Single unit activities recorded in the thalamus and the overlying parietal cortex of subjects affected by disorders of consciousness

The lack of direct neurophysiological recordings from the thalamus and the cortex hampers our understanding of vegetative state/unresponsive wakefulness syndrome and minimally conscious state in humans. We obtained microelectrode recordings from the thalami and the homolateral parietal cortex of two...

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Published inPloS one Vol. 13; no. 11; p. e0205967
Main Authors Magrassi, Lorenzo, Zippo, Antonio G., Azzalin, Alberto, Bastianello, Stefano, Imberti, Roberto, Biella, Gabriele E. M.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 07.11.2018
Public Library of Science (PLoS)
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ISSN1932-6203
1932-6203
DOI10.1371/journal.pone.0205967

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Abstract The lack of direct neurophysiological recordings from the thalamus and the cortex hampers our understanding of vegetative state/unresponsive wakefulness syndrome and minimally conscious state in humans. We obtained microelectrode recordings from the thalami and the homolateral parietal cortex of two vegetative state/unresponsive wakefulness syndrome and one minimally conscious state patients during surgery for implantation of electrodes in both thalami for chronic deep brain stimulation. We found that activity of the thalamo-cortical networks differed among the two conditions. There were half the number of active neurons in the thalami of patients in vegetative state/unresponsive wakefulness syndrome than in minimally conscious state. Coupling of thalamic neuron discharge with EEG phases also differed in the two conditions and thalamo-cortical cross-frequency coupling was limited to the minimally conscious state patient. When consciousness is physiologically or pharmacologically reversibly suspended there is a significant increase in bursting activity of the thalamic neurons. By contrast, in the thalami of our patients in both conditions fewer than 17% of the recorded neurons showed bursting activity. This indicates that these conditions differ from physiological suspension of consciousness and that increased thalamic inhibition is not prominent. Our findings, albeit obtained in a limited number of patients, unveil the neurophysiology of these conditions at single unit resolution and might be relevant for inspiring novel therapeutic options.
AbstractList The lack of direct neurophysiological recordings from the thalamus and the cortex hampers our understanding of vegetative state/unresponsive wakefulness syndrome and minimally conscious state in humans. We obtained microelectrode recordings from the thalami and the homolateral parietal cortex of two vegetative state/unresponsive wakefulness syndrome and one minimally conscious state patients during surgery for implantation of electrodes in both thalami for chronic deep brain stimulation. We found that activity of the thalamo-cortical networks differed among the two conditions. There were half the number of active neurons in the thalami of patients in vegetative state/unresponsive wakefulness syndrome than in minimally conscious state. Coupling of thalamic neuron discharge with EEG phases also differed in the two conditions and thalamo-cortical cross-frequency coupling was limited to the minimally conscious state patient. When consciousness is physiologically or pharmacologically reversibly suspended there is a significant increase in bursting activity of the thalamic neurons. By contrast, in the thalami of our patients in both conditions fewer than 17% of the recorded neurons showed bursting activity. This indicates that these conditions differ from physiological suspension of consciousness and that increased thalamic inhibition is not prominent. Our findings, albeit obtained in a limited number of patients, unveil the neurophysiology of these conditions at single unit resolution and might be relevant for inspiring novel therapeutic options.
The lack of direct neurophysiological recordings from the thalamus and the cortex hampers our understanding of vegetative state/unresponsive wakefulness syndrome and minimally conscious state in humans. We obtained microelectrode recordings from the thalami and the homolateral parietal cortex of two vegetative state/unresponsive wakefulness syndrome and one minimally conscious state patients during surgery for implantation of electrodes in both thalami for chronic deep brain stimulation. We found that activity of the thalamo-cortical networks differed among the two conditions. There were half the number of active neurons in the thalami of patients in vegetative state/unresponsive wakefulness syndrome than in minimally