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J Neurophysiol (August 23, 2006). doi:10.1152/jn.00524.2006
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Submitted on May 16, 2006
Accepted on August 21, 2006

Fast modulation of prefrontal cortex activity by basal forebrain non-cholinergic neuronal ensembles

Shih-Chieh Lin1*, Damien Gervasoni2, and Miguel A. L. Nicolelis1

1 Neurobiology, Duke University Medical Center, Durham, North Carolina, United States
2 UMR5167, CNRS, Lyon, France

* To whom correspondence should be addressed. E-mail: sclin{at}neuro.duke.edu.

Traditionally, most basal forebrain (BF) functions have been attributed to its cholinergic neurons. However, the majority of cortical-projecting BF neurons are non-cholinergic and their in vivo functions remain unclear. We investigated how BF modulates cortical dynamics by simultaneously recording up to 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 (~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 msec interspike interval. Spike bursts among BFTNs were highly correlated, leading to transient population synchronization events of BFTN ensembles that lasted on average 160 msec. 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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