Habituation of auditory startle reflex is a new sign of minimally conscious state
Neurological examination of non-communicating patients relies on a few decisive items that enable the crucial distinction between vegetative state (VS)—also coined unresponsive wakefulness syndrome (UWS)—and minimally conscious state. Over the past 10 years, this distinction has proven its diagnosti...
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| Published in | Brain (London, England : 1878) Vol. 143; no. 7; pp. 2154 - 2172 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article Web Resource |
| Language | English |
| Published |
England
Oxford University Press
01.07.2020
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0006-8950 1460-2156 1460-2156 |
| DOI | 10.1093/brain/awaa159 |
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| Abstract | Neurological examination of non-communicating patients relies on a few decisive items that enable the crucial distinction between vegetative state (VS)—also coined unresponsive wakefulness syndrome (UWS)—and minimally conscious state. Over the past 10 years, this distinction has proven its diagnostic value as well as its important prognostic value on consciousness recovery. However, clinicians are currently limited by three factors: (i) the current behavioural repertoire of minimally conscious state items is limited and restricted to a few cognitive domains in the goldstandard revised version of the Coma Recovery Scale; (ii) a proportion of ∼15–20% clinically VS/UWS patients are actually in a richer state than VS/UWS as evidenced by functional brain imaging; and (iii) the neurophysiological and cognitive interpretation of each minimally conscious state item is still unclear and debated. In the current study we demonstrate that habituation of the auditory startle reflex (hASR) tested at bedside constitutes a novel, simple and powerful behavioural sign that can accurately distinguish minimally conscious state from VS/UWS. In addition to enlarging the minimally conscious state items repertoire, and therefore decreasing the low sensitivity of current behavioural measures, we also provide an original and rigorous description of the neurophysiological basis of hASR through a combination of functional (high density EEG and 18F-fluorodeoxyglucose PET imaging) and structural (diffusion tensor imaging MRI) measures. We show that preservation of hASR is associated with the functional and structural integrity of a brain-scale fronto-parietal network, including prefrontal regions related to control of action and inhibition, and meso-parietal areas associated with minimally conscious and conscious states. Lastly, we show that hASR predicts 6-month improvement of consciousness. Taken together, our results show that hASR is a cortically-mediated behaviour, and suggest that it could be a new clinical item to clearly and accurately identify non-communicating patients who are in the minimally conscious state. |
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| AbstractList | Disorders of consciousness are challenging to diagnose. Hermann
et al
. identify a new clinical sign, the habituation of auditory startle reflex, which indexes the activity of a fronto-parietal network and predicts improved consciousness at 6 months. The measure could be a new bedside sign of minimally conscious state.
Neurological examination of non-communicating patients relies on a few decisive items that enable the crucial distinction between vegetative state (VS)—also coined unresponsive wakefulness syndrome (UWS)—and minimally conscious state. Over the past 10 years, this distinction has proven its diagnostic value as well as its important prognostic value on consciousness recovery. However, clinicians are currently limited by three factors: (i) the current behavioural repertoire of minimally conscious state items is limited and restricted to a few cognitive domains in the goldstandard revised version of the Coma Recovery Scale; (ii) a proportion of ∼15–20% clinically VS/UWS patients are actually in a richer state than VS/UWS as evidenced by functional brain imaging; and (iii) the neurophysiological and cognitive interpretation of each minimally conscious state item is still unclear and debated. In the current study we demonstrate that habituation of the auditory startle reflex (hASR) tested at bedside constitutes a novel, simple and powerful behavioural sign that can accurately distinguish minimally conscious state from VS/UWS. In addition to enlarging the minimally conscious state items repertoire, and therefore decreasing the low sensitivity of current behavioural measures, we also provide an original and rigorous description of the neurophysiological basis of hASR through a combination of functional (high density EEG and
