Simultaneous scalp recorded EEG and local field potentials from monkey ventral premotor cortex during action observation and execution reveals the contribution of mirror and motor neurons to the mu-rhythm

Abstract

The desynchronization of alpha and beta oscillations (mu rhythm) in the central scalp EEG during action observation and action execution is thought to reflect neural mirroring processes. However, the extent to which mirror neurons (MNs) or other populations of neurons contribute to such EEG desynchronization is still unknown. Here, we provide the first evidence that, in the monkey, the neuronal activity recorded from the ventral premotor cortex (PMv) strongly contributes to the EEG changes occurring in the beta band over central scalp electrodes, during executed and observed actions. We simultaneously recorded scalp EEG and extracellular activity, Multi Unit Activity (MUA) and Local Field Potentials (LFP), from area F5 of two macaques executing and observing grasping actions. We found that MUA highly correlates with an increase in high gamma LFP power and, interestingly, such LFP power increase also correlates to EEG beta - and in part also to alpha - desynchronization. In terms of timing of signal changes, the increase in high gamma LFP power precedes the EEG desynchronization, during both action observation and execution, thus suggesting a causal role of PMv neuronal activity in the modulation of the alpha and beta mu-rhythm. Lastly, neuronal signals from deeper layers of PMv exert a greater contribution than superficial layers to the EEG beta rhythm modulation, especially during the motor task. Our findings have clear implications for EEG studies in that they demonstrate that the activity of different populations of neurons in PMv contribute to the generation of the mu-rhythm.

A causal role for frontal cortico-cortical coordination in social action monitoring

“…This suppression has been hypothesized to reflect mirror neuron activity 7 , 40 and can be weakened or absent in people with ASD 7 , 41 . In macaques, similar phenomena, but in higher frequency bands, were consistently reported in the PMv 42 – 45 , whereas possible contributions of the MPFC to mu suppression have not been reported. Here we confirmed in the RA condition that LFP power in the high-beta band (23–30 Hz; black arrows in Fig.…”

Developmental trajectory of interpersonal motor alignment: Positive social effects and link to social cognition

“…This is also evidenced in indirect electrophysiological measures of brain activity using electro- or magneto-encephalography (EEG and MEG), which show the same signature of brain activity, namely a decrease in power in mu (8−13 Hz), and often also beta (15−20 Hz), frequency bands over the motor cortex (central electrodes) for both action execution and observation (for review see Marshall and Meltzoff, 2011 ). Experiments in non-human primates indicate that the mu rhythm would reflect activity of motor and mirror neurons ( Bimbi et al, 2018 ).…”

The role of the motor system in action understanding and communication: Evidence from human infants and non‐human primates

“…Over the past decade or so there has been an uptick in developmental research utilizing mu rhythm desynchronization (see Cuevas, Cannon, Yoo, & Fox, ; Marshall & Meltzoff, for reviews). Work with non‐human primates has also provided evidence that the EEG mu rhythm is a valid measure of the MNS across species (Bimbi et al, ; Coudé et al, ; Vanderwert et al, ).…”