Sustained increase of somatosensory cortex excitability by tactile coactivation studied by paired median nerve stimulation in humans correlates with perceptual gain

Abstract

Cortical excitability can be reliably assessed by means of paired-pulse stimulation techniques. Recent studies demonstrated particularly for motor and visual cortex that cortical excitability is systematically altered following the induction of learning processes or during the development of pathological symptoms. A recent tactile coactivation protocol developed by Godde and coworkers showed that improvement of tactile performance in humans can be achieved also without training through passive stimulation on a time scale of a few hours. Tactile coactivation evokes plastic changes in somatosensory cortical areas as measured by blood oxygenation level-dependent (BOLD) activation in fMRI or SEP-dipole localization, which correlated with the individual gain in performance. To demonstrate changes in excitability of somatosensory cortex after tactile coactivation, we combined assessment of tactile performance with recordings of paired-pulse SEPs after electrical median nerve stimulation of both the right coactivated and left control hand at ISIs of 30 and 100 ms before, 3 h after and 24 h after tactile coactivation. Amplitudes and latencies of the first and second cortical N20/P25 response components were calculated. For the coactivated hand, we found significantly lowered discrimination thresholds and significantly reduced paired-pulse ratios (second N20/P25 response/first N20/P25 response) at an ISI of 30 ms after tactile coactivation indicating enhanced cortical excitability. No changes in paired-pulse behaviour were observed for ISIs of 100 ms. Both psychophysical and cortical effects recovered to baseline 24 h after tactile coactivation. The individual increase of excitability correlated with the individual gain in discrimination performance. For the left control hand we found no effects of tactile coactivation on paired-pulse behaviour and discrimination threshold. Our results indicate that changes in cortical excitability are modified by tactile coactivation and were scaled with the degree of improvement of the individual perceptual learning. Conceivably, changes of cortical excitability seem to constitute an additional important marker and mechanism underlying plastic reorganization.

Figures

Figure 1. Cortical responses to paired-pulse stimulation of one subject at an ISI of 30 ms before (left), 3 h after (middle) and 24 h after (right) tactile coactivation

The N20–P25 amplitudes of the first (A1) and second (A2) response are marked by grey bars. Note the reduction of paired pulse inhibition after tactile coactivation, which recovers to baseline 24 h later.

Figure 2. Experimental schedule: measurement of baseline performance of the right IF consisting of four sessions, one session post-tactile coactivation (S5) and one session 24 h after tactile coactivation (S6)

Performance of the left IF was tested in session 4, 5 and 8. SEPs were recorded in session 4, 5 and 6.

Figure 3. Mean paired-pulse ratio at ISIs of 30 (grey bars) and 100 ms (black bars) of the test side (right median nerve stimulation)

Significantly reduced suppression of paired-pulse ratio after tactile coactivation (post) at ISIs of 30 ms; the effect recovered 24 h after tactile coactivation (recovery). There was no significant influence of coactivation on the paired-pulse ratio at ISIs of 100 ms.

Figure 4. Mean paired-pulse ratio at ISIs of 30 (grey bars) and 100 ms (black bars) of the control side (left median nerve stimulation)

We found no significant effect of the contralateral tactile coactivation on the paired-pulse behaviour of the left control side.

Figure 5. Mean two-point discrimination thresholds in mm in the different sessions

Thresholds of right the index finger (IF) are shown in grey, thresholds of the left index finger in black. Thresholds of the right index finger were significantly lower after coactivation (post) in session 5. In the recovery measurement (recovery) 24 h after coactivation the threshold was back to baseline. There was no influence of coactivation on the test side (left IF) which was not coactivated.

Figure 6

Linear bivariate correlation analysis of coactivation-induced reduction of discrimination thresholds (x-axis) and the induced suppression of paired pulse inhibition (y-axis) with linear regression