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Parieto-frontal mechanisms underlying observation of complex hand-object manipulation.

ABSTRACT: The observation of actions performed by others is believed to activate the Action Observation Network (AON). Previous evidence suggests that subjects with a specific motor skill show increased activation of the AON during observation of the same skill. The question arises regarding which modulation of the AON occurs during observation of novel complex manipulative actions that are beyond the personal motor repertoire. To address this issue, we carried out a functional MRI study in which healthy volunteers without specific hand motor skills observed videos displaying hand-object manipulation executed by an expert with high manual dexterity, by an actor with intermediate ability or by a naïve subject. The results showed that the observation of actions performed by a naïve model produced stronger activation in a dorso-medial parieto-premotor circuit including the superior parietal lobule and dorsal premotor cortex, compared to observation of an expert actor. Functional connectivity analysis comparing the observation of the naïve model with that of the expert model, revealed increased connectivity between dorsal areas of the AON. This suggests a possible distinction between ventral and dorsal brain circuits involved in the processing of different aspects of action perception, such as kinematics and final action goal.

SUBMITTER: Errante A

PROVIDER: S-EPMC6344645 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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Parieto-frontal mechanisms underlying observation of complex hand-object manipulation.

Errante Antonino A Fogassi Leonardo L

Scientific reports 20190123 1

The observation of actions performed by others is believed to activate the Action Observation Network (AON). Previous evidence suggests that subjects with a specific motor skill show increased activation of the AON during observation of the same skill. The question arises regarding which modulation of the AON occurs during observation of novel complex manipulative actions that are beyond the personal motor repertoire. To address this issue, we carried out a functional MRI study in which healthy ...[more]

PMID: 30674948

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Project description:The activity of frontal motor areas during hand-object interaction is coordinated by dense communication along specific white matter pathways. This architecture allows the continuous shaping of voluntary motor output but, despite extensive investigation in non-human primate studies, remains poorly understood in humans. Disclosure of this system is crucial for predicting and treatment of motor deficits after brain lesions. For this purpose, we investigated the effect of direct electrical stimulation on white matter pathways within the frontal lobe on hand-object manipulation. This was tested in 34 patients (15 left hemisphere, mean age 42 years, 17 male, 15 with tractography) undergoing awake neurosurgery for frontal lobe tumour removal with the aid of the brain mapping technique. The stimulation outcome was quantified based on hand-muscle activity required by task execution. The white matter pathways responsive to stimulation with an interference on muscles were identified by means of probabilistic density estimation of stimulated sites, tract-based lesion-symptom (disconnectome) analysis and diffusion tractography on the single patient level. Finally, we assessed the effect of permanent tract disconnection on motor outcome in the immediate postoperative period using a multivariate lesion-symptom mapping approach. The analysis showed that stimulation disrupted hand-muscle activity during task execution at 66 sites within the white matter below dorsal and ventral premotor regions. Two different EMG interference patterns associated with different structural architectures emerged: (i) an 'arrest' pattern, characterized by complete impairment of muscle activity associated with an abrupt task interruption, occurred when stimulating a white matter area below the dorsal premotor region. Local middle U-shaped fibres, superior fronto-striatal, corticospinal and dorsal fronto-parietal fibres intersected with this region. (ii) a 'clumsy' pattern, characterized by partial disruption of muscle activity associated with movement slowdown and/or uncoordinated finger movements, occurred when stimulating a white matter area below the ventral premotor region. Ventral fronto-parietal and inferior fronto-striatal tracts intersected with this region. Finally, only resections partially including the dorsal white matter region surrounding the supplementary motor area were associated with transient upper-limb deficit (P = 0.05; 5000 permutations). Overall, the results identify two distinct frontal white matter regions possibly mediating different aspects of hand-object interaction via distinct sets of structural connectivity. We suggest the dorsal region, associated with arrest pattern and postoperative immediate motor deficits, to be functionally proximal to motor output implementation, while the ventral region may be involved in sensorimotor integration required for task execution.

Project description:Many neuroimaging studies have demonstrated the different functional contributions of spatially distinct brain areas to working memory (WM) subsystems in cognitive tasks that demand both local information processing and interregional coordination. In WM cognitive task paradigms employing electroencephalography (EEG), brain rhythms such as θ and α have been linked to specific functional roles over given brain areas, but their functional coupling has not been extensively studied. Here we analyzed an arithmetic task with five cognitive workload levels (CWLs) and demonstrated functional/effective coupling between the two WM subsystems: the central executive located over frontal (F) brain areas that oscillates on the dominant θ rhythm (Frontal(θ)/F(θ)) and the storage buffer located over parieto-occipital (PO) brain areas that operates on the α2 dominant brain rhythm (Parieto-Occipital(α2)/PO(α2)). We focused on important differences between and within WM subsystems in relation to behavioral performance. A repertoire of brain connectivity estimators was employed to elucidate the distinct roles of amplitude, phase within and between frequencies, and the hierarchical role of functionally specialized brain areas related to the task. Specifically, for each CWL, we conducted a) a conventional signal power analysis within both frequency bands at F(θ) and PO(α2), b) the intra- and inter-frequency phase interactions between F(θ) and PO(α2), and c) their causal phase and amplitude relationship. We found no significant statistical difference of signal power or phase interactions between correct and wrong answers. Interestingly, the study of causal interactions between F(θ) and PO(α2) revealed frontal brain region(s) as the leader, while the strength differentiated between correct and wrong responses in every CWL with absolute accuracy. Additionally, zero time-lag between bilateral F(θ) and right PO(a2) could serve as an indicator of mental calculation failure. Overall, our study highlights the significant role of coordinated activity between F(θ) and PO(α2) via their causal interactions and the timing for arithmetic performance.

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Parieto-frontal mechanisms underlying observation of complex hand-object manipulation.

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Parieto-frontal mechanisms underlying observation of complex hand-object manipulation.

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