Elsevier

Neuroscience

Volume 123, Issue 1, 2004, Pages 269-278
Neuroscience

Halothane augments event-related γ oscillations in rat visual cortex

https://doi.org/10.1016/j.neuroscience.2003.09.014Get rights and content

Abstract

Cortical γ oscillations have been associated with neural processes supporting cognition and the state of consciousness but the effect of general anesthesia on γ oscillations is controversial. Here we studied the concentration-dependent effect of halothane on γ (20–60 Hz) power of event-related potentials (ERP) in rat primary visual cortex. ERP to light flashes repeated at 5-s intervals was recorded with chronically implanted, bipolar, intracortical electrodes at selected steady-state halothane concentrations between 0 and 2%. γ-Band power was calculated for 0–1000, 0–300 and 300–1000 ms poststimulus periods and corresponding prestimulus (PS) periods. Multitaper power spectral analysis was used to estimate γ power from both single-trial and average ERP in order to differentiate between phase-locked (evoked) and non-phase-locked (induced) γ activities. Significant PS γ power was present at all halothane concentrations. Flash elicited an increase in γ power that lasted up to 1 s poststimulus at all halothane concentrations. Halothane at intermediate concentrations (0.5–1.2%) augmented both PS and ERP γ power two to four times relative to the waking baseline. γ Power was not different between waking and deeply anesthetized (2%) levels. γ Power reached maximum, as predicted by a Gaussian fit of power-concentration data, at halothane concentration (0.86%) similar to the concentration (0.73%) that abolished the righting reflex, a behavioral index of loss of consciousness. Evoked, i.e. stimulus-locked, γ power was present during the first 300 ms poststimulus but not later, and was approximately 50% of single-trial ERP γ power. Single-trial γ power was present also at 300–1000 ms poststimulus, reflecting ERP not phase-locked to the stimulus.

In summary, these observations suggest that (1) γ activity is present in states ranging from waking to deep halothane anesthesia, (2) halothane does not prevent the transfer of visual input to striate cortex even at surgical plane of anesthesia, and (3) anesthetic-induced loss of consciousness, as reflected by the loss of righting reflex, is not correlated with a reduction in γ power. Variance with other studies may be due to an underestimation of γ power by ERP signal averaging as compared with single-trial analysis.

Section snippets

Experimental procedures

The experimental procedures and protocols used in this investigation were reviewed and approved by the Institutional Animal Care and Use Committee. All procedures conformed to the Guiding Principles in the Care and Use of Animals of the American Physiologic Society and were in accordance with the Guide for the Care and Use of Laboratory Animals (National Academy Press, Washington, D.C., 1996). All efforts were made to minimize the number of animals used and their suffering.

Righting reflex

Six animals that were tested for the loss of righting reflex as a function of halothane concentration demonstrated consistent results. The righting reflex of all rats was lost between 0.7% and 0.8% halothane. Namely, in four animals the loss of righting reflex occurred at 0.7% halothane; in the other two rats the righting reflex was lost at 0.8%.

Effect of halothane on ERP power spectrum

Fig. 1 shows average power spectral estimates of 1-s long single-trial ERP data at seven halothane concentrations. It is apparent that various

Discussion

In this study, we examined the concentration-dependent effects of halothane on γ oscillations in the rat visual cortex before and after single flash stimuli. We demonstrated that both pre- and poststimulus γ activity was enhanced at intermediate halothane concentrations but was not different from its waking baseline and surgically anesthetized levels. We also showed that during the first 300 ms poststimulus, approximately half of the γ power was phase-locked to the flash while the other half

Acknowledgements

This publication is based on work supported by grants from the National Institute of Health, GM-56398, and MH-51358 and from the National Science Foundation, BES-0002945. Special thanks to Senior Engineer Richard Rys for the design and construction of electronic equipment.

References (57)

  • G. Pfurtscheller et al.

    Differentiation between finger, toe and tongue movement in man based on 40 Hz EEG

    Electroencephalogr Clin Neurophysiol

    (1994)
  • L.S. Rabe et al.

    Effects of halothane on evoked field potentials recorded from cortical and subcortical nuclei

    Neuropharmacology

    (1980)
  • D. Schwender et al.

    Anesthetic control of 40-Hz brain activity and implicit memory

    Conscious Cogn

    (1994)
  • J.W. Sleigh et al.

    Comparison of changes in electroencephalographic measures during induction of general anaesthesiainfluence of the gamma frequency band and electromyogram signal

    Br J Anaesth

    (2001)
  • C. Tallon-Baudry et al.

    Oscillatory gamma activity in humans and its role in object representation

    Trends Cogn Sci

    (1999)
  • C.H. Vanderwolf

    Are neocortical gamma waves related to consciousness?

    Brain Res

    (2000)
  • V. Bonhomme et al.

    Auditory steady-state response and bispectral index for assessing level of consciousness during propofol sedation and hypnosis

    Anesth Analg

    (2000)
  • J.J. Bouyer et al.

    C R Seances Acad Sci D

    (2000)
  • T.P. Bronez

    On the performance advantage of multitaper spectral analysis

    IEEE Trans Signal Proc

    (1992)
  • G. Buzsaki

    Hippocampal GABAergic interneuronsa physiological perspective

    Neurochem Res

    (2001)
  • J.P. Donoghue et al.

    Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements

    J Neurophysiol

    (1998)
  • R.C. Dutton et al.

    Inhaled nonimmobilizers do not alter the middle latency auditory-evoked response of rats

    Anesth Analg

    (2000)
  • R.C. Dutton et al.

    Forty-hertz midlatency auditory evoked potential activity predicts wakeful response during desflurane and propofol anesthesia in volunteers

    Anesthesiology

    (1999)
  • R. Eckhorn et al.

    Coherent oscillationsa mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat

    Biol Cybern

    (1988)
  • V.A. Feshchenko et al.

    Comparison of the EEG effects of midazolam, thiopental, and propofolthe role of underlying oscillatory systems

    Neuropsychobiology

    (1997)
  • P. Flood et al.

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

    Anesthesiology

    (2002)
  • P. Fries et al.

    Modulation of oscillatory neuronal synchronization by selective visual attention

    Science

    (2001)
  • I. Gilron et al.

    40 Hz Auditory steady-state response and EEG spectral edge frequency during sufentanil anesthesia

    Can J Anaesth

    (1998)
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