Projections from basal forebrain cholinergic neurons (BFCNs) densely innervate neocortex, releasing acetylcholine to regulate arousal, sensory processing and learning. Although the cholinergic system is one of the extensively studied neuromodulatory system, its impact on cortical processing remains unclear. Earlier studies have shown that BFCNs in rostral and caudal basal forebrain nuclei respond largely similar to reward and punishment despite their non-overlapping cortical projections, suggesting that BFCNs act as a unified broadcasting system. In contrast, more recent findings revealed distinct population activity in rostral and caudal BFCNs, with rostral BFCNs being more activated by omission of expected reward, while the caudal BFCNs were more strongly driven by punishment and punishment-predicting auditory cues. To further investigate the functional heterogeneity of individual BFCNs in rostral and caudal basal forebrain nuclei and directly assess their impact on cortical processing, we performed simultaneous high-density electrophysiological recordings in the rostral and caudal BFCNs while using cortex-wide functional imaging to relate BFCN activity to cortical dynamics. Recordings were done in awake mice, performing a reinforcement learning task where three different tones were associated with reward, punishment or absence of any reinforcement. Mice were able to achieve high performance in this task within several sessions and clearly differentiated rewarded from non-rewarded or punished tones. Electrophysiological recordings from optogenetically identified BFCNs revealed variability across individual neurons with specialized responses to primary reinforcers. Moreover, the activity of individual BFCNs was correlated with different cortical activity patterns, suggesting that they differentially affected cortical processing during learning and task performance.