Dynamics of propofol-induced loss of consciousness across primate neocortex

Yumiko Ishizawa, Omar J. Ahmed, Shaun R. Patel, John T. Gale, Demetrio Sierra-Mercado, Emery N. Brown, Emad N. Eskandar

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

The precise neural mechanisms underlying transitions between consciousness and anesthetic-induced unconsciousness remain unclear. Here, we studied intracortical neuronal dynamics leading to propofol-induced unconsciousness by recording single-neuron activity and local field potentials directly in the functionally interconnecting somatosensory (S1) and frontal ventral premotor (PMv) network during a gradual behavioral transition from full alertness to loss of consciousness (LOC) and on through a deeper anesthetic level. Macaque monkeys were trained for a behavioral task designed to determine the trial-by-trial alertness and neuronal response to tactile and auditory stimulation.Weshow that disruption of coherent beta oscillations between S1 and PMv preceded, but did not coincide with, the LOC. LOC appeared to correspond to pronounced but brief gamma-/high-beta-band oscillations (lasting~3 min) in PMv, followed by a gamma peak in S1. We also demonstrate that the slow oscillations appeared after LOC in S1 and then in PMv after a delay, together suggesting that neuronal dynamics are very different across S1 versus PMv during LOC. Finally, neurons in both S1 and PMv transition from responding to bimodal (tactile and auditory) stimulation before LOC to only tactile modality during unconsciousness, consistent with an inhibition of multisensory integration in this network. Our results show that propofol-induced LOC is accompanied by spatiotemporally distinct oscillatory neuronal dynamics across the somatosensory and premotor network and suggest that a transitional state from wakefulness to unconsciousness is not a continuous process, but rather a series of discrete neural changes.

Original languageEnglish (US)
Pages (from-to)7718-7726
Number of pages9
JournalJournal of Neuroscience
Volume36
Issue number29
DOIs
StatePublished - Jul 20 2016
Externally publishedYes

Fingerprint

Unconsciousness
Neocortex
Propofol
Primates
Touch
Acoustic Stimulation
Anesthetics
Neurons
Wakefulness
Macaca
Consciousness
Haplorhini

Keywords

  • General anesthesia
  • Local field potential
  • Loss of consciousness
  • Primate
  • Sensory premotor network
  • Single-neuron activity

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Ishizawa, Y., Ahmed, O. J., Patel, S. R., Gale, J. T., Sierra-Mercado, D., Brown, E. N., & Eskandar, E. N. (2016). Dynamics of propofol-induced loss of consciousness across primate neocortex. Journal of Neuroscience, 36(29), 7718-7726. https://doi.org/10.1523/JNEUROSCI.4577-15.2016

Dynamics of propofol-induced loss of consciousness across primate neocortex. / Ishizawa, Yumiko; Ahmed, Omar J.; Patel, Shaun R.; Gale, John T.; Sierra-Mercado, Demetrio; Brown, Emery N.; Eskandar, Emad N.

In: Journal of Neuroscience, Vol. 36, No. 29, 20.07.2016, p. 7718-7726.

Research output: Contribution to journalArticle

Ishizawa, Y, Ahmed, OJ, Patel, SR, Gale, JT, Sierra-Mercado, D, Brown, EN & Eskandar, EN 2016, 'Dynamics of propofol-induced loss of consciousness across primate neocortex', Journal of Neuroscience, vol. 36, no. 29, pp. 7718-7726. https://doi.org/10.1523/JNEUROSCI.4577-15.2016
Ishizawa Y, Ahmed OJ, Patel SR, Gale JT, Sierra-Mercado D, Brown EN et al. Dynamics of propofol-induced loss of consciousness across primate neocortex. Journal of Neuroscience. 2016 Jul 20;36(29):7718-7726. https://doi.org/10.1523/JNEUROSCI.4577-15.2016
Ishizawa, Yumiko ; Ahmed, Omar J. ; Patel, Shaun R. ; Gale, John T. ; Sierra-Mercado, Demetrio ; Brown, Emery N. ; Eskandar, Emad N. / Dynamics of propofol-induced loss of consciousness across primate neocortex. In: Journal of Neuroscience. 2016 ; Vol. 36, No. 29. pp. 7718-7726.
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