Basal forebrain cholinergic input mediates adaptive attention allocation to enhance olfactory discrimination

Abstract

By selectively amplifying relevant sensory input, animals efficiently allocate limited cognitive resources to improve decision-making. Allocation of attention is aligned with behavioral goals and adaptive to cognitive demand, but the circuit mechanisms remain unclear. Here, we identify an attention circuit for odor processing where cholinergic neurons in the horizontal nucleus of the diagonal band provide top-down control through inhibitory dopaminergic short-axon cells in the mouse olfactory bulb. Attentional cue triggered cholinergic activity provides preparatory disinhibition of olfactory sensory axons to enhance response to reward-associated odors and improves decision-making. Preparatory, but not reward-dependent, cholinergic activity is disengaged in proficient animals when the task becomes routine, underlying a trade-off between proficiency and attention engagement. Direct manipulation of the disinhibitory circuit reinstates attentional effect without eliciting general arousal. A computational model of the circuit recapitulates the dynamic change in attention responses and illustrates a two-stage adaptation that efficiently allocates cognitive resources.