conscious state. Coupling of thalamic neuron discharge with EEG phases also differed in the two conditions and thalamo-cortical cross-frequency coupling was limited to the minimally conscious state patient. When consciousness is physiologically or pharmacologically reversibly suspended there is a significant increase in bursting activity of the thalamic neurons. By contrast, in the thalami of our patients in both conditions fewer than 17% of the recorded neurons showed bursting activity. This indicates that these conditions differ from physiological suspension of consciousness and that increased thalamic inhibition is not prominent. Our findings, albeit obtained in a limited number of patients, unveil the neurophysiology of these conditions at single unit resolution and might be relevant for inspiring novel therapeutic options.The lack of direct neurophysiological recordings from the thalamus and the cortex hampers our understanding of vegetative state/unresponsive wakefulness syndrome and minimally conscious state in humans. We obtained microelectrode recordings from the thalami and the homolateral parietal cortex of two vegetative state/unresponsive wakefulness syndrome and one minimally conscious state patients during surgery for implantation of electrodes in both thalami for chronic deep brain stimulation. We found that activity of the thalamo-cortical networks differed among the two conditions. There were half the number of active neurons in the thalami of patients in vegetative state/unresponsive wakefulness syndrome than in minimally conscious state. Coupling of thalamic neuron discharge with EEG phases also differed in the two conditions and thalamo-cortical cross-frequency coupling was limited to the minimally conscious state patient. When consciousness is physiologically or pharmacologically reversibly suspended there is a significant increase in bursting activity of the thalamic neurons. By contrast, in the thalami of our patients in both conditions fewer than 17% of the recorded neurons showed bursting activity. This indicates that these conditions differ from physiological suspension of consciousness and that increased thalamic inhibition is not prominent. Our findings, albeit obtained in a limited number of patients, unveil the neurophysiology of these conditions at single unit resolution and might be relevant for inspiring novel therapeutic options.
Author Magrassi, Lorenzo
Zippo, Antonio G.
Biella, Gabriele E. M.
Azzalin, Alberto
Imberti, Roberto
Bastianello, Stefano
AuthorAffiliation 1 Neurochirurgia, Dipartimento di Scienze Clinico-Chirurgiche, Diagnostiche e Pediatriche, University of Pavia—Fondazione IRCCS Policlinico S. Matteo, Pavia, Italy
3 Istituto di Bioimmagini e Fisiologia Molecolare, CNR, LITA Bldg, Segrate, Italy
5 Phase I Clinical Trial Unit and Experimental Therapy, Fondazione IRCCS Policlinico S. Matteo, Pavia, Italy
4 State University of Pavia, Dept. of Brain and Behavioral Sciences, Neuroradiology Department—C. Mondino National Neurological Institute, Pavia, Italy
2 Istituto di Genetica Molecolare IGM-CNR, Pavia, Italy
University of Regensburg, GERMANY
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– name: 4 State University of Pavia, Dept. of Brain and Behavioral Sciences, Neuroradiology Department—C. Mondino National Neurological Institute, Pavia, Italy
– name: 1 Neurochirurgia, Dipartimento di Scienze Clinico-Chirurgiche, Diagnostiche e Pediatriche, University of Pavia—Fondazione IRCCS Policlinico S. Matteo, Pavia, Italy
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Snippet The lack of direct neurophysiological recordings from the thalamus and the cortex hampers our understanding of vegetative state/unresponsive wakefulness...
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SourceType Open Website
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StartPage e0205967
SubjectTerms Biology and Life Sciences
Brain
Bursting
Consciousness
Cortex (parietal)
Coupling
Deep brain stimulation
EEG
Electroencephalography
Engineering and Technology
Firing pattern
Implantation
Medicine and Health Sciences
Microelectrodes
Neurons
Neurophysiology
NMR
Nuclear magnetic resonance
Patients
Pharmacology
Research and Analysis Methods
Sleep
Sleep and wakefulness
Studies
Surgery
Thalamus
Unconsciousness
Wakefulness
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Title Single unit activities recorded in the thalamus and the overlying parietal cortex of subjects affected by disorders of consciousness
URI https://www.ncbi.nlm.nih.gov/pubmed/30403761
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https://pubmed.ncbi.nlm.nih.gov/PMC6221278
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http://dx.doi.org/10.1371/journal.pone.0205967
Volume 13
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