Propofol disrupts alpha dynamics in functionally distinct thalamocortical networks during loss of consciousness

Author:

Weiner Veronica S.12,Zhou David W.1234ORCID,Kahali Pegah23,Stephen Emily P.2ORCID,Peterfreund Robert A.35,Aglio Linda S.56ORCID,Szabo Michele D.3,Eskandar Emad N.57,Salazar-Gomez Andrés F.3,Sampson Aaron L.3,Cash Sydney S.45ORCID,Brown Emery N.12358,Purdon Patrick L.35ORCID

Affiliation:

1. Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA 02139

2. Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, MA 02139

3. Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital, Boston, MA 02114

4. Center for Neurotechnology and Recovery, Department of Neurology, Massachusetts General Hospital, Boston, MA 02114

5. Harvard Medical School, Boston, MA 02115

6. Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital, Boston, MA 02115

7. Department of Neurological Surgery, Massachusetts General Hospital, Boston, MA 02114

8. Division of Health Sciences and Technology, Harvard Medical School/Massachusetts Institute of Technology, Cambridge, MA 02139

Abstract

During propofol-induced general anesthesia, alpha rhythms measured using electroencephalography undergo a striking shift from posterior to anterior, termed anteriorization, where the ubiquitous waking alpha is lost and a frontal alpha emerges. The functional significance of alpha anteriorization and the precise brain regions contributing to the phenomenon are a mystery. While posterior alpha is thought to be generated by thalamocortical circuits connecting nuclei of the sensory thalamus with their cortical partners, the thalamic origins of the propofol-induced alpha remain poorly understood. Here, we used human intracranial recordings to identify regions in sensory cortices where propofol attenuates a coherent alpha network, distinct from those in the frontal cortex where it amplifies coherent alpha and beta activities. We then performed diffusion tractography between these identified regions and individual thalamic nuclei to show that the opposing dynamics of anteriorization occur within two distinct thalamocortical networks. We found that propofol disrupted a posterior alpha network structurally connected with nuclei in the sensory and sensory associational regions of the thalamus. At the same time, propofol induced a coherent alpha oscillation within prefrontal cortical areas that were connected with thalamic nuclei involved in cognition, such as the mediodorsal nucleus. The cortical and thalamic anatomy involved, as well as their known functional roles, suggests multiple means by which propofol dismantles sensory and cognitive processes to achieve loss of consciousness.

Funder

NIH

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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