Time‐varying enhancement of human cortical excitability mediated by cutaneous inputs during precision grip.

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Abstract
1. We have investigated the afferent neurogram, muscular activity and mechanical responses while subjects restrained, with a precision grip, an object subjected to pulling loads directed away from the hand. At unpredictable times 'ramp-and-hold' loads of 1 N were delivered at a rate of ca 80 N s-1. The load ramp produced a sharp increase in multiunit activity recorded from cutaneous afferents of the median nerve. The first response in the EMG of distal hand muscles commenced at 51 +/- 2.4 ms (mean +/- S.D.); a further steep increase in activity began about 20 ms later, and this was associated with a marked augmentation of the grip force increase. 2. In four subjects, transcranial magnetic stimulation (TMS) was delivered to the contralateral motor cortex in 1000 out of a total of 1500 loading trials. The time of the stimulus was randomly selected to occur either at one of nine defined points (separated by 20 ms) before and after the computer command triggering the load force increase, or during steady periods of grip. 3. In most hand and arm muscles, there was a powerful facilitation of the short-latency EMG responses evoked by TMS delivered 40-140 ms after the load force command. The amplitudes of the largest responses (TMS delivered at 80-100 ms) were 850% higher on average than those observed when subjects gripped the unloaded object or when they restrained the statically loaded object. This large modulation was only obtained with stimulus intensities that were subthreshold in the relaxed subject. 4. The modulation was not simply a reflection of the time-varying level of motoneuronal activity during the loading trial. In most muscles, changes in the amplitude of the TMS-evoked responses were disproportionately larger than the corresponding modulation of the background EMG activity. At its maximum, the modulation in the TMS-evoked response was nearly 300% larger. Furthermore, the strength of the TMS-evoked responses did not strictly co-vary with amplitude of background EMG, i.e. inverse relationships were seen. 5. Since motor responses to the loading of the object depend on cutaneous afferent input from the gripping digits, the results demonstrate an interaction between the effects of these inputs and those of TMS. A possible site of this interaction is the primary motor cortex; the strong modulation of the responses to TMS could reflect variation in the excitability of cortical neurons mediated by the cutaneous afferent input. However, such excitability changes lagged the predicted onset of cortical excitation in a manner suggesting that the earliest 20 ms of the subjects' EMG responses to the load increase are subcortical in origin. In contrast, the results are consistent with a cortical mediation of the subsequent powerful boosting of the EMG responses associated with the robust grip force response.

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