Action Observation and Execution Differentially Modulate Basal Ganglia-Cortical Activity in Humans

Abstract INTRODUCTION To understand an observed action, without overt execution, the observer is thought to run similar motor plans; indicating a strong coupling between the neural representation of action observation and execution. Imaging studies show activation of basal ganglia (BG) and motor cortex during movement yet comparative studies using direct and invasive human recordings are sparse. We aimed to characterize how movement execution and observation differentially modulate local and inter-regional activity across BG and sensorimotor cortex. METHODS We recorded LFP from globus palidus internus (GPi) and electrocorticography from ipsilateral sensorimotor cortex in 9 PD subjects during deep brain stimulation surgery. Subjects performed block design tasks alternating between 30 s of rest and performing or observing finger tapping with random order. We assessed changes in spectral power, along with pallidocortical coherence and cortical PAC. RESULTS We observed suppression of alpha-beta (9-25 Hz) power in contralateral GPi and sensorimotor cortex during both activities. This power suppression was significantly weaker in the motor cortex during the action observation compared to the execution (P = .02). However pallidal spectral changes in alpha-beta frequencies were not different across tasks (P = .3). Uniquely during the action execution, there was a significant increase in the gamma power (80-200 Hz) at the motor cortex (P < .05). In addition, Pallidocortical beta coherence, and motor cortical beta-gamma PAC were significantly suppressed during action execution (P < .05) and not the observation. CONCLUSION Our results support the functional dissociation within the BG-cortical network during action observation and execution. Although spectral power changes in a-ß in the BG are largely similar across tasks, suppression of BG-cortical functional connectivity is a feature of movement execution. In addition, increase in the cortical gamma power and beta-gamma phase amplitude decoupling only happen during the movement execution, in line with the theory that during movement execution the gamma signal is released from the constraint of beta.

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Movement-related changes in pallidocortical synchrony differentiate action execution and observation in humans

10.1101/2020.05.27.117416 ◽

2020 ◽

Author(s):

Katy A. Cross ◽

Mahsa Malekmohammadi ◽

Jeong Woo Choi ◽

Nader Pouratian

Keyword(s):

Parkinson Disease ◽

Globus Pallidus ◽

Action Observation ◽

Phase Coupling ◽

Movement Execution ◽

Action Execution ◽

Beta Power ◽

Alpha Beta ◽

Motor Cortical ◽

Phase Amplitude

AbstractSuppression of local and network alpha (8-12 Hz) and beta (12-35 Hz) oscillations in the human basal ganglia-thalamocortical (BGTC) circuit is a prominent feature of movement. Local alpha/beta power, cross-region beta phase coupling, and phase-amplitude coupling (PAC) have all been shown to be suppressed during movement in multiple nodes of the BGTC. However, the specificity of these various movement-related changes to actual movement execution remains poorly understood. To differentiate signals that are specifically related to movement execution, we compared changes in globus pallidus internus (GPi) and motor cortical local oscillatory activity and coupling (cross-region phase coupling and local PAC) during movement execution and movement observation in 12 patients with Parkinson disease undergoing deep brain stimulator implantation. We hypothesized that network coupling is more directly related to movement execution than local power changes, given the putative role of pathological network coupling in movement disorders such as Parkinson disease. We observed suppression of alpha/beta power during action observation and execution in the globus pallidus and motor cortex during both action execution and action observation. In contrast, pallidocortical coherence and GPi and motor cortical alpha/beta-gamma PAC were significantly suppressed only during action execution. Our results demonstrate a functional dissociation within the BG-cortical network during action execution and observation in which suppression of BG-cortical functional connectivity and local phase amplitude coupling are features specifically of overt movement, suggesting a particularly important role in motor execution. This has implications for identification and use of intracranial signals for closed loop brain stimulation therapies.

