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Behavior in naturalistic scenarios occurs in diverse environments. Adaptive strategies rely on multiple neural circuits and competing decision systems. However, past studies of rodent decision making have largely measured behavior in simple environments. To fill this gap, we recorded neural ensembles from hippocampus (HC), dorsolateral striatum (DLS), and dorsomedial prefrontal cortex (dmPFC) while rats foraged for food under changing rules in environments with varying topological complexity. Environmental complexity increased behavioral variability, lengthened HC nonlocal sequences, and modulated action caching. We found contrasting representations between DLS and HC, supporting a competition between decision systems. dmPFC activity was indicative of setting this balance, in particular predicting the extent of HC non-local coding. Inactivating mPFC impaired short-term behavioral adaptation and produced long-term deficits in balancing decision systems. Our findings reveal the dynamic nature of decision-making systems and how environmental complexity modulates their engagement with implications for behavior in naturalistic environments., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2024 Elsevier Inc. All rights reserved.)

A frequent assumption in value-based decision-making tasks is that agents make decisions based on the feature dimension that reward probabilities vary on. However, in complex, multidimensional environments, stimuli can vary on multiple dimensions at once, meaning that the feature deserving the most credit for outcomes is not always obvious. As a result, individuals may vary in the strategies used to sample stimuli across dimensions, and these strategies may have an unrecognized influence on decision-making. Sex is a proxy for multiple genetic and endocrine influences on behavior, including how environments are sampled. In this study, we examined the strategies adopted by female and male mice as they learned the value of stimuli that varied in both image and location in a visually cued two-armed bandit, allowing two possible dimensions to learn about. Female mice acquired the correct image-value associations more quickly than male mice, preferring a fundamentally different strategy. Female mice were more likely to constrain their decision-space early in learning by preferentially sampling one location over which images varied. Conversely, male mice were more likely to be inconsistent, changing their choice frequently and responding to the immediate experience of stochastic rewards. Individual strategies were related to sex-biased changes in neuronal activation in early learning. Together, we find that in mice, sex is associated with divergent strategies for sampling and learning about the world, revealing substantial unrecognized variability in the approaches implemented during value-based decision making., Competing Interests: Declaration of Interests The authors declare no competing interests., (Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.)

During decision making, hippocampal activity encodes information sometimes about present and sometimes about potential future plans. The mechanisms underlying this transition remain unknown. Building on the evidence that gamma oscillations at different frequencies (low gamma [LG], 30-55 Hz; high gamma [HG], 60-90 Hz; and epsilon, 100-140 Hz) reflect inputs from different circuits, we identified how changes in those frequencies reflect different information-processing states. Using a unique noradrenergic manipulation by clonidine, which shifted both neural representations and gamma states, we found that future representations depended on gamma components. These changes were identifiable on each cycle of theta as asymmetries in the theta cycle, which arose from changes within the ratio of LG and HG power and the underlying phases of those gamma rhythms within the theta cycle. These changes in asymmetry of the theta cycle reflected changes in representations of present and future on each theta cycle., (Copyright © 2018 The Author(s). Published by Elsevier Inc. All rights reserved.)

Current theories posit that memories encoded during experiences are subsequently consolidated into longer-term storage. Hippocampal sharp-wave-ripple (SWR) events have been linked to this consolidation process during sleep, but SWRs also occur during awake immobility, where their role remains unclear. We report that awake SWR rates at the reward site are inversely related to the prevalence of vicarious trial and error (VTE) behaviors, thought to be involved in deliberation processes. SWR rates were diminished immediately after VTE behaviors and an increase in the rate of SWR events at the reward site predicted a decrease in subsequent VTE behaviors at the choice point. Furthermore, SWR disruptions increased VTE behaviors. These results suggest an inverse relationship between SWRs and VTE behaviors and suggest that awake SWRs and associated planning and memory consolidation mechanisms are engaged specifically in the context of higher levels of behavioral certainty., (Copyright © 2016 Elsevier Inc. All rights reserved.)

Hippocampal pyramidal cells can be divided into place cells, which fire action potentials when an animal is in specific locations, and silent cells, which are not spatially selective. In this issue of Neuron, Epsztein et al. find intracellular differences between place and silent cells by using whole-cell recordings in freely moving rats., (Copyright © 2011 Elsevier Inc. All rights reserved.)

Decision-making studies across different domains suggest that decisions can arise from multiple, parallel systems in the brain: a flexible system utilizing action-outcome expectancies and a more rigid system based on situation-action associations. The hippocampus, ventral striatum, and dorsal striatum make unique contributions to each system, but how information processing in each of these structures supports these systems is unknown. Recent work has shown covert representations of future paths in hippocampus and of future rewards in ventral striatum. We developed analyses in order to use a comparative methodology and apply the same analyses to all three structures. Covert representations of future paths and reward were both absent from the dorsal striatum. In contrast, dorsal striatum slowly developed situation representations that selectively represented action-rich parts of the task. This triple dissociation suggests that the different roles these structures play are due to differences in information-processing mechanisms.

Replay of behavioral sequences in the hippocampus during sharp wave ripple complexes (SWRs) provides a potential mechanism for memory consolidation and the learning of knowledge structures. Current hypotheses imply that replay should straightforwardly reflect recent experience. However, we find these hypotheses to be incompatible with the content of replay on a task with two distinct behavioral sequences (A and B). We observed forward and backward replay of B even when rats had been performing A for >10 min. Furthermore, replay of nonlocal sequence B occurred more often when B was infrequently experienced. Neither forward nor backward sequences preferentially represented highly experienced trajectories within a session. Additionally, we observed the construction of never-experienced novel-path sequences. These observations challenge the idea that sequence activation during SWRs is a simple replay of recent experience. Instead, replay reflected all physically available trajectories within the environment, suggesting a potential role in active learning and maintenance of the cognitive map., (Copyright 2010 Elsevier Inc. All rights reserved.)