18
F-fluorodeoxyglucose PET imaging) and structural (diffusion tensor imaging MRI) measures. We show that preservation of hASR is associated with the functional and structural integrity of a brain-scale fronto-parietal network, including prefrontal regions related to control of action and inhibition, and meso-parietal areas associated with minimally conscious and conscious states. Lastly, we show that hASR predicts 6-month improvement of consciousness. Taken together, our results show that hASR is a cortically-mediated behaviour, and suggest that it could be a new clinical item to clearly and accurately identify non-communicating patients who are in the minimally conscious state. Neurological examination of non-communicating patients relies on a few decisive items that enable the crucial distinction between vegetative state (VS)-also coined unresponsive wakefulness syndrome (UWS)-and minimally conscious state. Over the past 10 years, this distinction has proven its diagnostic value as well as its important prognostic value on consciousness recovery. However, clinicians are currently limited by three factors: (i) the current behavioural repertoire of minimally conscious state items is limited and restricted to a few cognitive domains in the goldstandard revised version of the Coma Recovery Scale; (ii) a proportion of ∼15-20% clinically VS/UWS patients are actually in a richer state than VS/UWS as evidenced by functional brain imaging; and (iii) the neurophysiological and cognitive interpretation of each minimally conscious state item is still unclear and debated. In the current study we demonstrate that habituation of the auditory startle reflex (hASR) tested at bedside constitutes a novel, simple and powerful behavioural sign that can accurately distinguish minimally conscious state from VS/UWS. In addition to enlarging the minimally conscious state items repertoire, and therefore decreasing the low sensitivity of current behavioural measures, we also provide an original and rigorous description of the neurophysiological basis of hASR through a combination of functional (high density EEG and 18F-fluorodeoxyglucose PET imaging) and structural (diffusion tensor imaging MRI) measures. We show that preservation of hASR is associated with the functional and structural integrity of a brain-scale fronto-parietal network, including prefrontal regions related to control of action and inhibition, and meso-parietal areas associated with minimally conscious and conscious states. Lastly, we show that hASR predicts 6-month improvement of consciousness. Taken together, our results show that hASR is a cortically-mediated behaviour, and suggest that it could be a new clinical item to clearly and accurately identify non-communicating patients who are in the minimally conscious state. Neurological examination of non-communicating patients relies on a few decisive items that enable the crucial distinction between vegetative state (VS)-also coined unresponsive wakefulness syndrome (UWS)-and minimally conscious state. Over the past 10 years, this distinction has proven its diagnostic value as well as its important prognostic value on consciousness recovery. However, clinicians are currently limited by three factors: (i) the current behavioural repertoire of minimally conscious state items is limited and restricted to a few cognitive domains in the goldstandard revised version of the Coma Recovery Scale; (ii) a proportion of ∼15-20% clinically VS/UWS patients are actually in a richer state than VS/UWS as evidenced by functional brain imaging; and (iii) the neurophysiological and cognitive interpretation of each minimally conscious state item is still unclear and debated. In the current study we demonstrate that habituation of the auditory startle reflex (hASR) tested at bedside constitutes a novel, simple and powerful behavioural sign that can accurately distinguish minimally conscious state from VS/UWS. In addition to enlarging the minimally conscious state items repertoire, and therefore decreasing the low sensitivity of current behavioural measures, we also provide an original and rigorous description of the neurophysiological basis of hASR through a combination of functional (high density EEG and 18F-fluorodeoxyglucose PET imaging) and structural (diffusion tensor imaging MRI) measures. We show that preservation of hASR is associated with the functional and structural integrity of a brain-scale fronto-parietal network, including prefrontal regions related to control of action and inhibition, and meso-parietal areas associated with minimally conscious and conscious