Volatile anesthetics disrupt frontal-posterior recurrent information transfer at gamma frequencies in rat

doi:10.1016/j.neulet.2005.06.018

Neuroscience Letters

Volume 387, Issue 3, 28 October 2005, Pages 145-150

https://doi.org/10.1016/j.neulet.2005.06.018 Get rights and content

Abstract

We seek to understand neural correlates of anesthetic-induced unconsciousness. We hypothesize that cortical integration of sensory information may underlie conscious perception and may be disrupted by anesthetics. A critical role in frontal-posterior interactions has been proposed, and gamma (20–60 Hz) oscillations have also been assigned an essential role in consciousness. Here we investigated whether general anesthetics may interfere with the exchange of information encoded in gamma oscillations between frontal and posterior cortices. Bipolar electrodes for recording of event-related potentials (ERP) were chronically implanted in the primary visual cortex, parietal association and frontal association cortices of six rats. Sixty light flashes were presented every 5 s, and ERPs were recorded at increasing concentrations of halothane or isoflurane (0–2%). Information exchange was estimated by transfer entropy, a novel measure of directional information transfer. Transfer entropy was calculated from 1-s wavelet-transformed ERPs. We found that (1) feedforward transfer entropy (FF-TE) and feedback transfer entropy (FB-TE) were balanced in conscious-sedated state; (2) anesthetics at concentrations producing unconsciousness augmented both FF-TE and FB-TE at 30 Hz but reduced them at 50 Hz; (3) reduction at 50 Hz was more pronounced for FB-TE, especially between frontal and posterior regions; (4) at high concentrations, both FF-TE and FB-TE at all frequencies were at or below conscious-sedated baseline. Our findings suggest that inhalational anesthetics preferentially impair frontal-posterior FB information transfer at high gamma frequencies consistent with the postulated role of frontal-posterior interactions in consciousness.

Section snippets

Acknowledgements

This publication is based on work supported by grants from the NIH (GM-56398), and from the NSF (BES-0002945), and by predoctoral GAANN fellowship from the Department of Education. We thank Richard Rys (Senior Research Engineer) for the design and construction of electronic equipment, and Samhita S. Rhodes, Ph.D. for the implementation of the peak-detection algorithm.

References (34)

O.A. Imas et al.
Halothane augments event-related gamma oscillations in rat visual cortex
Neuroscience
(2004)
E.R. John et al.
Invariant reversible QEEG effects of anesthetics
Conscious Cogn.
(2001)
V.A. Lamme
Blindsight: the role of feedforward and feedback corticocortical connections
Acta Psychol.
(2001)
S. Laureys et al.
Impaired effective cortical connectivity in vegetative state: preliminary investigation using PET
Neuroimage
(1999)
B.D. Mitchell et al.
Corticocortical and thalamocortical projections to layer I of the frontal neocortex in rats
Brain Res.
(2001)
G.W. Nietgen et al.
Volatile anaesthetics have differential effects on recombinant m1 and m3 muscarinic acetylcholine receptor function
Br. J. Anaesth.
(1998)
M. Sarter et al.
The cognitive neuroscience of sustained attention: where top-down meets bottom-up
Brain Res. Brain Res. Rev.
(2001)
N.S. White et al.
Impaired thalamocortical connectivity in humans during general-anesthetic-induced unconsciousness
Neuroimage
(2003)
F. Crick et al.
A framework for consciousness
Nat. Neurosci.
(2003)
P. Flood et al.
Heteromeric nicotinic inhibition by isoflurane does not mediate MAC or loss of righting reflex
Anesthesiology
(2002)

P. Fries et al.

Rapid feature selective neuronal synchronization through correlated latency shifting

Nat. Neurosci.

(2001)

Y. Gonchar et al.

Distinct GABAergic targets of feedforward and feedback connections between lower and higher areas of rat visual cortex

J. Neurosci.

(2003)

T.D. Hansen et al.

Distribution of cerebral blood flow during halothane versus isoflurane anesthesia in rats

Anesthesiology

(1988)

E.R. John

The anesthetic cascade: a theory of how anesthesia suppresses consciousness

Anesthesiology

(2005)

R.R. Johnson et al.

A polysynaptic feedback circuit in rat visual cortex

J. Neurosci.

(1997)

I. Kissin et al.

Pentobarbital-morphine anesthetic interactions in terms of intensity of noxious stimulation required for arousal

Anesthesiology

(1993)

M.D. Krasowski et al.

General anaesthetic actions on ligand-gated ion channels

Cell Mol. Life Sci.

(1999)

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Volatile anesthetics disrupt frontal-posterior recurrent information transfer at gamma frequencies in rat

Abstract

Section snippets

Acknowledgements

Neuroscience

Conscious Cogn.

Acta Psychol.

Neuroimage

Brain Res.

Br. J. Anaesth.

Brain Res. Brain Res. Rev.

Neuroimage

A framework for consciousness

Nat. Neurosci.

Heteromeric nicotinic inhibition by isoflurane does not mediate MAC or loss of righting reflex

Anesthesiology

Rapid feature selective neuronal synchronization through correlated latency shifting

Nat. Neurosci.

Distinct GABAergic targets of feedforward and feedback connections between lower and higher areas of rat visual cortex

J. Neurosci.

Distribution of cerebral blood flow during halothane versus isoflurane anesthesia in rats

Anesthesiology

The anesthetic cascade: a theory of how anesthesia suppresses consciousness

Anesthesiology

A polysynaptic feedback circuit in rat visual cortex

J. Neurosci.

Pentobarbital-morphine anesthetic interactions in terms of intensity of noxious stimulation required for arousal

Anesthesiology

General anaesthetic actions on ligand-gated ion channels

Cell Mol. Life Sci.