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 in | PloS one Vol. 13; no. 11; p. e0205967 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
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07.11.2018
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ISSN | 1932-6203 1932-6203 |
DOI | 10.1371/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. |
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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 |
AuthorAffiliation_xml | – name: 5 Phase I Clinical Trial Unit and Experimental Therapy, Fondazione IRCCS Policlinico S. Matteo, Pavia, Italy – name: 2 Istituto di Genetica Molecolare IGM-CNR, Pavia, Italy – name: 3 Istituto di Bioimmagini e Fisiologia Molecolare, CNR, LITA Bldg, Segrate, Italy – 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 – name: University of Regensburg, GERMANY |
Author_xml | – sequence: 1 givenname: Lorenzo orcidid: 0000-0002-8308-2720 surname: Magrassi fullname: Magrassi, Lorenzo – sequence: 2 givenname: Antonio G. surname: Zippo fullname: Zippo, Antonio G. – sequence: 3 givenname: Alberto surname: Azzalin fullname: Azzalin, Alberto – sequence: 4 givenname: Stefano surname: Bastianello fullname: Bastianello, Stefano – sequence: 5 givenname: Roberto surname: Imberti fullname: Imberti, Roberto – sequence: 6 givenname: Gabriele E. M. surname: Biella fullname: Biella, Gabriele E. M. |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30403761$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1016_j_xinn_2025_100846 crossref_primary_10_1111_ner_12944 crossref_primary_10_1186_s40779_024_00585_w crossref_primary_10_1007_s00415_020_10076_2 crossref_primary_10_1523_JNEUROSCI_1216_23_2023 crossref_primary_10_1111_epi_16657 crossref_primary_10_1093_texcom_tgab024 crossref_primary_10_1136_jnnp_2019_322030 |
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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 |
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