Effects of anodal transcranial direct current stimulation over the leg motor area on lumbar spinal network excitability in healthy subjects

Abstract

In recent years, two techniques have become available for the non-invasive stimulation of human motor cortex: transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS). The effects of TMS and tDCS when applied over motor cortex should be considered with regard not only to cortical circuits but also to spinal motor circuits. The different modes of action and specificity of TMS and tDCS suggest that their effects on spinal network excitability may be different from that in the cortex. Until now, the effects of tDCS on lumbar spinal network excitability have never been studied. In this series of experiments, on healthy subjects, we studied the effects of anodal tDCS over the lower limb motor cortex on (i) reciprocal Ia inhibition projecting from the tibialis anterior muscle (TA) to the soleus (SOL), (ii) presynaptic inhibition of SOL Ia terminals, (iii) homonymous SOL recurrent inhibition, and (iv) SOL H-reflex recruitment curves. The results show that anodal tDCS decreases reciprocal Ia inhibition, increases recurrent inhibition and induces no modification of presynaptic inhibition of SOL Ia terminals and of SOL-H reflex recruitment curves. Our results indicate therefore that the effects of tDCS are the opposite of those previously described for TMS on spinal network excitability. They also indicate that anodal tDCS induces effects on spinal network excitability similar to those observed during co-contraction suggesting that anodal tDCS activates descending corticospinal projections mainly involved in co-contractions.

Figure 1. Schematic of the experimental procedure

The series of experiments comprised four spinal reflex recording periods, a baseline period prior to tDCS application, the Per 1 time period which corresponds to the first 10 min of tDCS (0–10 min), the Per 2 time period which corresponds to the second 10 min of recording during tDCS (11–20 min), the Post 1 time period which corresponds to the first 10 min following termination of tDCS (21–30 min).

Figure 2. Diagram of lumbar spinal circuits studied

A, diagram of reciprocal inhibition directed from TA to SOL and presynaptic inhibition on SOL Ia terminals. B, diagram of recurrent inhibition experimental procedure. The arrow S1 corresponds to the conditioning stimulus, the arrow SM corresponds to the test stimulus. The dashed arrow H1 represents the conditioning reflex discharge.

Figure 3. Changes of reciprocal Ia inhibition in the anodal tDCS condition and in the sham condition

A, effect of anodal tDCS on reciprocal Ia inhibition in each of the 14 subjects. Ordinate: amount of reciprocal Ia inhibition. Amount of reciprocal Ia inhibition is calculated with 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 respectively obtained from 40 Hreflexes. Each full line represents one subject; the black line illustrates the subjects for whom anodal tDCS decreases the amount of reciprocal Ia inhibition, and grey lines indicate those subjects for whom anodal tDCS increases the amount of reciprocal Ia inhibition. Abscissa: time period; baseline corresponds to the recording period before the onset of tDCS, and Per 2 to the second 10 min of recording during tDCS. B, time course of the effects of anodal tDCS on reciprocal Ia inhibition. Ordinate: grand average of the amount of reciprocal Ia inhibition. The grand average of the amount of reciprocal Ia inhibition is illustrated by a filled triangle in each of the time periods of recording. Vertical bars represent the standard error of the mean (±1 SEM). Asterisks (*) indicate a significant value (with P < 0.05) compared to baseline amount of inhibition. Abscissa: the four recording time periods; baseline corresponds to the recording period before the onset of tDCS, Per 1 to the first 10 min of recording during tDCS, Per 2 to the second 10 min of recording during tDCS, and Post 1 to the first 10 min of recording after the end of tDCS. C, effect of sham condition on reciprocal Ia inhibition in each of the 14 subjects. Ordinate and abscissa: same as A. D, time course of the effects of sham condition on reciprocal Ia inhibition. Ordinate and abscissa: same as B.

Figure 4. Changes of presynaptic inhibition of SOL Ia afferents in the anodal tDCS condition and in the sham condition

A, effect of anodal tDCS on presynaptic Ia inhibition in each of the 14 subjects. Ordinate: amount of presynaptic Ia inhibition. Amount of presynaptic Ia 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 respectively obtained from 40 H-reflexes. Each full line represents one subject, the dark line illustrates the subjects for whom anodal tDCS decreases the amount of presynaptic Ia inhibition, and the grey line illustrates the subjects for whom anodal tDCS increases the amount of presynaptic Ia inhibition. Abscissa: time period; baseline corresponds to the recording period before the onset of tDCS, and Per 2 to the second 10 min of recording during tDCS. B, time course of the effects of anodal tDCS on presynaptic Ia inhibition. Ordinate: grand average of the amount of presynaptic Ia inhibition. The grand average of the amount of presynaptic Ia inhibition is illustrated by a filled triangle in each of the time periods of recording. Vertical bars represent the standard error of the mean (±1 SEM). Asterisks (*) indicate a significant value (with P < 0.05) compared to baseline amount of inhibition. Abscissa: the four recording time periods; baseline corresponds to the recording period before the onset of tDCS, Per 1 to the first 10 min of recording during tDCS, Per 2 to the second 10 min of recording during tDCS, and Post 1 to the first 10 min of recording after the end of tDCS. C, effect of sham condition on presynaptic Ia inhibition in each of the 14 subjects. Ordinate and absciss: same as A. D, time course of the effects of sham condition on reciprocal Ia inhibition. Ordinate and abscissa: same as B.

Figure 5. Changes of recurrent inhibition in the anodal tDCS condition and in the sham condition

A, effect of anodal tDCS on H′ response in each of the 14 subjects. Ordinate: H′ response expressed in% of M_max. Mean H′ response of one subject was obtained from 40 H′ responses. Each full line represents one subject, the dark line illustrates the subjects for who anodal tDCS decreases the mean H′ response value (and thus increases recurrent inhibition), the grey line illustrates the subjects for whom anodal tDCS increases the mean H′ response value (and thus decreases recurrent inhibition). Abscissa: time period; baseline corresponds to the recording period before the onset of tDCS, and Per 2 to the second 10 min of recording during tDCS. B, time course of the effects of anodal tDCS on the grand average of the mean H′ response. Ordinate: grand average of the mean H′ response obtained in each of the 14 subjects studied. The grand average of the mean H′ response is illustrated by a filled triangle in each of the time periods of recording. Vertical bars represent the standard error of the mean (±1 SEM). Asterisks (*) indicate a significant value (with P < 0.05) compared to baseline amount of inhibition. Abscissa: the four recording time periods; baseline corresponds to the recording period before the onset of tDCS, Per 1 to the first 10 min of recording during tDCS, Per 2 to the second 10 min of recording during tDCS, and Post 1 to the first 10 min of recording after the end of tDCS. C, effect of sham condition on mean H′ response in each of the 14 subjects. Ordinate and absciss: same as A. D, time course of the effects of sham condition on reciprocal Ia inhibition. Ordinate and abscissa: same as B.

Figure 6. Modification of the grand average of the FCR H-reflex threshold, H_max/M_max ratio and the slope of the ascending part of the FCR H-reflex recruitment curve induced by anodal tDCS

Abscissa for A–C: the four recording time periods; baseline corresponds to the recording period before the onset of tDCS, Per 1 to the first 10 min of recording during tDCS, Per 2 to the second 10 min of recording during tDCS, and Post 1 to the first 10 min of recording after the end of tDCS. For A–C, abscissa: the 4 recording time periods. Vertical bars: stand error of the mean. Asterisks indicate a significant value with P < 0.05. A: FCR H reflex threshold expressed in % of M_max. B: FCR H_max/M_max ratio. C: slop of the ascending part of the FCR H reflex recruitment curve.