The rodent hippocampus spontaneously generates bursts of neural activity (replay) that can depict spatial trajectories to reward locations, suggesting a role in model-based behavioral control. A ...largely separate literature emphasizes reward revaluation as the litmus test for such control, yet the content of hippocampal replay under revaluation conditions is unknown. We examined the content of awake replay events following motivational shifts between hunger and thirst. On a T-maze offering free choice between food and water outcomes, rats shifted their behavior toward the restricted outcome, but replay content was shifted away from the restricted outcome. This effect preceded experience on the task each day and did not reverse with experience. These results demonstrate that replay content is not limited to reflecting recent experience or trajectories toward the preferred goal and suggest a role for motivational states in determining replay content.
Highlights • Several brain areas display sequences of neural activity generated on the basis of internal dynamics. • These sequences occur in brain areas implicated in memory and goal-directed ...behavior. • Such sequences can contribute to internal simulation and recombination of information. • Data as well as computational models suggest these sequences are instrumental for on-line choice and learning. • These models use sequences to infer future events and plan actions from previously acquired knowledge.
The encoding and storage of experience by the hippocampus is essential for the formation of episodic memories and the transformation of individual experiences into semantic structures such as maps ...and schemas. The rodent hippocampus compresses ongoing experience into repeating theta sequences, but the factors determining the content of theta sequences are not understood. Here we first show that the spatial paths represented by theta sequences in rats extend farther in front of the rat during acceleration and higher running speeds and begin farther behind the rat during deceleration. Second, the length of the path is directly related to the length of the theta cycle and the number of gamma cycles in it. Finally, theta sequences represent the environment in segments or 'chunks'. These results imply that information encoded in theta sequences is subject to powerful modulation by behavior and task variables. Furthermore, these findings suggest a potential mechanism for the cognitive 'chunking' of experience.
The hippocampus is thought to enable the encoding and retrieval of ongoing experience, the organization of that experience into structured representations like contexts, maps, and schemas, and the ...use of these structures to plan for the future. A central goal is to understand what the core computations supporting these functions are, and how these computations are realized in the collective action of single neurons. A potential access point into this issue is provided by 'splitter cells', hippocampal neurons that fire differentially on the overlapping segment of trajectories that differ in their past and/or future. However, the literature on splitter cells has been fragmented and confusing, owing to differences in terminology, behavioral tasks, and analysis methods across studies. In this review, we synthesize consistent findings from this literature, establish a common set of terms, and translate between single-cell and ensemble perspectives. Most importantly, we examine the combined findings through the lens of two major theoretical ideas about hippocampal function: representation of temporal context and latent state inference. We find that unique signature properties of each of these models are necessary to account for the data, but neither theory, by itself, explains all of its features. Specifically, the temporal gradedness of the splitter signal is strong support for temporal context, but is hard to explain using state models, while its flexibility and task-dependence is naturally accounted for using state inference, but poses a challenge otherwise. These theories suggest a number of avenues for future work, and we believe their application to splitter cells is a timely and informative domain for testing and refining theoretical ideas about hippocampal function.
Neural activity in the nucleus accumbens (NAc) is thought to track fundamentally value-centric quantities linked to reward and effort. However, the NAc also contributes to flexible behavior in ways ...that are difficult to explain based on value signals alone, raising the question of if and how nonvalue signals are encoded in NAc. We recorded NAc neural ensembles while head-fixed mice performed an odor-based biconditional discrimination task where an initial discrete cue modulated the behavioral significance of a subsequently presented reward-predictive cue. We extracted single-unit and population-level correlates related to the cues and found value-independent coding for the initial, context-setting cue. This context signal occupied a population-level coding space orthogonal to outcome-related representations and was predictive of subsequent behaviorally relevant responses to the reward-predictive cues. Together, these findings support a gating model for how the NAc contributes to behavioral flexibility and provide a novel population-level perspective from which to view NAc computations.
