Impact of transcranial direct current stimulation on spinal network excitability in humans

Abstract

Transcranial direct current stimulation (tDCS) when applied over the motor cortex, modulates excitability dependent on the current polarity. The impact of this cortical modulation on spinal cord network excitability has rarely been studied. In this series of experiments, performed in healthy subjects, we show that anodal tDCS increases disynaptic inhibition directed from extensor carpi radialis (ECR) to flexor carpi radialis (FCR) with no modification of presynaptic inhibition of FCR Ia terminals and FCR H-reflex recruitment curves. We also show that cathodal tDCS does not modify spinal network excitability. Our results suggest that the increase of disynaptic inhibition observed during anodal tDCS relies on an increase of disynaptic interneuron excitability and that tDCS over the motor cortex in human subjects induces effects on spinal network excitability. Our results highlight the fact that the effects of tDCS should be considered in regard to spinal motor circuits and not only to cortical circuits.

Figures

Figure 1. Time course of radial-induced inhibition of the FCR H-reflex

A, time course of disynaptic inhibition of FCR H-reflex before, during and after 20 min of anodal tDCS applied over the hand motor cortex in one representative subject. Ordinate: amount of disynaptic inhibition. Amount of disynaptic inhibition is calculated using the following formula: ((mean control H value − mean conditioned H value)/mean control H value) × 100. Mean control H value and mean conditioned H value were obtained from 20 H-reflexes each. Vertical bars represent the standard error of the mean (±1 s.e.m.). ▴, amount of disynaptic inhibition during baseline time period. •, amount of disynaptic inhibition during Per1 time period. ▪, amount of disynaptic inhibition recorded during Per2 time period. ×, amount of disynaptic inhibition recorded in the Post1 time period. Arrow indicates the peak of disynaptic inhibition. Abscissa: conditioning test interval in milliseconds. B, time course of the presynaptic inhibition of FCR Ia afferents assessed by D1 method before, during and after 20 min of anodal tDCS applied over the hand motor cortex in one representative subject. Ordinate: amount of D1 inhibition. Amount of D1 inhibition is calculated using the following formula: ((mean control H value − mean conditioned H value)/mean control H value) × 100. Mean control H value and mean conditioned H value were obtained from 20 H-reflexes each. Vertical bars represent ±1 s.e.m.). ▴, amount of D1 inhibition during baseline time period. •, amount of D1 inhibition during Per1 time period. ▪ amount of D1 inhibition recorded during Per2 time period. ×, amount of D1 inhibition recorded in the Post1 time period. Abscissa: conditioning test interval in milliseconds.

Scheme 1

Schematic diagram of the experimental procedure

Figure 2. Changes in disynaptic inhibition in the anodal tDCS condition

A, changes in the amount of disynaptic inhibition between ECR and FCR induced by 20 min of anodal tDCS applied over the hand motor cortex in one subject. Ordinate: amount of disynaptic inhibition. Amount of disynaptic inhibition is calculated as in Fig. 1A and is represented by ▪. Mean control H value and mean conditioned H value were obtained from 40 H-reflexes each. Vertical bars represent ±1 s.e.m.). *P < 0.05. Abscissa: the 6 recording time periods, baseline corresponds to the period of recording before the onset of tDCS, Per1 to the first 10 min of recording during tDCS, Per2 to the second 10 min of recording during tDCS, Post1 to the first 10 min of recording after the end of tDCS, Post2 to the second 10 min of recording after the end of tDCS, Post3 to the last 10 min of recording after the end of tDCS. B, effect of anodal tDCS on disynaptic inhibition in each of the 13 subjects. Ordinate: as in Fig. 1A. Each full line represents one subject, the bold line represents the grand mean of the amount of disynaptic inhibition. Abscissa: time periods, baseline corresponds to the period of recording before the onset of tDCS, Per2 to the second 10 min of recording during tDCS, Post3 to the 10 min of recording after the end of tDCS.

Figure 3. Comparison between anodal (or cathodal) and sham condition

A, changes in disynaptic inhibition in the anodal tDCS condition and in the sham condition. Ordinate: disynaptic inhibition as a percentage of baseline value. The percentage of variation of disynaptic inhibition is calculated using the following formula in each of the thirteen subjects studied: ((mean disynaptic inhibition during period of measurement − mean disynaptic inhibition in the baseline condition)/mean disynaptic inhibition in the baseline condition) × 100. Mean disynaptic inhibition is obtained in a subject and in a given period from 40 control H-reflexes and 40 conditioned H-reflexes. The grand mean of these 13 values is then plotted on the graph. ▪, grand mean of the amount of disynaptic inhibition recorded in anodal condition. ▴, grand average of the amount of disynaptic inhibition recorded in the sham condition. Vertical bars represent ±1 s.e.m.*P < 0.05. Same abscissa as in Fig. 2A. B, changes of disynaptic inhibition in the cathodal and sham tDCS conditions. Ordinate as in Fig. 2A. □, grand mean of the amount of disynaptic inhibition recorded in cathodal condition. ▴, grand mean of the amount of disynaptic inhibition recorded in sham condition. Vertical bars represent ±1 s.e.m. Abscissa as in Fig. 2A.

Figure 4. Changes in D1 inhibition induced by tDCS

A, anodal tDCS condition and sham condition. Ordinate: D1 inhibition as a percentage of baseline value. The percentage of variation in D1 inhibition is calculated using the following formula in each of the thirteen subjects studied: ((mean D1 inhibition during period of measurement − mean D1 inhibition in baseline condition)/mean D1 inhibition in baseline condition) × 100. Mean D1 inhibition is obtained in a subject and in a given period from 40 control H-reflexes and 40 conditioned H-reflexes. The grand mean of these 13 values is then plotted on the graph. ▪, grand mean of the amount of D1 inhibition recorded in anodal condition. ▴, grand mean of the amount of D1 inhibition recorded in sham condition. Vertical bars represent ±1 s.e.m. Abscissa as in Fig. 2A. B, cathodal tDCS condition and sham condition. Ordinate is the same as those used in Fig. 4A. □, grand mean of amount of D1 inhibition recorded in cathodal condition. ▴, grand mean of the amount of D1 inhibition recorded in sham condition. Vertical bars represent ±1 s.e.m. Abscissa as in Fig. 2A.

Figure 5. Mean FCR H-reflex recruitment curves before, during and after anodal tDCS

Ordinate: H-reflex amplitude expressed as percentage Mmax value. Each point represents the grand mean of the amplitude of the H-reflex. Diamonds: H-reflex recruitment curve recorded during the baseline time period. Light squares: H-reflex recruitment curve recorded during the Per1 time period. Triangles: H-reflex recruitment curve recorded during Per2 time period. Black squares with dashed line: H-reflex recruitment curve recorded in the Post1 time period. Black squares with continuous line, H-reflex recruitment curve recorded in the Post2 time period. Vertical bars represent ±1 s.e.m. Abscissa: stimulus intensity expressed as a multiple of the intensity necessary to obtain a motor response equal to 25% of Mmax.