Uncertainty gates redundancy in reward integration in prefrontal-cortical and ventral-hippocampal nucleus accumbens inputs to tune engagement

Circuit neuroscience commonly seeks to assign specific functions to specific circuits. Yet, redundancy can be highly adaptive and is therefore a critical motif in circuit organization. The NAc, a highly integrative brain region controlling motivated behavior, is thought to receive distinct information from its various glutamatergic inputs yet strong evidence of functional specialization of inputs is lacking. Using dual-site fiber photometry in an operant reward task, we simultaneously recorded from two NAc glutamatergic afferents to assess circuit specialization. We identify a common neural motif that integrates reward history in medial prefrontal cortex (mPFC) and ventral hippocampus (vHip) inputs to NAc. Then, by systematically dissociating reward from choice and action, we identify key circuit-specificity in the behavioral conditions that recruit encoding. While mPFC-NAc invariantly encodes reward, vHip-NAc encoding requires goal-directed action and uncertainty. Ultimately, using optogenetic stimulation we demonstrate that both inputs co-operatively modulate task engagement. Taken together, we illustrate how similar encoding, with differential gating by behavioral state, supports outcome encoding to tune engagement to recent history of reward.