states. Lastly, we show that hASR predicts 6-month improvement of consciousness. Taken together, our results show that hASR is a cortically-mediated behaviour, and suggest that it could be a new clinical item to clearly and accurately identify non-communicating patients who are in the minimally conscious state.Neurological examination of non-communicating patients relies on a few decisive items that enable the crucial distinction between vegetative state (VS)-also coined unresponsive wakefulness syndrome (UWS)-and minimally conscious state. Over the past 10 years, this distinction has proven its diagnostic value as well as its important prognostic value on consciousness recovery. However, clinicians are currently limited by three factors: (i) the current behavioural repertoire of minimally conscious state items is limited and restricted to a few cognitive domains in the goldstandard revised version of the Coma Recovery Scale; (ii) a proportion of ∼15-20% clinically VS/UWS patients are actually in a richer state than VS/UWS as evidenced by functional brain imaging; and (iii) the neurophysiological and cognitive interpretation of each minimally conscious state item is still unclear and debated. In the current study we demonstrate that habituation of the auditory startle reflex (hASR) tested at bedside constitutes a novel, simple and powerful behavioural sign that can accurately distinguish minimally conscious state from VS/UWS. In addition to enlarging the minimally conscious state items repertoire, and therefore decreasing the low sensitivity of current behavioural measures, we also provide an original and rigorous description of the neurophysiological basis of hASR through a combination of functional (high density EEG and 18F-fluorodeoxyglucose PET imaging) and structural (diffusion tensor imaging MRI) measures. We show that preservation of hASR is associated with the functional and structural integrity of a brain-scale fronto-parietal network, including prefrontal regions related to control of action and inhibition, and meso-parietal areas associated with minimally conscious and conscious states. Lastly, we show that hASR predicts 6-month improvement of consciousness. Taken together, our results show that hASR is a cortically-mediated behaviour, and suggest that it could be a new clinical item to clearly and accurately identify non-communicating patients who are in the minimally conscious state. Neurological examination of non-communicating patients relies on a few decisive items that enable the crucial distinction between vegetative state (VS)-also coined unresponsive wakefulness syndrome (UWS)-and minimally conscious state. Over the past 10 years, this distinction has proven its diagnostic value as well as its important prognostic value on consciousness recovery. However, clinicians are currently limited by three factors: (i) the current behavioural repertoire of minimally conscious state items is limited and restricted to a few cognitive domains in the goldstandard revised version of the Coma Recovery Scale; (ii) a proportion of -15-20% clinically VS/UWS patients are actually in a richer state than VS/UWS as evidenced by functional brain imaging; and (iii) the neurophysiological and cognitive interpretation of each minimally conscious state item is still unclear and debated. In the current study we demonstrate that habituation of the auditory startle reflex (hASR) tested at bedside constitutes a novel, simple and powerful behavioural sign that can accurately distinguish minimally conscious state from VS/UWS. In addition to enlarging the minimally conscious state items repertoire, and therefore decreasing the low sensitivity of current behavioural measures, we also provide an original and rigorous description of the neurophysiological basis of hASR through a combination of functional (high density EEG and 18F-fluorodeoxyglucose PET imaging) and structural (diffusion tensor imaging MRI) measures. We show that preservation of hASR is associated with the functional and structural integrity of a brain-scale fronto-parietal network, including prefrontal regions related to control of action and inhibition, and meso-parietal areas associated with minimally conscious and conscious states. Lastly, we show that hASR predicts 6-month improvement of consciousness. Taken together, our results show that hASR is a cortically-mediated behaviour, and suggest that it could be a new clinical item to clearly and accurately identify non-communicating patients who are in the minimally conscious state. © The Author(s) (2020). Published by Oxford University Press on behalf of the Guarantors of Brain. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
