A hippocampus-accumbens code guides goal-directed appetitive behavior

Abstract

Neurons in dorsal hippocampus (dHPC) encode a rich repertoire of task-relevant environmental features, while downstream regions such as the nucleus accumbens (NAc) translate this information into task-adaptive behaviors. Yet, the contents of this information stream and their acute role in behavior remain largely unknown. Here, we used in vivo dual-color two-photon imaging to simultaneously record from both large numbers of hippocampal neurons and an identified subpopulation of NAc-projecting neurons during goal-directed navigation towards a hidden reward zone. We found that NAc-projecting neurons contain enriched spatial information and enhanced representations of non-spatial task-relevant behaviors such as deceleration and appetitive licking, both of which could be elicited by optogenetic activation of dHPC terminals in NAc. A generalized linear model revealed enhanced conjunctive coding in NAc-projecting dHPC neurons, improving the identification of the reward zone. We propose that dHPC routes specific reward-related spatial and behavioral state information to guide NAc action selection.

Hippocampal sequences span experience relative to rewards

“…In turn, the hippocampal-entorhinal network may send information about distance from expected rewards back to the prefrontal cortex and other regions where similar activity has been observed 1 , such as the nucleus accumbens [142][143][144][145][146][147] . Such goal-related hippocampal outputs to prefrontal cortex 148 and nucleus accumbens 149 have recently been reported, specifically in the deep sublayer of CA1 148 , where goal-related remapping is generally more prevalent 148,150 . Over learning, reward-relative sequences generated between the entorhinal cortices and hippocampus may become linked with codes for goal-related action sequences in the prefrontal cortex and striatum, helping the brain to generalize learned information surrounding reward to similar experiences 1 .…”

Flexible behavioral adjustment to frustrative nonreward in anticipatory behavior, but not in consummatory behavior, requires the dorsal hippocampus

“…Furthermore, some place neurons show systematic changes in firing rate and preferred firing sites across different environments in response to shifts in reward locations (Dupret et al, 2010; Krishnan et al, 2022; Poucet & Hok, 2017). Indeed, neurons in the dorsal HC (dHC) that project to the nucleus accumbens display amplified representations of task-relevant information, encompassing both spatial and non-spatial aspects (Barnstedt, 2023), that play a role in selecting actions and promoting effective appetitive behavior (Barnstedt, 2023; Trouche et al, 2019). Additionally, awake sharp-wave ripple (SWR) events, which coincide with bursts of HC place cell sequences, are enhanced in response to rewards (Singer & Frank, 2009).…”