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Comparative Study
. 2005 Apr 27;25(17):4365-9.
doi: 10.1523/JNEUROSCI.0178-05.2005.

Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep

Maan Gee Lee  1 , Oum K Hassani, Angel Alonso, Barbara E Jones
Affiliations
Comparative Study

Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep

Maan Gee Lee et al. J Neurosci. .

Abstract

It is known that acetylcholine can stimulate activation and promote plasticity in the cerebral cortex, yet it is not known how the cholinergic basal forebrain neurons, which release acetylcholine in the cortex, discharge in relation to natural cortical activity and sleep-wake states. By recording basal forebrain units in association with electroencephalographic activity across the sleep-wake cycle and labeling individual neurons with Neurobiotin for immunohistochemical identification, we show for the first time that cholinergic neurons discharge in bursts at maximal rates during active waking and paradoxical sleep, when gamma and theta electroencephalographic activity are maximal. They virtually cease firing during slow-wave sleep. Notably, their bursting discharge is synchronized with theta oscillations. Through their maximal firing and rhythmic theta discharge during active waking and paradoxical sleep, the cholinergic neurons can thus modulate the cortex to promote activation along with plasticity during these two states.

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Figures

Figure 1.
Figure 1.
Location and classification of Nb-labeled neurons. A, Image of a cell (#c30u13) labeled with Nb (stained by green fluorescent Cy2) and immunopositive for ChAT (stained by red Cy3). Scale bar, 20 μm. B, Plots of Nb-labeled neurons (n = 34) through the basal forebrain (from left to right at approximately -0.40, -0.92, and -1.30 mm from bregma) that were classified as discharging maximally during aW (circle), SWS (triangle), or PS (square) and distinguished as cholinergic (Nb+/ChAT+; filled symbols including one in red for the cell shown in A) or noncholinergic (Nb+/ChAT-; open symbols). BST, Bed nucleus of the stria terminalis; GP, globus pallidus; LPO, lateral preoptic area; MPO, medial preoptic nucleus; oc, optic chiasm. Scale bar, 1 mm.
Figure 2.
Figure 2.
Discharge of an Nb-labeled cholinergic neuron. A-D, Record of Nb+/ChAT+ unit discharge (Fig. 1 A, #c30u13) together with EEG and EMG activity during 10 s periods of aW (A), SWS (B), tPS (C), and PS (D). The unit fired during aW, virtually ceased firing during SWS, resumed firing during tPS, and discharged maximally during PS. As evident in the expanded 0.5 s traces (bottom), the unit discharged in bursts of spikes with theta EEG activity that was present intermittently during aW, briefly at the end of tPS, and continuously during PS. Calibration: 1 s, 1 mV (EEG, EMG), 1.5 mV (Unit).
Figure 3.
Figure 3.
Discharge profile and pattern of an Nb-labeled cholinergic neuron. A, Across sleep-wake (S-W) states (shown in the sleep-wake hypnogram), the Nb+/ChAT+ cell (Figs. 1 A, 2, #c30u13) discharged at variable rates (shown in unit rate histogram) in association with variable EEGs (shown in power spectral array). B, Its average discharge rate was moderately high in aW, minimal in SWS, and maximal in PS. C, Its discharge pattern was rhythmic during aW, tPS, and PS (shown in the ACHs). D, Its firing was significantly cross-correlated with the EEG during PS on both the RS and PF cortex (evident in the Unit-to-EEG STA in red compared with the shuffled train in gray). E, Its rhythmic discharge occurred in high-frequency bursts of spikes (∼143 Hz) at regular intervals corresponding to a theta oscillation (according to the first and second smoothed modes of the ISIH for PS). F, Its EEG-correlated discharge occurred at a theta frequency with a peak of 7 Hz (evident in the power spectra of the Unit-to-EEG STA shown in red) that also corresponded to the prominent peak of the EEG activity (in blue) on both the RS cortex and the PF cortex during PS.
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