Rat orbitofrontal ensemble activity contains a multiplexed but value-invariant representation of task structure in an odor sequence task

Abstract

The orbitofrontal cortex (OFC) has long been implicated in signaling information about expected outcomes to facilitate adaptive or flexible behavior. Current proposals focus on signaling of expected reward values versus the representation of a value-agnostic cognitive map of the task. While often suggested as mutually exclusive, these alternatives may represent two extreme ends of a continuum determined by the complexity of the environment and the subjects' experience in it. As learning proceeds, an initial, detailed cognitive map might be acquired, based largely on external information. With more experience, this hypothesized map can then be tailored to include relevant abstract hidden cognitive constructs. This might default to expected values in situations where other attributes are minimized or largely irrelevant, whereas in richer tasks, a more detailed structure might continue to be represented, at least where relevant to behavior, and possibly alongside value. Here we sought to arbitrate between these options by recording single unit activity from the OFC in rats navigating an odor sequence task analogous to a spatial maze. The odor sequences provided a clearly mappable state space, with 24 unique "positions" defined by sensory information, likelihood of reward, or both. Consistent with the hypothesis that the OFC represents a cognitive map tailored to the subjects' intentions or plans, we found a close correspondence between how subjects' behavior suggested they were using the sequences, and the neural representations of the sequences in OFC ensembles. Multiplexed with this value-invariant representation of the task, we also found a representation of the expected value at each location. Thus value and task structure are co-existing and potentially dissociable components of the neural code in OFC.

Entorhinal and ventromedial prefrontal cortices abstract and generalise the structure of reinforcement learning problems

“…Understanding how the brain represents abstract task state-spaces remains a major challenge. Our data joins growing evidence suggesting state-space representations rely on the hippocampal formation 5,9,[34][35][36] and interconnected regions in the ventral PFC 2,3,36,37 . This is particularly interesting in light of the historical role of these regions in generalisation and relational reasoning [38][39][40][41][42] , which are essential for efficient task representations.…”

Ventrolateral periaqueductal gray neurons prioritize threat probability over fear output

“…Ramping activity reflected threat probability and fear output, though probability emerged earlier and was stronger overall. While vlPAG signals for fear output could potentially emerge at the ensemble level ( Jones et al, 2007 ; Zhou et al, 2018 ), these multi-unit codes would be composed of single-units primarily signaling threat probability. Activity reflecting fear output may be found in other vlPAG populations, such as neurons showing inhibition of firing to cues ( Tovote et al, 2015 ), or in non-cue-responsive single-units ( Insanally et al, 2019 ).…”