The Journal of Neuroscience, October 31, 2007, 27(44):11999-12006; doi:10.1523/JNEUROSCI.2968-07.2007
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Behavioral/Systems/Cognitive
Cortical Acetylcholine Release Is Lateralized during Asymmetrical Slow-Wave Sleep in Northern Fur Seals
Jennifer L. Lapierre,1
Peter O. Kosenko,2
Oleg I. Lyamin,1,2
Tohru Kodama,3
Lev M. Mukhametov,2 and
Jerome M. Siegel1
1Department of Psychiatry, School of Medicine, University of California Los Angeles and Neurobiology Research, Veterans Affairs Greater Los Angeles Healthcare System, North Hills, California 91343, 2Utrish Dolphinarium Ltd., Moscow, Russia 119071, and 3Department of Psychology, Tokyo Metropolitan Institute for Neuroscience, Tokyo, Japan 183-8526
Correspondence should be addressed to Dr. Jerome M. Siegel, Neurobiology Research (151-A3), Department of Psychiatry, University of California Los Angeles School of Medicine, Veterans Affairs Greater Los Angeles Healthcare System, 16111 Plummer Street, North Hills, CA 91343. Email: jsiegel{at}ucla.edu
Fur seals are unique in that they display both bilateral slow-wave sleep (BSWS), as seen in all terrestrial mammals, and slow-wave sleep with interhemispheric electroencephalogram (EEG) asymmetry, resembling the unihemispheric slow waves of cetaceans. Little is known about the underlying mechanisms of this phenomenon, which is also termed asymmetrical slow wave sleep (ASWS). However, we may begin to understand the expression of ASWS by studying the neurotransmitter systems thought to be involved in the generation and maintenance of sleep–wake states in terrestrial mammals. We examined bilaterally the release of cortical acetylcholine (ACh), a neurotransmitter implicated in the regulation of cortical EEG and behavioral arousal, across the sleep–wake cycle in four juvenile northern fur seals (Callorhinus ursinus). In vivo microdialysis and high-performance liquid chromatography coupled with electrochemical detection were used to measure cortical ACh levels during polygraphically defined behavioral states. Cortical ACh release was state-dependent, showing maximal release during active waking (AW), similar levels during quiet waking (QW), and rapid eye movement (REM) sleep, and minimal release during BSWS. When compared with BSWS, cortical ACh levels increased
300% during AW, and
200% during QW and REM sleep. During these bilaterally symmetrical EEG states, ACh was synchronously released from both hemispheres. However, during ASWS, ACh release was lateralized with greater release in the hemisphere displaying lower voltage activity, at levels approximating those seen in QW. These findings demonstrate that cortical ACh release is tightly linked to hemispheric EEG activation.
Key words: sleep–wake cycle; acetylcholine; microdialysis; cerebral cortex; asymmetry; Callorhinus ursinus
Received June 29, 2007;
revised Sept. 10, 2007;
accepted Sept. 10, 2007.
Correspondence should be addressed to Dr. Jerome M. Siegel, Neurobiology Research (151-A3), Department of Psychiatry, University of California Los Angeles School of Medicine, Veterans Affairs Greater Los Angeles Healthcare System, 16111 Plummer Street, North Hills, CA 91343. Email: jsiegel{at}ucla.edu
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O. I. Lyamin, P. O. Kosenko, J. L. Lapierre, L. M. Mukhametov, and J. M. Siegel
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