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

Author:

Errante Antonino1ORCID,Ferraro Stefania23ORCID,Demichelis Greta3,Pinardi Chiara4,Stanziano Mario35,Sattin Davide6,Rossi Sebastiano Davide7,Rozzi Stefano1,D’Incerti Ludovico8,Catricalà Eleonora9,Leonardi Matilde10,Bruzzone Maria Grazia3,Fogassi Leonardo1,Nigri Anna3

Affiliation:

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

2. MOE Key Laboratory for Neuroinformation, School of Life Science and Technology, University of Electronic Science and Technology of China , 611731 Chengdu , China

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

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

5. Neurosciences Department ‘Rita Levi Montalcini’, University of Turin , 10126 Turin , Italy

6. Istituti Clinici Scientifici Maugeri IRCCS , 20138 Milan , Italy

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

8. Neuroradiology Unit, Children’s Hospital A. Meyer—University of Florence , 50139 Florence , Italy

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

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

Abstract

Abstract 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.

Funder

Italian Ministry of Health

Publisher

Oxford University Press (OUP)

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