Transcranial Random Noise Stimulation Acutely Lowers the Response Threshold of Human Motor Circuits.

Transcranial random noise stimulation (tRNS) over cortical areas has been shown to acutely improve performance in sensory detection tasks. One explanation for this behavioral effect is stochastic resonance (SR), a mechanism that explains how signal processing in nonlinear systems can benefit from added noise. While acute noise benefits of electrical RNS have been demonstrated at the behavioral level as well as in in vitro preparations of neural tissue, it is currently largely unknown whether similar effects can be shown at the neural population level using neurophysiological readouts of human cortex. Here, we hypothesized that acute tRNS will increase the responsiveness of primary motor cortex (M1) when probed with transcranial magnetic stimulation (TMS). Neural responsiveness was operationalized via the well-known concept of the resting motor threshold (RMT). We showed that tRNS acutely decreases RMT. This effect was small, but it was consistently replicated across four experiments including different cohorts (total N = 81, 46 females, 35 males), two tRNS electrode montages, and different control conditions. Our experiments provide critical neurophysiological evidence that tRNS can acutely generate noise benefits by enhancing the neural population response of human M1.SIGNIFICANCE STATEMENT A hallmark feature of stochastic resonance (SR) is that signal processing can benefit from added noise. This has mainly been demonstrated at the single-cell level in vitro where the neural response to weak input signals can be enhanced by simultaneously applying random noise. Our finding that transcranial random noise stimulation (tRNS) acutely increases the excitability of corticomotor circuits extends the principle of noise benefits to the neural population level in human cortex. Our finding is in line with the notion that tRNS might affect cortical processing via the SR phenomenon. It suggests that enhancing the response of cortical populations to an external stimulus might be one neurophysiological mechanism mediating performance improvements when tRNS is applied to sensory cortex during perception tasks.

Muscle-specific modulation of indirect inputs to primary motor cortex during action observation.

Single-pulse transcranial magnetic stimulation (spTMS) studies report that movement observation facilitates corticospinal excitability in primary motor cortex (M1) in a muscle-specific manner. However, motor evoked potentials (MEPs) elicited by spTMS are known to reflect the summation of several descending volleys in corticospinal neurons which are evoked via mono- and polysynaptic inputs (so-called indirect waves or I-waves). It is unclear which of these components contribute to the muscle-specific modulation of M1 during action observation. The interactions between different I-waves are reflected in the facilitatory peaks elicited with a short-intracortical facilitation (SICF) protocol when two pulses are sent to M1 at precise intervals (i.e., 1.3, 2.5 or 4.1 ms). Here, we explored the modulation of early and late SICF peaks during action observation by measuring highly specific MEP amplitude changes measured in two muscles (index, FDI and little finger, ADM) while participants observed two different actions (precision and whole-hand grip). Our results demonstrate that both early (1.3 ms) and late (2.5 and 4.1 ms) SICF peaks are modulated in the context of movement observation. However, only the second peak (ISI 2.5 ms) was significantly associated with the muscle-specific modulation of corticospinal excitability as measured with spTMS. This late SICF peak is believed to reflect the activity cortico-cortical pathways involved in the facilitation of muscle-specific representations in M1. Thus, our findings suggest that movement observation leads to widespread activation of different neural circuits within M1, including those mediating cortico-cortical communication.

Uncertainty in contextual and kinematic cues jointly modulates motor resonance in primary motor cortex.

Contextual information accompanying others' actions modulates "motor resonance", i.e., neural activity within motor areas that is elicited by movement observation. One possibility is that we weigh and combine such information in a Bayesian manner according to their relative uncertainty. Therefore, contextual information becomes particularly useful when others' actions are difficult to discriminate. It is unclear, however, whether this uncertainty modulates the neural activity in primary motor cortex (M1) during movement observation. Here, we applied single-pulse transcranial magnetic stimulation (TMS) while subjects watched different grasping actions. We operationalized motor resonance as grip-specific modulation of corticomotor excitability measured in the index (FDI) versus the little finger abductor (ADM). We experimentally modulated either the availability of kinematic information ( experiment 1) or the reliability of contextual cues ( experiment 2). Our results indicate that even in the absence of movement kinematics, reliable contextual information is enough to trigger significant muscle-specific corticomotor excitability changes in M1, which are strongest when both kinematics and contextual information are available. These findings suggest that bottom-up mechanisms that activate motor representations as a function of the observed kinematics and top-down mechanisms that activate motor representations associated with arbitrary cues converge in M1. NEW & NOTEWORTHY Our study reveals new neurophysiological insights in support of the Bayesian account of action observation by showing that "motor resonance", i.e., neural activity evoked by observing others' actions, incorporates the uncertainty related to both contextual (prior beliefs) and kinematic (sensory evidence) cues. Notably, we show that muscle-specific modulation of M1 is strongest when context and movement kinematics are available, and it can be elicited even in the absence of movement kinematics.