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.

Keywords: Action observation; LFP; Mirror neurons; Motor system; Mu rhythm.

Figure 1

Tasks. A) Grasping execution task (ET). A-I) The monkey has his right hand at rest on the starting handle for at least 1000ms (baseline). A transparent barrier is in place between the monkey and the target object. A-II) The barrier is removed (go signal). The monkey is reaching and grasping the target object; A-III) The monkey places the object in the container; A-IV) A liquid reward is delivered if the task is successfully executed. B) Grasping observation task (OT). B-I) The agent and the monkey have their hands in the starting position; B-II) The monkey fixates the target object; B-III) The agent grasps the object; B-IV) The monkey receives a liquid reward if the trial is correctly executed.

Figure 2

Simultaneous recording of EEG from scalp electrodes, and of MUA and LFP from a linear multielectrode array (LMA) during grasping execution (ET) and observation (OT). A) Schematic view of the monkey head with approximate position of scalp electrodes and single-unit recording chamber. In inset, diagram of LMA layout indicating relative electrode depth. B) Spectrograms of the EEG signal recorded from seven different sites on the scalp. Yellow and red colors denote significant power increase (synchronization), while blue color shows significant power decrease (desynchronization). Green color denotes not significant variations. In inset: enlarged view of two EEG spectrograms. C) Spectrograms of LFPs (color map) and MUA histograms (black line) recorded at different electrodes. In inset: enlarged view of two LFP spectrograms/MUA histograms. For all graphs the activity is aligned with the hand contact with the target object during grasping (indicated by the vertical dashed line at time = 0). The horizontal dashed lines separate the frequency bands of interest (from top to bottom: high gamma – not showed for EEG, low gamma, beta and alpha).

Figure 3.

Spike-Triggered Time-Frequency Average (STTFA). The color maps represent the averaged PSD of the LFPs time-aligned with neuronal spike emission (time = 0). Yellow and red colors represent significant PSD increase (i.e. direct correlation PSD-spike emission), while blue color denotes significant PSD decrease (i.e. inverse correlation PSD-spike emission). p values <0.01.

Figure 4.

Maps of Pearson’s correlation coefficients calculated between the LFP high gamma band, recorded at each microelectrode, and the EEG alpha and beta bands desynchronization, recorded at each EEG scalp location. The significance thresholds are in the yellow color range for ET and in the green color range for OT. p values <0.05.

Figure 5.

Mean latency (in milliseconds +/− SEM) between the onset time of EEG desynchronization and LFP power increase.

Figure 6.

Histological assessment. (A) Lateral view drawing of the macaque brain; the dashed line indicates the level at which the coronal section, shown in B, was taken. (B) Coronal section drawing where the dashed box indicates the location of the photomicrograph shown in C. (C) Photomicrograph of the Nissl-stained section. (D) Schematic drawing of the linear multielectrode array (LMA) superimposed on a high magnification view of the cytoarchitectonic area F5c. The location of the photomicrograph is indicated by the dashed box in the photomicrograph shown in C. Roman numerals correspond to the different cortical layers. White squares indicate the relative depth (in μm) of the LMA electrodes. C, central sulcus; Cg, cingulate sulcus; IA, inferior arcuate sulcus; IP, intraparietal sulcus; L, lateral sulcus; Lu, lunate sulcus; P, principal sulcus; SA, superior arcuate sulcus; ST, superior temporal sulcus.