Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness
The neurophysiological mechanisms by which anesthetic drugs cause loss of consciousness are poorly understood. Anesthetic actions at the molecular, cellular, and systems levels have been studied in detail at steady states of deep general anesthesia. However, little is known about how anesthetics alt...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | en_US |
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National Academy of Sciences (U.S.)
2013
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| Online Access: | http://hdl.handle.net/1721.1/77240 https://orcid.org/0000-0001-6888-5448 https://orcid.org/0000-0003-2668-7819 |
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| author | Lewis, Laura D. Weiner, Veronica S. Mukamel, Eran A. Donoghue, Jacob Alexander Eskandar, Emad Madsen, Joseph R. Anderson, William S. Hochberg, Leigh R. Cash, Sydney S. Browna, Emery N. Purdon, Patrick L. |
| author2 | Massachusetts Institute of Technology. Institute for Medical Engineering & Science |
| author_facet | Massachusetts Institute of Technology. Institute for Medical Engineering & Science Lewis, Laura D. Weiner, Veronica S. Mukamel, Eran A. Donoghue, Jacob Alexander Eskandar, Emad Madsen, Joseph R. Anderson, William S. Hochberg, Leigh R. Cash, Sydney S. Browna, Emery N. Purdon, Patrick L. |
| author_sort | Lewis, Laura D. |
| collection | MIT |
| description | The neurophysiological mechanisms by which anesthetic drugs cause loss of consciousness are poorly understood. Anesthetic actions at the molecular, cellular, and systems levels have been studied in detail at steady states of deep general anesthesia. However, little is known about how anesthetics alter neural activity during the transition into unconsciousness. We recorded simultaneous multiscale neural activity from human cortex, including ensembles of single neurons, local field potentials, and intracranial electrocorticograms, during induction of general anesthesia. We analyzed local and global neuronal network changes that occurred simultaneously with loss of consciousness. We show that propofol-induced unconsciousness occurs within seconds of the abrupt onset of a slow (<1 Hz) oscillation in the local field potential. This oscillation marks a state in which cortical neurons maintain local patterns of network activity, but this activity is fragmented across both time and space. Local (<4 mm) neuronal populations maintain the millisecond-scale connectivity patterns observed in the awake state, and spike rates fluctuate and can reach baseline levels. However, neuronal spiking occurs only within a limited slow oscillation-phase window and is silent otherwise, fragmenting the time course of neural activity. Unexpectedly, we found that these slow oscillations occur asynchronously across cortex, disrupting functional connectivity between cortical areas. We conclude that the onset of slow oscillations is a neural correlate of propofol-induced loss of consciousness, marking a shift to cortical dynamics in which local neuronal networks remain intact but become functionally isolated in time and space. |
| first_indexed | 2024-09-23T10:17:50Z |
| format | Article |
| id | mit-1721.1/77240 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T10:17:50Z |
| publishDate | 2013 |
| publisher | National Academy of Sciences (U.S.) |
| record_format | dspace |
| spelling | mit-1721.1/772402022-09-30T20:11:08Z Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness Lewis, Laura D. Weiner, Veronica S. Mukamel, Eran A. Donoghue, Jacob Alexander Eskandar, Emad Madsen, Joseph R. Anderson, William S. Hochberg, Leigh R. Cash, Sydney S. Browna, Emery N. Purdon, Patrick L. Massachusetts Institute of Technology. Institute for Medical Engineering & Science Harvard University--MIT Division of Health Sciences and Technology Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Lewis, Laura D. Weiner, Veronica S. Brown, Emery N. The neurophysiological mechanisms by which anesthetic drugs cause loss of consciousness are poorly understood. Anesthetic actions at the molecular, cellular, and systems levels have been studied in detail at steady states of deep general anesthesia. However, little is known about how anesthetics alter neural activity during the transition into unconsciousness. We recorded simultaneous multiscale neural activity from human cortex, including ensembles of single neurons, local field potentials, and intracranial electrocorticograms, during induction of general anesthesia. We analyzed local and global neuronal network changes that occurred simultaneously with loss of consciousness. We show that propofol-induced unconsciousness occurs within seconds of the abrupt onset of a slow (<1 Hz) oscillation in the local field potential. This oscillation marks a state in which cortical neurons maintain local patterns of network activity, but this activity is fragmented across both time and space. Local (<4 mm) neuronal populations maintain the millisecond-scale connectivity patterns observed in the awake state, and spike rates fluctuate and can reach baseline levels. However, neuronal spiking occurs only within a limited slow oscillation-phase window and is silent otherwise, fragmenting the time course of neural activity. Unexpectedly, we found that these slow oscillations occur asynchronously across cortex, disrupting functional connectivity between cortical areas. We conclude that the onset of slow oscillations is a neural correlate of propofol-induced loss of consciousness, marking a shift to cortical dynamics in which local neuronal networks remain intact but become functionally isolated in time and space. 2013-02-28T18:07:00Z 2013-02-28T18:07:00Z 2012-11 2012-06 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/77240 Lewis, L. D. et al. “From the Cover: PNAS Plus: Rapid Fragmentation of Neuronal Networks at the Onset of Propofol-induced Unconsciousness.” Proceedings of the National Academy of Sciences 109.49 (2012). © 2012 National Academy of Sciences https://orcid.org/0000-0001-6888-5448 https://orcid.org/0000-0003-2668-7819 en_US http://dx.doi.org/10.1073/pnas.1210907109 Proceedings of the National Academy of Sciences of the United States of America Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) PNAS |
| spellingShingle | Lewis, Laura D. Weiner, Veronica S. Mukamel, Eran A. Donoghue, Jacob Alexander Eskandar, Emad Madsen, Joseph R. Anderson, William S. Hochberg, Leigh R. Cash, Sydney S. Browna, Emery N. Purdon, Patrick L. Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness |
| title | Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness |
| title_full | Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness |
| title_fullStr | Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness |
| title_full_unstemmed | Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness |
| title_short | Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness |
| title_sort | rapid fragmentation of neuronal networks at the onset of propofol induced unconsciousness |
| url | http://hdl.handle.net/1721.1/77240 https://orcid.org/0000-0001-6888-5448 https://orcid.org/0000-0003-2668-7819 |
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