Short intracortical and surround inhibition are selectively reduced during movement initiation in focal hand dystonia

Abstract

In patients with focal hand dystonia (FHD), pathological overflow activation occurs in muscles not involved in the movement. Surround inhibition is a neural mechanism that can sharpen desired movement by inhibiting unwanted movement in adjacent muscles. To further establish the phenomenon of surround inhibition and to determine whether short intracortical inhibition (SICI) reflecting inhibition from the local interneurons in primary motor cortex (M1), might play a role in its genesis, single- and paired-pulse transcranial magnetic stimulation (TMS), and Hoffmann reflex testing were applied to evaluate the excitability of the relaxed abductor pollicis brevis muscle (APB) at various intervals during a movement of the index finger in 16 patients with FHD and 20 controls. Whereas controls showed inhibition of APB motor-evoked potential (MEP) size during movement initiation and facilitation of APB MEP size during the maintenance phase, FHD patients did not modulate APB MEP size. In contrast, SICI remained constant in controls, but FHD patients showed reduced SICI during movement initiation. The H(max)/M(max) ratio in control subjects increased during movement initiation. The results provide additional evidence for the presence of surround inhibition in M1, where it occurs only during movement initiation, indicating that different mechanisms underlie movement initiation and maintenance. Thus, surround inhibition is sculpted both in time and space and may be an important neural mechanism during movement initiation to counteract increased spinal excitability. SICI may contribute to its generation, because in patients with FHD, the lack of depression of APB MEP size is accompanied by a reduction in SICI.

Figure 1.

A, Experimental setup. Two pairs of surface electrodes were placed over the FDI and APB of the right hand, which is shown resting on a board. The tip of the index finger is resting on the force transducer. B, Time course of the task. Shown are the acoustic signal, which starts 200 ms after the begin of the recording, EMG in the FDI, the synergistic muscle, EMG in the APB, the surrounding muscle, and the forced produced. Stimuli were applied before the onset of the tone (rest, after 100 ms), during the premotor phase (20 ms before the onset of EMG in the FDI), the phasic phase (at the first peak of EMG in the FDI), and the tonic phase (1600 ms after the onset of the acoustic signal, maintenance phase of the contraction, steady state). C, Background EMG. Shown are the background EMG levels for the APB and FDI in all four different phases. Although there is no significant modulation of background EMG in APB, the EMG signal increases for the phasic and tonic phases in the FDI, reflecting its activation during the task. **p < 0.01; ***p < 0.005.

Figure 2.

MEP size in APB. Shown are the mean MEP sizes with SEs in APB during the FDI movement for both groups (FHD patients and controls) during the four phases. Whereas the MEP size shows a clear inhibition just before and during the first phase of EMG onset in the adjacent muscle (FDI), there is an enhancement during the tonic contraction. Both modulations are not observable in the FHD patient group. *p < 0.05; **p < 0.01; ***p < 0.005.

Figure 3.

MEP size in FDI. Shown are the mean MEP sizes with SEs in FDI during movement for both groups (FHD patients and controls) during the four phases. MEP size shows an increase for all active tasks compared with rest underlining its active role in the selected movement. There was no difference in modulation between FHD patients and controls. *p < 0.05; **p < 0.01; ***p < 0.005.

Figure 4.

SICI is shown as group mean percentage change [SICI = (MEP test − MEP conditioned/MEP test) × 100] with SEs. For the rest condition and tonic state, there is no difference between FHD patients and controls. For patients, SICI is reduced during premotor and phasic phases of the adjacent FDI contraction. In the control group, SICI shows no phase-specific modulation. **p < 0.01; ***p < 0.005.

Figure 5.

The graph shows mean and SE of the H_max/M_max ratios assessed in six young healthy volunteers. The H_max/M_max ratio is increased during the initiation phase of FDI contraction and returns to baseline during the tonic contraction phase. *p < 0.05.