Brain activation during processing of mouth actions in patients with disorders of consciousness.

action observation action verbs disorders of consciousness fMRI mirror neuron system

Journal

Brain communications
ISSN: 2632-1297
Titre abrégé: Brain Commun
Pays: England
ID NLM: 101755125

Informations de publication

Date de publication:
2024
Historique:
received: 14 07 2023
revised: 12 01 2024
accepted: 14 02 2024
medline: 4 3 2024
pubmed: 4 3 2024
entrez: 4 3 2024
Statut: epublish

Résumé

In the past 2 decades, several attempts have been made to promote a correct diagnosis and possible restorative interventions in patients suffering from disorders of consciousness. Sensory stimulation has been proved to be useful in sustaining the level of arousal/awareness and to improve behavioural responsiveness with a significant effect on oro-motor functions. Recently, action observation has been proposed as a stimulation strategy in patients with disorders of consciousness, based on neurophysiological evidence that the motor cortex can be activated not only during action execution but also when actions are merely observed in the absence of motor output, or during listening to action sounds and speech. This mechanism is provided by the activity of mirror neurons. In the present study, a group of patients with disorders of consciousness (11 males, 4 females; median age: 55 years; age range: 19-74 years) underwent task-based functional MRI in which they had, in one condition, to observe and listen to the sound of mouth actions, and in another condition, to listen to verbs with motor or abstract content. In order to verify the presence of residual activation of the mirror neuron system, the brain activations of patients were compared with that of a group of healthy individuals (seven males, eight females; median age: 33.4 years; age range: 24-65 years) performing the same tasks. The results show that brain activations were lower in patients with disorders of consciousness compared with controls, except for primary auditory areas. During the audiovisual task, 5 out of 15 patients with disorders of consciousness showed only residual activation of low-level visual and auditory areas. Activation of high-level parieto-premotor areas was present in six patients. During the listening task, three patients showed only low-level activations, and six patients activated also high-level areas. Interestingly, in both tasks, one patient with a clinical diagnosis of vegetative state showed activations of high-level areas. Region of interest analysis on blood oxygen level dependent signal change in temporal, parietal and premotor cortex revealed a significant linear relation with the level of clinical functioning, assessed with coma recovery scale-revised. We propose a classification of the patient's response based on the presence of low-level and high-level activations, combined with the patient's functional level. These findings support the use of action observation and listening as possible stimulation strategies in patients with disorders of consciousness and highlight the relevance of combined methods based on functional assessment and brain imaging to provide more detailed neuroanatomical specificity about residual activated areas at both cortical and subcortical levels.

Identifiants

pubmed: 38434219
doi: 10.1093/braincomms/fcae045
pii: fcae045
pmc: PMC10907975
doi:

Types de publication

Journal Article

Langues

eng

Pagination

fcae045

Informations de copyright

© The Author(s) 2024. Published by Oxford University Press on behalf of the Guarantors of Brain.

Déclaration de conflit d'intérêts

The authors report no competing interests.

Auteurs

Antonino Errante (A)

Department of Medicine and Surgery, University of Parma, 43125 Parma, Italy.

Stefania Ferraro (S)

MOE Key Laboratory for Neuroinformation, School of Life Science and Technology, University of Electronic Science and Technology of China, 611731 Chengdu, China.
Neuroradiology Unit, Diagnostic and Technology Department, Fondazione IRCCS Istituto Neurologico Carlo Besta, 20133 Milan, Italy.

Greta Demichelis (G)

Neuroradiology Unit, Diagnostic and Technology Department, Fondazione IRCCS Istituto Neurologico Carlo Besta, 20133 Milan, Italy.

Chiara Pinardi (C)

Health Department, Fondazione IRCCS Istituto Neurologico Carlo Besta, 20133 Milan, Italy.

Mario Stanziano (M)

Neuroradiology Unit, Diagnostic and Technology Department, Fondazione IRCCS Istituto Neurologico Carlo Besta, 20133 Milan, Italy.
Neurosciences Department 'Rita Levi Montalcini', University of Turin, 10126 Turin, Italy.

Davide Sattin (D)

Istituti Clinici Scientifici Maugeri IRCCS, 20138 Milan, Italy.

Davide Rossi Sebastiano (D)

Neurophysiology Unit, Diagnostic and Technology Department, Fondazione IRCCS Istituto Neurologico Carlo Besta, 20133 Milan, Italy.

Stefano Rozzi (S)

Department of Medicine and Surgery, University of Parma, 43125 Parma, Italy.

Ludovico D'Incerti (L)

Neuroradiology Unit, Children's Hospital A. Meyer-University of Florence, 50139 Florence, Italy.

Eleonora Catricalà (E)

ICoN Cognitive Neuroscience Center, IUSS, Institute for Advances Studies, 27100 Pavia, Italy.

Matilde Leonardi (M)

Disability Unit and Coma Research Centre, Fondazione IRCCS Istituto Neurologico Carlo Besta, 20133 Milan, Italy.

Maria Grazia Bruzzone (MG)

Neuroradiology Unit, Diagnostic and Technology Department, Fondazione IRCCS Istituto Neurologico Carlo Besta, 20133 Milan, Italy.

Leonardo Fogassi (L)

Department of Medicine and Surgery, University of Parma, 43125 Parma, Italy.

Anna Nigri (A)

Neuroradiology Unit, Diagnostic and Technology Department, Fondazione IRCCS Istituto Neurologico Carlo Besta, 20133 Milan, Italy.

Classifications MeSH