Surround inhibition in the motor system

Abstract

Surround inhibition is a physiological mechanism to focus neuronal activity in the central nervous system. This so-called center-surround organization is well known in sensory systems, where central signals are facilitated and eccentric signals are inhibited in order to sharpen the contrast between them. There is evidence that this mechanism is relevant to skilled motor behavior, and it is deficient, for example, in the affected primary motor cortex of patients with focal hand dystonia (FHD). While it is still not fully elucidated how surround inhibition is generated in healthy subjects, the process is enhanced with handedness and task difficulty indicating that it may be an important mechanism for the performance of individuated finger movements. In FHD, where involuntary overactivation of muscles interferes with precise finger movements, a loss of intracortical inhibition likely contributes to the loss of surround inhibition. Several intracortical inhibitory networks are modulated differently in FHD compared with healthy subjects, and these may contribute to the loss of surround inhibition. Surround inhibition can be observed and assessed in the primary motor cortex. It remains unclear, however, if the effects are created in the cortex or if they are derived from, or supported by, motor signals that come from the basal ganglia.

Figure 1

(from Mink et al. 1996): Relationship of GPi activity to inputs from striatum and subthalamic nucleus. During voluntary movement, excitatory subthalamopallidalneurons increase the activity of the pallidal neurons in the territory surrounding a functional center. Inhibitory striatopallidal neurons inhibit the functional center, resulting in a focused output pattern. The pallidal activity changes are conveyed to the targets in thalamus (VLo) and midbrain (MEA), causing disinhibition of neurons involved in the desired motor program and inhibition of surrounding neurons involved in competing motor programs. Abbreviations — GPi: globus pallidus, pars interna; MEA: midbrain extrapyramidal area; STN: subthalamic nucleus; VLO: ventral lateral thalamic nucleus, pars oralis. Excitatory projections are indicated with open arrows inhibitory projections are indicated with filled arrows. Relative magnitude of activity is represented by line thickness.

Fig. 2

(from Beck et al. 2008). MEP size in FDI (Wrst dorsal interosseus muscle, synergist muscle). Shown are the mean MEP sizes with SEs in FDI during movement in both groups (FHD patients and controls) during the four phases. MEP size shows an increase for all active tasks compared with rests underlining the muscle’s active role in the selected movement. There was no diVerence in modulation between FHD patients and controls (*P < 0.05, **P < 0.01, ***P < 0.005)

Figure 3. (from Beck et al. 2008)

MEP size in APB (abductor pollicis brevis muscle, surrounding muscle). Shown are the mean MEP sizes with SEs in APB during the FDI (first dorsal interosseus muscle) movement for both groups (FHD patients and controls) during the four phases of the movement. 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 4. (from Beck et al. 2008)

SICI (short intracortical inhibition) 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. (from Quartarone et al. 2003)

Effect of associative stimulation (AS) on the size of motor evoked potentials (MEPs) of the right APB and FDI muscle in 10 healthy controls (A) and 10 patients with writer’s cramp (B). The bar chart illustrate the mean peak-to-peak amplitude (mV) of MEPs recorded at rest before (open columns) and after (shaded columns) associative stimulation. Each error bar equals SEM. Associative stimulation led to an increase in MEP size in patients and controls. However, the facilitatory effect was significantly stronger and less focal in patients.