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

Abstract

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.

Low or High-Level Motor Coding? The Role of Stimulus Complexity

“…No modulation of CSE resulted from AO in incongruent contexts. In a second study by Cretu et al (2019), participants observed either full or occluded videos of an actor grasping and lifting a jar using a precision or a whole-hand grip. Color cues preceded observation trials and were manipulated in terms of their informativeness in predicting the upcoming action.…”

Top-down contextual requirement to suppress self-movement influences grasp-specific modulation of corticospinal excitability during action observation

“…Another recent study comparably found that reliable contextual cues were sufficient to elicit muscle-specific CSE changes when visual kinematic cues were absent, and that CSE modulation was strongest when both contextual and kinematic cues were present 18 . In the authors' framework, M1 is the site of convergence for bottom-up kinematic cues regarding the actual observed action, presumably arriving via the parieto-frontal grasping circuitry which houses mirror neurons 34 , and top-down contextual cues or priors.…”

Reward modulates behaviour and neural responses in motor cortex during action observation

“…Stimuli were created by showing a series of three still shots from videos of a hand reaching, grasping and lifting a round jar (9 cm diameter, 14.5 cm height, 1.5 kg weight). These still shots were chosen from videos that were used previously (Cretu, Ruddy, Germann, & Wenderoth, 2019; de Beukelaar, Alaerts, Swinnen, & Wenderoth, 2016). In WHG all fingers were used to grasp the lid of the jar, whereas for the PG, only the thumb and index finger grasped a small knob mounted on the top of the jar.…”

“…From the EMG data, peak-to-peak amplitudes of the MEPs were calculated using custom-made Matlab scripts (Matlab 2015, Mathworks, Natick, MA, USA). Data preprocessing was done using the same criteria presented previously (Cretu et al, 2019). Shortly, the root mean square (rms) of background EMG in the period 110 to 10ms before the TMS pulses was calculated and MEPs with background rms higher than 10 μV were excluded.…”

“…Our method offers the advantage of extracting specific information regarding the neural tuning of action representations evoked by movement observation. This is essential when describing the functional role of action value during motor resonance (Alaerts, Senot, et al, 2010;Bunday et al, 2016;Cretu et al, 2019;de Beukelaar et al, 2016). We operationalized action-specific motor resonance as changes in corticomotor excitability as measured with single-pulse TMS simultaneously in the first dorsal interosseous (FDI) and the abductor digiti minimi (ADM) muscles when subjects observed whole-hand versus precision grip actions.…”