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The Journal of Neuroscience, September 23, 2009, 29(38):11828-11840; doi:10.1523/JNEUROSCI.1259-09.2009

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Behavioral/Systems/Cognitive
Discharge Profiles of Identified GABAergic in Comparison to Cholinergic and Putative Glutamatergic Basal Forebrain Neurons across the Sleep–Wake Cycle

Oum Kaltoum Hassani,¹ Maan Gee Lee,² Pablo Henny,¹ and Barbara E. Jones¹

¹Department of Neurology and Neurosurgery, Montreal Neurological Institute, McGill University, Montreal, Quebec H3A 2B4, Canada, and ²Department of Pharmacology, School of Medicine, Kyungpook National University, Daegu 700-422, South Korea

Correspondence should be addressed to Dr. Barbara E. Jones, Montreal Neurological Institute, McGill University, 3801 University Street, Montreal, QC H3A 2B4, Canada. Email: barbara.jones{at}mcgill.ca

Whereas basal forebrain (BF) cholinergic neurons are known to participate in processes of cortical activation during wake (W) and paradoxical sleep (PS or P, also called REM sleep), codistributed GABAergic neurons have been thought to participate in processes of cortical deactivation and slow-wave sleep (SWS or S). To learn the roles the GABAergic neurons might play, in relation to cholinergic and glutamatergic neurons, we juxtacellularly recorded and labeled neurons during natural sleep–wake states in head-fixed rats. Neurobiotin (Nb)-labeled cells were identified immunohistochemically as choline acetyltransferase (ChAT)+, glutamic acid decarboxylase (GAD)+, or ChAT–/GAD–. Of the latter, some were identified as glutamatergic by immunostaining of their terminals with the vesicular glutamate transporter (VGluT2). In contrast to ChAT+ neurons, which all discharged maximally during W and PS, GAD+ neurons comprised multiple sleep–wake subgroups. Some GABAergic neurons discharged maximally during W and PS, as WP-max active cells (36%), and in positive correlation with gamma electroencephalographic (EEG) activity. Some discharged maximally during SWS, as S-max active cells (28%), and in positive correlation with delta EEG activity. Others increased their discharge progressively during sleep to discharge maximally during PS, as P-max active cells (36%), and in negative association with electromyographic (EMG) activity. ChAT–/GAD– cells comprised WP-max (46%), S-max (17%), P-max (17%), and W-max active cells (14%), whose discharge was positively correlated with EMG activity. GABAergic neurons would thus play similar or reciprocal roles to other cholinergic and glutamatergic BF neurons in regulating cortical activity and muscle tone along with behavior across sleep–wake states.

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Received March 13, 2009; revised June 18, 2009; accepted June 24, 2009.

Correspondence should be addressed to Dr. Barbara E. Jones, Montreal Neurological Institute, McGill University, 3801 University Street, Montreal, QC H3A 2B4, Canada. Email: barbara.jones{at}mcgill.ca

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