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Alpha/beta power decreases during episodic memory formation predict the magnitude of alpha/beta power decreases during subsequent retrieval

10.1101/2020.07.08.193763 ◽

2020 ◽

Author(s):

Benjamin J. Griffiths ◽

María Carmen Martín-Buro ◽

Bernhard P. Staresina ◽

Simon Hanslmayr ◽

Tobias Staudigl

Keyword(s):

Episodic Memory ◽

Memory Retrieval ◽

Spectral Power ◽

Learning Task ◽

Neural Representation ◽

Parameter Estimates ◽

Beta Activity ◽

Amount Of Information ◽

Beta Power ◽

Alpha Beta

AbstractEpisodic memory retrieval is characterised by the vivid reinstatement of information about a personally-experienced event. Growing evidence suggests that the reinstatement of such information is supported by reductions in the spectral power of alpha/beta activity. Given that the amount of information that can be recalled depends on the amount of information that was originally encoded, information-based accounts of alpha/beta activity would suggest that retrieval-related alpha/beta power decreases similarly depend upon decreases in alpha/beta power during encoding. To test this hypothesis, seventeen human participants completed a sequence-learning task while undergoing concurrent MEG recordings. Regression-based analyses were then used to estimate how alpha/beta power decreases during encoding predicted alpha/beta power decreases during retrieval, on a trial-by-trial basis. When subjecting these parameter estimates to group-level analysis, we find evidence to suggest that retrieval-related alpha/beta (7-15Hz) power decreases fluctuate as a function of encoding-related alpha/beta power decreases. These results suggest that retrieval-related alpha/beta power decreases are contingent on the decrease in alpha/beta power that arose during encoding. Subsequent analysis uncovered no evidence to suggest that these alpha/beta power decreases reflect stimulus identity, indicating that the contingency between encoding- and retrieval-related alpha/beta power reflects the reinstatement of a neurophysiological operation, rather than neural representation, during episodic memory retrieval.

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Moving Mirrors: A High-density EEG Study Investigating the Effect of Camera Movements on Motor Cortex Activation during Action Observation

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00602 ◽

2014 ◽

Vol 26 (9) ◽

pp. 2087-2101 ◽

Cited By ~ 23

Author(s):

Katrin Heimann ◽

Maria Alessandra Umiltà ◽

Michele Guerra ◽

Vittorio Gallese

Keyword(s):

Social Cognition ◽

Motor Cortex ◽

Time Course ◽

Action Observation ◽

High Density ◽

Human Observer ◽

Mu Rhythm ◽

Fixed Position ◽

Action Execution ◽

The One

Action execution–perception links (mirror mechanism) have been repeatedly suggested to play crucial roles in social cognition. Remarkably, the designs of most studies exploring this topic so far excluded even the simplest traces of social interaction, such as a movement of the observer toward another individual. This study introduces a new design by investigating the effects of camera movements, possibly simulating the observer's own approaching movement toward the scene. We conducted a combined high-density EEG and behavioral study investigating motor cortex activation during action observation measured by event-related desynchronization and resynchronization (ERD/ERS) of the mu rhythm. Stimuli were videos showing a goal-related hand action filmed while using the camera in four different ways: filming from a fixed position, zooming in on the scene, approaching the scene by means of a dolly, and approaching the scene by means of a steadycam. Results demonstrated a consistently stronger ERD of the mu rhythm for videos that were filmed while approaching the scene with a steadycam. Furthermore, videos in which the zoom was applied reliably demonstrated a stronger rebound. A rating task showed that videos in which the camera approached the scene were felt as more involving and the steadycam was most able to produce a visual experience close to the one of a human approaching the scene. These results suggest that filming technique predicts time course specifics of ERD/ERS during action observation with only videos simulating the natural vision of a walking human observer eliciting a stronger ERD than videos filmed from a fixed position. This demonstrates the utility of ecologically designed studies for exploring social cognition.

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The Activation of the Mirror Neuron System during Action Observation and Action Execution with Mirror Visual Feedback in Stroke: A Systematic Review

Neural Plasticity ◽

10.1155/2018/2321045 ◽

2018 ◽

Vol 2018 ◽

pp. 1-14 ◽

Cited By ~ 20

Author(s):

Jack J. Q. Zhang ◽

Kenneth N. K. Fong ◽

Nandana Welage ◽

Karen P. Y. Liu

Keyword(s):

