Task Demand-dependent Contribution of Frontal-Sensory Cortical Projections to Attentional Behavior in Mice

Top-down attention is a dynamic cognitive process that facilitates the detection of the task-relevant stimuli from our complex sensory environment. A neural mechanism capable of deployment under specific task-demand conditions would be crucial to efficiently control attentional processes and improve goal-directed attention performance in task demand-dependent manner. Previous studies have shown that frontal top-down neurons projecting from anterior cingulate area (ACA) to the visual cortex (VIS; ACAvis) are required for attentional behavior during the 5-choice serial reaction time task (5CSRTT) in mice. However, it is unknown whether the contribution of this projecting neurons is dependent on the extent of task demand. Here, we examine the differential contribution of ACAvis projection neurons to the attentional behavior in adult male mice performing two visual attention tasks of varying task demand: the 5CSRTT and 2-choice serial reaction time task (2CSRTT). We found that optogenetic suppression ACAvis projections immediately before stimulus presentation has no effect during the 2CSRTT in contrast to the impaired performance during the 5CSRTT. Fiber photometry calcium imaging of ACAvis neuron activity revealed that these neurons, which are recruited after errors during 5CSRTT, are not recruited during 2CSRTT. These results suggest that ACAvis projections are necessary only when task demand is high and that ACAvis neuron activity may not provide an error monitoring signal when task demand is low. Collectively, this frontal-sensory ACAvis projection regulates visual attention behavior during specific high task demand conditions, pointing to a flexible circuit-based mechanism for promoting attentional behavior.