Basal forebrain cholinergic neurons (BFCNs) modulate synaptic plasticity, cortical
processing, brain states and oscillations. However, whether distinct types of BFCNs
support different functions remains unclear. Therefore, we recorded BFCNs in vivo,
to examine their behavioral functions, and in vitro, to study their intrinsic properties.
We identified two distinct types of BFCNs that differ in their firing modes, synchronization
properties and behavioral correlates. Bursting cholinergic neurons (Burst-BFCNs) fired
synchronously, phase-locked to cortical theta activity and fired precisely timed bursts
after reward and punishment. Regular-firing cholinergic neurons (Reg-BFCNs) were found
predominantly in the posterior basal forebrain, displayed strong theta rhythmicity
and responded with precise single spikes after behavioral outcomes. In an auditory
detection task, synchronization of Burst-BFCNs to the auditory cortex predicted the
timing of behavioral responses, whereas tone-evoked cortical coupling of Reg-BFCNs
predicted correct detections. We propose that differential recruitment of two basal
forebrain cholinergic neuron types generates behavior-specific cortical activation.