Information processing in the rodent hippocampus is fundamentally shaped by internally generated sequences (IGSs), expressed during two different network states: theta sequences, which repeat and ...reset at the ∼8 Hz theta rhythm associated with active behavior, and punctate sharp wave‐ripple (SWR) sequences associated with wakeful rest or slow‐wave sleep. A potpourri of diverse functional roles has been proposed for these IGSs, resulting in a fragmented conceptual landscape. Here, we advance a unitary view of IGSs, proposing that they reflect an inferential process that samples a policy from the animal's generative model, supported by hippocampus‐specific priors. The same inference affords different cognitive functions when the animal is in distinct dynamical modes, associated with specific functional networks. Theta sequences arise when inference is coupled to the animal's action–perception cycle, supporting online spatial decisions, predictive processing, and episode encoding. SWR sequences arise when the animal is decoupled from the action–perception cycle and may support offline cognitive processing, such as memory consolidation, the prospective simulation of spatial trajectories, and imagination. We discuss the empirical bases of this proposal in relation to rodent studies and highlight how the proposed computational principles can shed light on the mechanisms of future‐oriented cognition in humans.
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.
► Hippocampal replay content is inconsistent with current proposals for replay generation ► The content of hippocampal replay reflects the behavioral demands of the task ► “Replay” content includes never and rarely experienced shortcut trajectories ► Hippocampal replay may help in learning a cognitive map and prevent catastrophic interference
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.
► Hippocampus, dorsal, and ventral striatum show different information processing ► HC, but not dStr, shows covert representations ahead of the animal at choice points ► vStr, but not dStr, shows covert reward representations at choice points ► dStr, but not vStr or HC, slowly reorganizes representation with experience
Local field potentials (LFPs) recorded from the human and rodent ventral striatum (vStr) exhibit prominent, behaviorally relevant gamma-band oscillations. These oscillations are related to local ...spiking activity and transiently synchronize with anatomically related areas, suggesting a possible role in organizing vStr activity. However, the origin of vStr gamma is unknown. We recorded vStr gamma oscillations across a 1.4 mm
grid spanned by 64 recording electrodes as male rats rested and foraged for rewards, revealing a highly consistent power gradient originating in the adjacent piriform cortex. Phase differences across the vStr were consistently small (<15°) and current source density analysis further confirmed the absence of local sink-source pairs in the vStr. Reversible occlusions of the ipsilateral (but not contralateral) nostril, known to abolish gamma oscillations in the piriform cortex, strongly reduced vStr gamma power and the occurrence of transient gamma-band events. These results imply that local circuitry is not a major contributor to gamma oscillations in the vStr LFP and that piriform cortex is an important driver of gamma-band oscillations in the vStr and associated limbic areas.
The ventral striatum (vStr) is an area of anatomical convergence in circuits underlying motivated behavior, but it remains unclear how its inputs from different sources interact. A major proposal about how neural circuits may switch dynamically between convergent inputs is through temporal organization reflected in local field potential (LFP) oscillations. Our results show that, in the rat, the mechanisms controlling gamma-band oscillations in the vStr LFP are primarily located in the in the adjacent piriform cortex rather than in the vStr itself, providing a novel interpretation of previous rodent work on gamma oscillations in the vStr and related circuits and an important consideration for future work seeking to use oscillations in these areas as biomarkers for behavioral and neurological disorders.
Decision making is impacted by uncertainty and risk (i.e., variance). Activity in the orbitofrontal cortex, an area implicated in decision making, covaries with these quantities. However, this ...activity could reflect the heightened salience of situations in which multiple outcomes—reward and reward omission—are expected. To resolve these accounts, rats were trained to respond to cues predicting 100%, 67%, 33%, or 0% reward. Consistent with prior reports, some orbitofrontal neurons fired differently in anticipation of uncertain (33% and 67%) versus certain (100% and 0%) reward. However, over 90% of these neurons also fired differently prior to 100% versus 0% reward (or baseline) or prior to 33% versus 67% reward. These responses are inconsistent with risk but fit well with the representation of acquired salience linked to the sum of cue-outcome and cue-no-outcome associative strengths. These results expand our understanding of how the orbitofrontal cortex might regulate learning and behavior.
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► Orbitofrontal neurons are reported to signal risk or uncertainty ► Here we show that this activity violates predictions for risk encoding ► Instead orbitofrontal activity is better explained by salience ► This has implications for neuroeconomic models and orbitofrontal function
Risk is salient, yet salience can be safe. Here Ogawa et al. took advantage of this asymmetry to dissociate neural correlates of risk and salience. The results indicate that the activity of risk-responsive neurons in the orbitofrontal cortex tracks salience.
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