Fast modulation of prefrontal cortex activity by basal forebrain noncholinergic neuronal ensembles.

Full Abstract

Traditionally, most basal forebrain (BF) functions have been attributed to its cholinergic neurons. However, the majority of cortical-projecting BF neurons are noncholinergic and their in vivo functions remain unclear. We investigated how BF modulates cortical dynamics by simultaneously recording </=50 BF single neurons along with local field potentials (LFPs) from the prefrontal cortex (PFCx) in different wake-sleep states of adult rats. Using stereotypical spike time correlations, we identified a large (roughly 70%) subset of BF neurons, which we named BF tonic neurons (BFTNs). BFTNs fired tonically at 2-8 Hz without significantly changing their average firing rate across wake-sleep states. As such, these cannot be classified as cholinergic neurons. BFTNs substantially increased the spiking variability during waking and rapid-eye-movement sleep, by exhibiting frequent spike bursts with <50-ms interspike interval. Spike bursts among BFTNs were highly correlated, leading to transient population synchronization events of BFTN ensembles that lasted on average 160 ms. Most importantly, BFTN synchronization occurred preferentially just before the troughs of PFCx LFP oscillations, which reflect increased cortical activity. Furthermore, BFTN synchronization was accompanied by transient increases in prefrontal cortex gamma oscillations. These results suggest that synchronization of BFTN ensembles, which are likely to be formed by cortical-projecting GABAergic neurons from the BF, could be primarily responsible for fast cortical modulations to provide transient amplification of cortical activity.

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Author information

Author/s: Lin, Shih-Chieh (SC); Gervasoni, Damien (D); Nicolelis, Miguel A L (MA);

Affiliation: Department of Neurobiology, Duke University Medical Center, 101 Research Drive, Box 3209, Durham, NC 27710, USA. sclin(-atsign-)neuro.duke.edu

Journal and publication information

Publication Type: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't; Research Support, U.S. Gov't, Non-P.H.S.

Journal: Journal of neurophysiology (J Neurophysiol), published in United States. (Language: eng)

Reference: 2006-Dec; vol 96 (issue 6) : pp 3209-19

Dates: Created 2006/11/19; Completed 2007/01/17;

PMID: 16928796, status: MEDLINE (last retrieval date: 12/26/2008)

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MeSH headings (categories)

This article was linked to the MESH Headings shown below.

Animals
Autonomic Nervous System - cytology; physiology
Cell Size
Data Interpretation, Statistical
Electric Stimulation
Electrodes, Implanted
Electrophysiology
Female
Microelectrodes

Microelectrodes
Neurons - physiology; ultrastructure
Prefrontal Cortex - cytology; physiology
Principal Component Analysis
Prosencephalon - cytology; physiology
Rats
Sleep - physiology
Sleep, REM - physiology
Wakefulness - physiology

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