Motor Cortex ◽

Visual Feedback ◽

Primary Motor Cortex ◽

Mirror Neuron System ◽

Action Observation ◽

Mirror Neuron ◽

Action Execution ◽

Neuron System ◽

Mu Suppression ◽

Mirror Visual Feedback

Objective. To evaluate the concurrent and training effects of action observation (AO) and action execution with mirror visual feedback (MVF) on the activation of the mirror neuron system (MNS) and its relationship with the activation of the motor cortex in stroke individuals. Methods. A literature search using CINAHL, PubMed, PsycINFO, Medline, Web of Science, and SCOPUS to find relevant studies was performed. Results. A total of 19 articles were included. Two functional magnetic resonance imaging (fMRI) studies reported that MVF could activate the ipsilesional primary motor cortex as well as the MNS in stroke individuals, whereas two other fMRI studies found that the MNS was not activated by MVF in stroke individuals. Two clinical trials reported that long-term action execution with MVF induced a shift of activation toward the ipsilesional hemisphere. Five fMRI studies showed that AO activated the MNS, of which, three found the activation of movement-related areas. Five electroencephalography (EEG) studies demonstrated that AO or MVF enhanced mu suppression over the sensorimotor cortex. Conclusions. MVF may contribute to stroke recovery by revising the interhemispheric imbalance caused by stroke due to the activation of the MNS. AO may also promote motor relearning in stroke individuals by activating the MNS and motor cortex.

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Early-onset cortico-cortical synchronization in the hemiparkinsonian rat model

Journal of Neurophysiology ◽

10.1152/jn.00690.2014 ◽

2015 ◽

Vol 113 (3) ◽

pp. 925-936 ◽

Cited By ~ 12

Author(s):

B. N. Jávor-Duray ◽

M. Vinck ◽

M. van der Roest ◽

A. B. Mulder ◽

C. J. Stam ◽

...

Keyword(s):

Basal Ganglia ◽

Motor Cortex ◽

Granger Causality ◽

Subthalamic Nucleus ◽

Spectral Power ◽

Field Potential ◽

Cell Loss ◽

Oscillatory Activity ◽

Connectivity Pattern ◽

Phase Lag

Changes in synchronized neuronal oscillatory activity are reported in both cortex and basal ganglia of Parkinson's disease patients. The origin of these changes, in particular their relationship with the progressive nigrostriatal dopaminergic denervation, is unknown. Therefore, in the present study we studied interregional neuronal synchronization in motor cortex and basal ganglia during the development of dopaminergic degeneration induced by a unilateral infusion of 6-hydroxydopamine (6-OHDA) into the rat medial forebrain bundle. We performed serial local field potential recordings bilaterally in the motor cortex and the subthalamic nucleus of the lesioned hemisphere prior to, during, and after development of the nigrostriatal dopaminergic cell loss. We obtained signal from freely moving rats in both resting and walking conditions, and we computed local spectral power, interregional synchronization (using phase lag index), and directionality (using Granger causality). After neurotoxin injection the first change in phase lag index was an increment in cortico-cortical synchronization. We observed increased bidirectional Granger causality in the beta frequency band between cortex and subthalamic nucleus within the lesioned hemisphere. In the walking condition, the 6-OHDA lesion-induced changes in synchronization resembled that of the resting state, whereas the changes in Granger causality were less pronounced after the lesion. Considering the relatively preserved connectivity pattern of the cortex contralateral to the lesioned side and the early emergence of increased cortico-cortical synchronization during development of the 6-OHDA lesion, we suggest a putative compensatory role of cortico-cortical coupling.

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The extended features of mirror neurons and the voluntary control of vocalization in the pathway to language

Language and Cognition ◽

10.1515/langcog-2013-0009 ◽

2013 ◽

Vol 5 (2-3) ◽

pp. 145-155 ◽

Cited By ~ 14

Author(s):

Leonardo Fogassi ◽

Gino Coudé ◽

Pier Francesco Ferrari

Keyword(s):

Motor Cortex ◽

Mirror Neurons ◽

Action Observation ◽

Mirror System ◽

Voluntary Control ◽

Action Execution ◽

Action Sequences ◽

Neurophysiological Data ◽

Action Goals

AbstractIn this book it has been proposed that the mirror system can be a scaffold for building a language-ready brain, because of its property of matching action observation with action execution, a feature that can correspond to the “parity” requirement for communication. In this commentary we will first emphasize two properties of mirror neurons and motor cortex that may have contributed to language: the generalization of the property of understanding action goals and the capacity to decode the goal of action sequences. Then we will propose, based on recent behavioural and neurophysiological data in monkeys, that the vocalization in non-human primates could have reached a partial voluntary control, thus contributing to the emergence of a communicative system relying on the coordination of gestures and utterances.

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