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Coupling changes in cortical and pontine sigma and theta frequency oscillations following monoaminergic lesions in rat

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Abstract

Purpose

Sigma and theta frequency electroencephalogram (EEG) oscillations exhibit substantial and well-recognized shifts with transitions across sleep and wake states. We aimed in this study to test the changes in coupling between these characteristic oscillations of non-rapid-eye-movement (NREM)/rapid-eye-movement (REM) sleep within and between cortical and pontine EEGs following monoaminergic lesion, by using the Pearson's product-moment correlation coefficients.

Methods

Experiments were performed in 14 adult, male Sprague Dawley rats chronically instrumented for sleep recording. We lesioned the dorsal raphe nucleus axon terminals in four rats using PCA neurotoxin (p-chloroamphetamine; Sigma-Aldrich, MO) administered as two intraperitoneal (IP) injections (6 mg/kg) 24 h apart. Lesioning of locus coeruleus axon terminals was performed in five rats using DSP-4 neurotoxin (N-2-chloroethyl-N-ethyl-2-bromobenzilamine; Sigma-Aldrich, MO) in a single IP dose of 50 mg/kg.

Results & Conclusions

Our previous study [Saponjic et al., Physiol Behav 90:1–10, 2007] demonstrated that these systemically induced monoaminergic lesions failed to produce significant changes in sleep/wake distribution from control conditions. The present study, by using spectral analysis and by examining the Pearson's correlation coefficients and their approximate probability density (APD) distribution profiles in control and lesion condition, demonstrates significant augmentation of the sigma/theta coupling strength, an inversion of cortical sigma/theta coupling direction and emergence of an additional sigma/theta coupling “mode” specific to the post-lesion state only within the cortex. By using the Pearson's correlation coefficients and their APD profiles, instead of classical sleep/wake distribution analysis, as a measure of direction and strength of sigma/theta coupling within and between cortex and pons, we were able to uncover the impact of a tonically decreased level of brain monoamines as altered strength and mode of coupling between sigma and theta oscillations. Specifically, a new mode of sigma/theta coupling emerged following lesion, which was specific to NREM sleep, suggests that loss of monoaminergic signaling interferes with NREM sleep consolidation. Our results also indicate an importance of monoamines in control of the sleep spindle and theta rhythm generators.

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Acknowledgments

This work was supported by Serbian Ministry of Science and Technological Development Grant 143005, 143027, and NIH Grant AG01630.

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Authors and Affiliations

  1. Department of Neurobiology, Institute for Biological Research - Sinisa Stankovic, University of Belgrade, Despot Stefan Blvd. 142, 11 000, Belgrade, Serbia

    Srdjan Kesic & Jasna Saponjic

  2. Department for Life Sciences, Institute for Multidisciplinary Research, 11 000, Belgrade, Serbia

    Aleksandar Kalauzi

  3. Department of Pharmacology, University of Illinois, Chicago, IL, 60612, USA

    Miodrag Radulovacki

  4. Center for Narcolepsy, Sleep and Health Research, University of Illinois, Chicago, IL, 60612, USA

    Miodrag Radulovacki & David W. Carley

Authors
  1. Srdjan Kesic
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  2. Aleksandar Kalauzi
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  3. Miodrag Radulovacki
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  4. David W. Carley
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  5. Jasna Saponjic
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Correspondence to Jasna Saponjic.

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Kesic, S., Kalauzi, A., Radulovacki, M. et al. Coupling changes in cortical and pontine sigma and theta frequency oscillations following monoaminergic lesions in rat. Sleep Breath 15, 35–47 (2011). https://doi.org/10.1007/s11325-010-0327-6

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  • DOI: https://doi.org/10.1007/s11325-010-0327-6

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