| Author | Hermann, Bertrand Perlbarg, Vincent Galanaud, Damien Habert, Marie-Odile Perez, Pauline Naccache, Lionel Kas, Aurélie Rohaut, Benjamin Raimondo, Federico Pyatigorskaya, Nadya Salah, Amina Ben Stender, Johan Puybasset, Louis Valente, Mélanie Sitt, Jacobo D |
| AuthorAffiliation | a1 Institut du Cerveau et de la Moelle épinière - ICM , Inserm U1127, CNRS UMR 7225, F-75013, Paris, France a12 Department of Neurology , Columbia University, New York, NY 10027, USA a3 Faculté de Médecine Pitié-Salpêtrière, Sorbonne Universités , UPMC Université Paris 06, Paris, France a4 Sorbonne Université, CNRS, INSERM, Laboratoire d’Imagerie Biomédicale, LIB , F-75006, Paris, France a7 Department of Neuroradiology, Groupe hospitalier Pitié-Salpêtrière , AP-HP, F-75013, Paris, France a8 Department of Nuclear Medicine, Groupe hospitalier Pitié-Salpêtrière , AP-HP, F-75013, Paris, France a9 Coma Science Group, GIGA Consciousness, University of Liège , Belgium a11 Department of Anesthesia and Critical Care, Multidisciplinary Intensive Care Unit, Groupe hospitalier Pitié-Salpêtrière , AP-HP, F-75013, Paris, France a6 Department of Clinical Neurophysiology, Groupe hospitalier Pitié-Salpêtrière , AP-HP, F-75013, Paris, France a10 Centre du Cerveau, University Hospital of Liège , Belgium a2 Departm |
| AuthorAffiliation_xml | – name: a2 Department of Neurology, Groupe hospitalier Pitié-Salpêtrière , AP-HP, F-75013, Paris, France – name: a11 Department of Anesthesia and Critical Care, Multidisciplinary Intensive Care Unit, Groupe hospitalier Pitié-Salpêtrière , AP-HP, F-75013, Paris, France – name: a7 Department of Neuroradiology, Groupe hospitalier Pitié-Salpêtrière , AP-HP, F-75013, Paris, France – name: a1 Institut du Cerveau et de la Moelle épinière - ICM , Inserm U1127, CNRS UMR 7225, F-75013, Paris, France – name: a3 Faculté de Médecine Pitié-Salpêtrière, Sorbonne Universités , UPMC Université Paris 06, Paris, France – name: a10 Centre du Cerveau, University Hospital of Liège , Belgium – name: a12 Department of Neurology , Columbia University, New York, NY 10027, USA – name: a4 Sorbonne Université, CNRS, INSERM, Laboratoire d’Imagerie Biomédicale, LIB , F-75006, Paris, France – name: a5 BrainTale SAS , F-75013, Paris, France – name: a9 Coma Science Group, GIGA Consciousness, University of Liège , Belgium – name: a6 Department of Clinical Neurophysiology, Groupe hospitalier Pitié-Salpêtrière , AP-HP, F-75013, Paris, France – name: a8 Department of Nuclear Medicine, Groupe hospitalier Pitié-Salpêtrière , AP-HP, F-75013, Paris, France |
| Author_xml | – sequence: 1 givenname: Bertrand orcidid: 0000-0001-9071-3415 surname: Hermann fullname: Hermann, Bertrand organization: Institut du Cerveau et de la Moelle épinière - ICM, Inserm U1127, CNRS UMR 7225, F-75013, Paris, France, Department of Neurology, Groupe hospitalier Pitié-Salpêtrière, AP-HP, F-75013, Paris, France, Faculté de Médecine Pitié-Salpêtrière, Sorbonne Universités, UPMC Université Paris 06, Paris, France – sequence: 2 givenname: Amina Ben surname: Salah fullname: Salah, Amina Ben organization: Institut du Cerveau et de la Moelle épinière - ICM, Inserm U1127, CNRS UMR 7225, F-75013, Paris, France – sequence: 3 givenname: Vincent surname: Perlbarg fullname: Perlbarg, Vincent organization: Sorbonne Université, CNRS, INSERM, Laboratoire d’Imagerie Biomédicale, LIB, F-75006, Paris, France, BrainTale SAS, F-75013, Paris, France – sequence: 4 givenname: Mélanie surname: Valente fullname: Valente, Mélanie organization: Institut du Cerveau et de la Moelle épinière - ICM, Inserm U1127, CNRS UMR 7225, F-75013, Paris, France, Department of Clinical Neurophysiology, Groupe hospitalier Pitié-Salpêtrière, AP-HP, F-75013, Paris, France – sequence: 5 givenname: Nadya orcidid: 0000-0002-2070-1299 surname: Pyatigorskaya fullname: Pyatigorskaya, Nadya organization: Institut du Cerveau et de la Moelle épinière - ICM, Inserm U1127, CNRS UMR 7225, F-75013, Paris, France, Faculté de Médecine Pitié-Salpêtrière, Sorbonne Universités, UPMC Université Paris 06, Paris, France, Department of Neuroradiology, Groupe hospitalier Pitié-Salpêtrière, AP-HP, F-75013, Paris, France – sequence: 6 givenname: Marie-Odile surname: Habert fullname: Habert, Marie-Odile organization: Sorbonne Université, CNRS, INSERM, Laboratoire d’Imagerie Biomédicale, LIB, F-75006, Paris, France, Department of Nuclear Medicine, Groupe hospitalier Pitié-Salpêtrière, AP-HP, F-75013, Paris, France – sequence: 7 givenname: Federico surname: Raimondo fullname: Raimondo, Federico organization: Institut du Cerveau et de la Moelle épinière - ICM, Inserm U1127, CNRS UMR 7225, F-75013, Paris, France, Coma Science Group, GIGA Consciousness, University of Liège, Belgium, Centre