The ventral hippocampus is necessary for cue-elicited, but not outcome driven approach-avoidance conflict decisions: a novel operant choice decision-making task

Abstract

Approach-avoidance conflict is induced when an organism encounters a stimulus that carries both positive and negative attributes. Accumulating evidence implicates the ventral hippocampus (VH) in the detection and resolution of approach-avoidance conflict, largely on the basis of maze-based tasks assaying innate and conditioned responses to situations of conflict. However, its role in discrete trial approach-avoidance decision-making has yet to be elucidated. In this study, we designed a novel cued operant conflict decision-making task in which rats were required to choose and respond for a low reward option or high reward option paired with varying shock intensities on a differential reinforcement of low rates of responding schedule. Post training, the VH was chemogenetically inhibited while animals performed the task with the usual outcomes delivered, and with the presentation of cues associated with the reward vs. conflict options only (extinction condition). We found that VH inhibition led to an avoidance of the conflict option and longer latency to choose this option when decision-making was being made on the basis of cues alone with no outcomes. Consistent with these findings, VH-inhibited animals spent more time in the central component of the elevated plus maze (EPM), indicating a potential deficit in decision-making under innate forms of approach-avoidance conflict. Taken together, these findings implicate the VH in cue-driven approach-avoidance decisions in the face of motivational conflict.

A Corticothalamic Circuit Trades off Speed for Safety during Decision-Making under Motivational Conflict

“…Two brain regions, the vSub, located in the temporal lobe ( Gray, 1982 ; Gray and McNaughton, 2000 ; Ito and Lee, 2016 ; Marchant et al, 2016 ; Çavdaroğlu et al, 2021 ), and the PVT, located in the midline thalamus ( Choi and McNally, 2017 ; Zhu et al, 2018 ; Choi et al, 2019 ; Engelke et al, 2021 ; Ma et al, 2021 ), have been implicated in motivational conflict, and so could contribute to these decision-making dynamics. Yet how activity in these brain regions relates to approach–avoidance decision-making remains poorly understood.…”

“…The role of vSub in these processes is less clear. vSub is implicated in behavior under motivational conflict ( Ito and Lee, 2016 ; Marchant et al, 2016 ; Çavdaroğlu et al, 2021 ). However, the role of vSub in conflict behavior here was distinct to that of PVT.…”

“…These roles are due, at least in part, to prefrontal interactions with amygdala and striatum ( Verharen et al, 2019 , 2020 ; Kyriazi et al, 2020 ). The ventral hippocampus, and in particular the ventral subiculum (vSub), is also well established in approach–avoidance conflict ( Gray, 1982 ; O'Neil et al, 2015 ; Ito and Lee, 2016 ; Schumacher et al, 2016 ; Gray and McNaughton, 2000 ; Çavdaroğlu et al, 2021 ). For example, human neuroimaging studies show hippocampal recruitment during approach–avoidance conflict ( Bach et al, 2014 ; O'Neil et al, 2015 ), and pharmacological ( Nguyen et al, 2015 ; Schumacher et al, 2016 ) or chemogenetic ( Marchant et al, 2016 ) manipulation of vSub in rodents alters decision-making under conflict.…”

Two opposing hippocampus to prefrontal cortex pathways for the control of approach and avoidance behaviour

“…10), suggesting many more variables are represented by these neurons than we describe here. Therefore, an important future direction will be to investigate the activity of the two vH-PFC layers in behavioural tasks where the learning and updating of different stages of the decision process can be accurately separated [67][68][69] .…”

The ventral hippocampus CA3 is critical in regulating timing uncertainty in temporal decision-making

“…That being said, accumulating evidence suggests that the VH may be particularly important in regulating goal-directed behaviors under the control of cues that signal potential reward or threat, as opposed to actual appetitive/aversive outcomes, with the present task falling into the latter category. Thus, approachavoidance conflict situations that are sensitive to VH lesions, such as the elevated plus maze, the cued approach-avoidance conflict maze, or even cued extinction sessions, are all instances in which stimulus features signal safety/reward or threat in the absence of actual outcomes (Bannerman et al, 2004;Schumacher et al, 2016Schumacher et al, , 2018Ç avdaro glu et al, 2020, 2021. However, this possibility clearly warrants further investigation.…”