead to behavioral changes in performance of tactile discriminative tasks.

Methods

Using an accurate tactile discrimination task (grating orientation task: GOT) we tested the hypothesis that application of 1 mA of tDCSanodal (current density at the electrodes of 0.04 mA/cm2) over the left S1 can lead to an improved tactile spatial acuity in the contralateral index-finger (IF).

Results

Performance in the GOT task with the contralateral IF but not with the ipsilateral IF was enhanced for about 40 min after a 20 min application of tDCSanodal in the absence of changes with sham stimulation.

Conclusions

These results provide the first evidence that tDCSanodal over S1 improves performance in a complex somatosensory task beyond the period of stimulation.

Significance

The ability to induce performance improvement in the somatosensory domain with tDCS applied over S1 could be used to promote functional recovery in patients with diminished tactile perception.

Introduction

Somatosensory input is crucial for skillful motor control and for learning new motor skills (Johansson and Westling, 1984, Pause et al., 1989, Hermsdorfer et al., 2004). In animal experiments, surgically abolished sensation in one of the forelimbs in monkeys leads to a decrease of voluntary motor activity (Taub, 1977). More recently, the same phenomenon has been studied in detail in human subjects. For example, a reduction of somatosensory input by local anesthesia impairs motor control in normal volunteers (Monzee et al., 2003, Duque et al., 2005). Conversely, it has been shown that increased somatosensory input by means of peripheral nerve stimulation modulates cortico-motor excitability in healthy volunteers and enhances transiently motor function in chronic stroke patients (Ridding et al., 2000, Kaelin-Lang et al., 2002, Conforto et al., 2007). Additionally, previous studies demonstrated that it is possible to modulate somatosensory (Tegenthoff et al., 2005, Dieckhofer et al., 2006, Pleger et al., 2006) and motor (Hummel et al., 2005) function by noninvasive brain stimulation. These techniques might therefore play an adjuvant role in rehabilitative treatments of neurological and psychiatric disorders (for review see (Kobayashi and Pascual-Leone, 2003, Ward and Cohen, 2004, Cooke and Bliss, 2006)).

Transcranial direct current stimulation (tDCS), a particular form of noninvasive brain stimulation, is a procedure used to polarize brain regions through the application of weak direct currents (Nitsche and Paulus, 2000, Wassermann and Grafman, 2005). For example, anodal tDCS (tDCSanodal) applied over the primary motor cortex (M1) transiently increases cortical excitability beyond the period of stimulation, while cathodal stimulation often decreases it (Priori et al., 1998, Nitsche and Paulus, 2001). Furthermore, tDCS-induced excitability changes seem to be associated with effects on performance of motor as well as non-motor tasks (Hummel et al., 2005, Hummel and Cohen, 2006).

In the somatosensory cortex, comparable polarity-specific differential effects of tDCS on the high and low frequency components or amplitudes of somatosensory evoked potentials (SEPs) have also been demonstrated (Matsunaga et al., 2004, Dieckhofer et al., 2006). However, it is still unknown if tDCSanodal application over primary somatosensory cortex (S1) is capable to induce changes in tactile spatial acuity in human subjects.

Here, we intended to clarify if application of tDCSanodal centered over the left S1 influences tactile discrimination skills on the index-finger (IF) contralateral to stimulation in healthy volunteers. As a behavioral outcome measure, we choose the grating orientation task (GOT), an accurate and commonly accepted measure of tactile spatial acuity in human subjects (Johnson and Phillips, 1981, Van Boven and Johnson, 1994).

Since tDCS elicits lesser perceptual phenomena than transcranial magnetic stimulation (TMS) or theta burst stimulation (TBS) such as acoustic noise or sudden scalp sensation, tDCS has possibly a greater potential for sham-controlled studies and clinical applications. Furthermore, one technical advantage of tDCS application is that performance changes can be measured during the time of stimulation. Therefore, tDCS could be a useful adjuvant tool when combined with performance of complex cognitive tasks or rehabilitative treatments after brain lesions (Gandiga et al., 2006).

Section snippets

Subjects

We studied ten healthy volunteers between 23 and 34 years of age (26.8 ± 3.9 years (SD); 5/10 females). They gave written informed consent to participate in the experiment according to the declaration of Helsinki and the NINDS Institutional Review Board approved the study. Prior to participation, all volunteers underwent a comprehensive neurological examination. According to the Oldfield questionnaire for the assessment of handedness (Oldfield, 1971), all subjects were right-handed.

Main experiment

We tested the

Results

All volunteers achieved a stable baseline performance in the GOT task on the right IF prior to tDCS application (see Fig. 2a and b). There was no significant difference between GOT thresholds on the right IF within the familiarization measurements (GOT1–4) between tDCSanodal and tDCSsham (tDCSanodal: 1.60 ± 0.15 mm; tDCSsham: 1.63 ± 0.14 mm; repeated measures ANOVA with factor INTERVENTION: F(1, 18) = 0.021; p = 0.888, see also Table 1 and 2 for individual subject data). ANOVARM revealed a significant

Discussion

Our results demonstrate that a short period of tDCSanodal applied over the human S1 enhances tactile spatial acuity in the contralateral hand relative to sham stimulation. This performance improvement lasts for at least 40 min after the end of the stimulation period and is not present in the hand ipsilateral to the stimulated S1.

Improvements in tactile performance after non-invasive brain stimulation have been reported in previous studies. For example, 5 Hz rTMS, paired-associative stimulation or

Acknowledgements

This research was supported by a grant from the Deutsche Forschungsgemeinschaft (DFG) to P.R. (Ra 1391/1–1) and by the Intramural Research Program of the NIH, NINDS. Y.V. was supported by a NINDS Competitive Fellowship grant and a FSR Post-Doctoral Grant from the Université catholique de Louvain (Belgium).

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