du Cerveau, University Hospital of Liège, Belgium – sequence: 8 givenname: Johan surname: Stender fullname: Stender, Johan organization: Institut du Cerveau et de la Moelle épinière - ICM, Inserm U1127, CNRS UMR 7225, F-75013, Paris, France – sequence: 9 givenname: Damien surname: Galanaud fullname: Galanaud, Damien organization: Institut du Cerveau et de la Moelle épinière - ICM, Inserm U1127, CNRS UMR 7225, F-75013, Paris, France, Faculté de Médecine Pitié-Salpêtrière, Sorbonne Universités, UPMC Université Paris 06, Paris, France, Department of Neuroradiology, Groupe hospitalier Pitié-Salpêtrière, AP-HP, F-75013, Paris, France – sequence: 10 givenname: Aurélie surname: Kas fullname: Kas, Aurélie organization: Sorbonne Université, CNRS, INSERM, Laboratoire d’Imagerie Biomédicale, LIB, F-75006, Paris, France, Department of Nuclear Medicine, Groupe hospitalier Pitié-Salpêtrière, AP-HP, F-75013, Paris, France – sequence: 11 givenname: Louis surname: Puybasset fullname: Puybasset, Louis organization: Faculté de Médecine Pitié-Salpêtrière, Sorbonne Universités, UPMC Université Paris 06, Paris, France, Sorbonne Université, CNRS, INSERM, Laboratoire d’Imagerie Biomédicale, LIB, F-75006, Paris, France, Department of Anesthesia and Critical Care, Multidisciplinary Intensive Care Unit, Groupe hospitalier Pitié-Salpêtrière, AP-HP, F-75013, Paris, France – sequence: 12 givenname: Pauline surname: Perez fullname: Perez, Pauline organization: Institut du Cerveau et de la Moelle épinière - ICM, Inserm U1127, CNRS UMR 7225, F-75013, Paris, France – sequence: 13 givenname: Jacobo D surname: Sitt fullname: Sitt, Jacobo D organization: Institut du Cerveau et de la Moelle épinière - ICM, Inserm U1127, CNRS UMR 7225, F-75013, Paris, France – sequence: 14 givenname: Benjamin surname: Rohaut fullname: Rohaut, Benjamin organization: Institut du Cerveau et de la Moelle épinière - ICM, Inserm U1127, CNRS UMR 7225, F-75013, Paris, France, Department of Neurology, Groupe hospitalier Pitié-Salpêtrière, AP-HP, F-75013, Paris, France, Faculté de Médecine Pitié-Salpêtrière, Sorbonne Universités, UPMC Université Paris 06, Paris, France, Department of Neurology, Columbia University, New York, NY 10027, USA – sequence: 15 givenname: Lionel orcidid: 0000-0002-2874-1009 surname: Naccache fullname: Naccache, Lionel organization: Institut du Cerveau et de la Moelle épinière - ICM, Inserm U1127, CNRS UMR 7225, F-75013, Paris, France, Department of Neurology, Groupe hospitalier Pitié-Salpêtrière, AP-HP, F-75013, Paris, France, Faculté de Médecine Pitié-Salpêtrière, Sorbonne Universités, UPMC Université Paris 06, Paris, France, Department of Clinical Neurophysiology, Groupe hospitalier Pitié-Salpêtrière, AP-HP, F-75013, Paris, France |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32582938$$D View this record in MEDLINE/PubMed https://hal.sorbonne-universite.fr/hal-02886037$$DView record in HAL |
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| Issue | 7 |
| Keywords | disorders of consciousness auditory startle reflex cortically mediated state habituation minimally conscious state |
| Language | English |
| License | http://creativecommons.org/licenses/by-nc/4.0 The Author(s) (2020). Published by Oxford University Press on behalf of the Guarantors of Brain. Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
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| Snippet | Neurological examination of non-communicating patients relies on a few decisive items that enable the crucial distinction between vegetative state (VS)—also... Neurological examination of non-communicating patients relies on a few decisive items that enable the crucial distinction between vegetative state (VS)-also... Disorders of consciousness are challenging to diagnose. Hermann et al . identify a new clinical sign, the habituation of auditory startle reflex, which indexes... |
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| SubjectTerms | Adult Auditory startle reflex Brain Brain - physiopathology Cortically mediated state Disorders of consciousness Editor's Choice Female Habituation Habituation, Psychophysiologic Habituation, Psychophysiologic - physiology Human health sciences Humans Life Sciences Male Middle Aged Minimally conscious state Neurologie Neurology Neurons and Cognition Original Persistent Vegetative State Persistent Vegetative State - diagnosis Persistent Vegetative State - physiopathology Recovery of Function Recovery of Function - physiology Reflex, Startle Reflex, Startle - physiology Review Sciences de la santé humaine |
| Title | Habituation of auditory startle reflex is a new sign of minimally conscious state |
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