Parallel modulation of interhemispheric inhibition and the size of a cortical hand muscle representation during active contraction

Abstract

Interhemispheric inhibition (IHI) between motor cortexes is thought to suppress unwanted mirror movements during voluntary behaviors and can be assessed using paired-pulse transcranial magnetic stimulation (TMS). The magnitude of IHI may be related to the size of the cortical representation for a given muscle as a mechanism for facilitating unimanual control. To date, the relationship between IHI and cortical muscle representations remains unknown. Fifteen healthy, right-handed individuals participated in the present study. IHI was examined in the right first dorsal interosseous (FDI) muscle by delivering conditioning TMS to ipsilateral (right) primary motor cortex (M1) followed by a test TMS pulse to contralateral (left) M1. The size of the FDI representation in M1 was determined by delivering suprathreshold TMS over a 5 × 5-cm grid centered on the FDI motor hotspot of the left M1. Both IHI and cortical territory were obtained during three conditions: rest, contralateral (right) FDI contraction, and ipsilateral (left) FDI contraction. Results indicate a significant association between IHI and the size of the FDI representation only in the context of contraction and not when the FDI muscle was relaxed. Specifically, reduced IHI corresponded to larger cortical FDI representations during both contralateral and ipsilateral contraction. These data demonstrate that, for a muscle of the hand, the magnitude of IHI and the cortical territory are associated within the context of muscle contraction. NEW & NOTEWORTHY This study provides evidence from noninvasive brain stimulation that communication between the motor cortexes of the two hemispheres plays a role in shaping the motor cortical map that outputs to a hand muscle during active contraction of that muscle. This relationship exists only when the hand muscle is contracted. The findings presented further our understanding of motor control during unilateral movement and may inform future research targeting clinical populations that exhibit impaired unilateral control.

Keywords: FDI; IHI; TMS; motor map; transcranial magnetic stimulation.

Fig. 1.

Depictions of the dependent variables and experimental conditions. A: in the REST condition, interhemispheric inhibition (IHI) was probed by delivering a conditioning stimulus (CS) over the right hemisphere at either 10 ms (SIHI) or 40 ms (LIHI) before a test stimulus (TS) delivered over the left hemisphere. Map area was obtained by delivering 4 pulses to each grid point over a 5 × 5 cm grid space that was centered on the motor hotspot for the target first dorsal interosseous (FDI) muscle. B: in the condition of right FDI contraction (CONTRA), SIHI, LIHI, and map area were obtained while the right FDI was isometrically contracted to 10% maximum voluntary contraction (MVC). C: in the condition of left FDI contraction (IPSI), SIHI, LIHI, and map area were obtained while the left FDI was isometrically contracted to 10% MVC.

Fig. 2.

Effects of muscle contraction on right first dorsal interosseous (FDI) muscle representation. A: the size of the muscle representation was greater during condition of right FDI contraction (CONTRA) relative to both REST condition and condition of left FDI contraction (IPSI) (P < 0.001 for both). B: compared with REST, short-interval interhemispheric inhibition (SIHI) was significantly reduced from REST in both CONTRA (P < 0.001) and IPSI (P = 0.042) conditions. SIHI was reduced more so during CONTRA compared with IPSI (P = 0.002). C: compared with rest, long-interval interhemispheric inhibition (LIHI) was significantly reduced from REST in CONTRA (P = 0.006). *Significant difference.

Fig. 3.

Individual data representing the right first dorsal interosseous (RFDI) map area, short-interval interhemispheric inhibition (SIHI), and long-interval interhemispheric inhibition (LIHI) for each participant (P). The color labels on the top represent the coding of individual data seen in other figures. The legend on the left indicates the color code for each condition, as well as the relationship between color intensity and corticospinal excitability. MEP_max, maximum average motor-evoked potential amplitude obtained within the motor map. The color intensity scales with percentages of MEP_max. For example, grid points with the greatest color intensity represent MEPs obtained within 75–100% of the maximum average MEP. CoG, center of gravity; CONTRA, condition of right first dorsal interosseous (FDI) contraction; IPSI, condition of left FDI contraction.

Fig. 4.

The relationship between right first dorsal interosseous (FDI) muscle representation and short-interval interhemispheric inhibition (SIHI) and long-interval interhemispheric inhibition (LIHI). A: top: no significant correlation was observed between SIHI or LIHI and the right FDI representation at REST (top). A: middle: significant association between the depth of both SIHI and LIHI and the FDI representation was observed during condition of right FDI contraction (CONTRA). A: bottom: a significant association between the depth of both SIHI and LIHI and the right FDI representation was observed during IPSI. Each point is color coded for individual participant data. Correlation coefficients and P values are provided on the plots. B: the currently proposed model of the mechanism of IHI. IHI_INT, IHI inhibitory interneurons.

Fig. 5.

Shows the average (±SD) location of hotspot, center of gravity (CoG), and maximum motor-evoked potential (MEP_max) obtained within the map of the right first dorsal interosseous (FDI) muscle during the condition of REST, condition of right FDI contraction (CONTRA), and condition of left FDI contraction (IPSI). A two-way Conover’s ANOVA was performed in each condition to determine if the locations of hotspot, CoG, and the grid point that evoked the maximum MEP was distinct, using within-subject factors of LANDMARK (3 levels: hotspot, CoG, MEP_max) and PLANE (2 levels: location in medial-lateral direction, location in anterior-posterior direction). In the REST and IPSI conditions, there was a main effect of LANDMARK [REST, F_(2,28) = 6.148, P = 0.005; IPSI, F_(2,28) = 3.919, P = 0.032], such that the location of hotspot on the FDI map was significantly lateral and posterior to the location of CoG (Wilcoxon signed rank: REST, P = 0.005, d = 1.02; IPSI, P = 0.015, d = 1.12) and MEP_max (Wilcoxon signed rank: REST, P = 0.027, d = 0.68; IPSI, P = 0.036, d = 0.68). However, these 3 locations were not distinct from each other in the CONTRA condition (no main effects or interaction). *P < 0.05.