Differential effect of muscle vibration on intracortical inhibitory circuits in humans

Abstract

Low amplitude muscle vibration (0.5 ms; 80 Hz; duration 1.5 s) was applied in turn to each of three different intrinsic hand muscles (first dorsal interosseus, FDI; abductor pollicis brevis, APB; and abductor digiti minimi, ADM) in order to test its effect on the EMG responses evoked by transcranial magnetic stimulation (TMS). Recordings were also taken from flexor and extensor carpi radialis (FCR and ECR, respectively). We evaluated the amplitude of motor evoked potentials (MEPs) produced by a single TMS pulse, short interval intracortical inhibition and facilitation (SICI and ICF) and long interval intracortical inhibition (LICI). TMS pulses were applied 1 s after the start of vibration with subjects relaxed throughout. Vibration increased the amplitude of MEPs evoked in the vibrated muscle (162 +/- 6 % of MEP with no vibration; mean +/- S.E.M.), but suppressed MEPs in the two non-vibrated hand muscles (72 +/- 9 %). Compared with no vibration (test response reduced to 51 +/- 5 % of control), there was less SICI in the vibrated muscle (test response reduced to 92 +/- 28 % of control) and more in the non-vibrated hand muscles (test response reduced to 27 +/- 5 % of control). The opposite occurred for LICI: compared with the no vibration condition (test response reduced to 33 +/- 6 % control), there was more LICI in the vibrated muscle (test response reduced to 17 +/- 3 % control) than in the non-vibrated hand muscles (test response reduced to 80 +/- 11 % control) even when the intensity of the test stimulus was adjusted to compensate for the changes in baseline MEP. There was no effect on ICF. Cutaneous stimulation of the index finger (80 Hz, 1.5 s duration, twice sensory threshold) had no consistent differential effect on any of the parameters. We conclude that vibratory input from muscle can differentially modulate excitability in motor cortical circuits.

Figure 1. MEPs in response to single TMS stimuli (rest SI 1 mV) in all vibration conditions

A, average MEP recordings showing the effect of vibration in three hand muscles from one representative subject. MEPs from all hand muscles are shown at rest (baseline) and during vibration of each muscle in turn. MEPs in a muscle were facilitated when the muscle itself was vibrated, but suppressed during vibration of a different hand muscle. B, mean MEP amplitudes (± s.e.m.) obtained with SI 1 mV during vibration of the FDI (vib FDI), APB (vib APB) or ADM (vib ADM) expressed as percentage of MEP size at rest. The MEPs increased in the vibrated muscle, whereas they decreased in the non-vibrated hand muscles. Asterisks indicate statistically significant differences from baseline without vibration (paired t test; *P < 0.05; **P < 0.01).

Figure 2. Short latency intracortical inhibition (SICI) and facilitation (ICF) in the FDI with and without vibration of FDI, APB or ADM muscles

A and B show the raw data of MEP amplitude obtained with (A) constant (SI 1 mV; open symbols) and (B) adjusted (ADJ- SI 1 mV; filled symbols) test pulse intensity. The different symbols indicate data collected without vibration of any muscle (♦), with vibration of FDI (▪, ▪), with vibration of APB (▵, ▴) and with vibration of ADM (○, •). On the x-axis, ‘test’ indicates the size of response to test stimulus alone, ISI 2 ms, 3 ms, 4 ms, etc. indicates the size of responses preceded by conditioning pulses at the intervals indicated. C and D show the same data expressed as percentages of the test values. SICI (ISI 2, 3 and 4 ms) decreases with vibration of the FDI (target muscle), but increases with vibration of APB and ADM. The effect on ICF (ISI 10 and 15 ms) is not clear. E, the pooled data from C and D, with data points at ISIs of 2, 3 and 4 ms averaged to yield a mean value for SICI, and data points from ISIs of 10 and 15 ms averaged to yield a mean value for ICF. Data are means ± s.e.m. Asterisks indicate statistically significant differences from baseline without vibration (paired t test; *P < 0.001).

Figure 3. SICI and ICF in APB and ADM with and without vibration of different hand muscles

The graphs are equivalent to those in Fig. 2E and show data collected simultaneously from APB (top) and ADM (bottom). The bars plot SICI and ICF with no vibration and with vibration of FDI, APB or ADM. As in Fig. 2E, data obtained with test intensities of SI 1 mV and ADJ-SI 1 mV have been pooled since they were not significantly different. Both hand muscles show the same pattern of changes as seen in the FDI: SICI is reduced by vibration of the muscle itself, whereas it increases during vibration of another hand muscle. The effect on ICF is not clear. Data are means ± s.e.m. Asterisks indicate statistically significant differences from baseline without vibration (paired t test; *P < 0.005).

Figure 4. LICI in the FDI, APB and ADM with and without hand muscle vibration

LICI is expressed as the mean (± s.e.m.) percentage of conditioned MEP amplitude/test MEP amplitude for the conditions with and without vibration. Data obtained with the two different test intensities are shown in A; since the results were not significantly different, the data were pooled as shown in B. The effect of vibration was similar in all three hand muscles: LICI increased during vibration of the muscle itself and decreased during vibration of remote hand muscles. All changes during vibration as shown in B were significantly different from the baseline obtained without vibration (paired t test; P < 0.05).

Figure 5. Single MEPs, SICI and ICF obtained with digital nerve stimulation

A, mean (± s.e.m.) MEPs in response to single TMS pulses during stimulation of the digital nerves of the index finger (SI 1 mV) expressed as percentages of baseline values without stimulation. Index finger stimulation had no significant effect on the size of any MEP, although there was a tendency for MEPs to be smaller in the APB and larger in the ADM. B, normalized MEP amplitudes obtained with both test pulse intensities. The different symbols indicate data collected without digital nerve stimulation (♦) and with digital nerve stimulation and test pulse intensities of SI 1 mV (▪) and ADJ-SI 1 mV (▴). C, SICI (mean of ISI 2, 3 and 4 ms as percentage of test MEP size ± s.e.m.) at rest and during index finger stimulation. Index finger stimulation reduced SICI in all three muscles to the same extent. D, ICF (mean of ISI 10 and 15 ms as percentage of test MEP size ± s.e.m.) at rest and with index finger stimulation. Stimulation increased ICF in APB, but had no effect in other muscles. C and D show pooled data obtained with test stimulus intensities of SI 1 mV and ADJ-SI 1 mV since the individual results from each intensity were not different from each other. Asterisks indicate values significantly different from the baseline without index finger stimulation (paired t test; *P < 0.01).

Figure 6. Interpretation of the main results of the present experiments

The three vertical modules represent motor cortex output zones that project to the three hand muscles studied. Each module consists of a notional output cell (the large open circle) with three different inputs: an excitatory input (open neurone) and two inhibitory inputs (grey and black neurones). The latter two represent the circuits involved in SICI and LICI. Vibratory input causes a change in the pattern of excitability in the circuits responsible for SICI and LICI. Neurones filled with black have increased excitability compared to rest whereas those filled with grey have decreased excitability compared to rest. Thus vibration increases LICI to the module that projects to the vibrated muscle and decreases SICI. It has the opposite effect on the two non-vibrated muscles. The net result of this on cortical processing is illustrated by the grey vertical arrows. The top three arrows represent equal input to the three cortical output zones. The bottom arrows show that the pattern of SICI changes would tend to increase the contrast in the final output between vibrated and non-vibrated muscle. This could contribute, for example, to explaining why MEPs are larger compared with rest in the vibrated muscle and smaller in the non-vibrated muscle.