Ventral Striatal Dopamine Increases following Hippocampal Sharp-Wave Ripples.

Leading theories suggest that hippocampal replay drives offline learning through coupling with an internal teaching signal such as ventral striatal dopamine (DA); however, the relationship between hippocampal replay and dopamine is unknown. Simultaneous recording of putative hippocampal replay events (dorsal CA1 sharp-wave ripples, SWRs) and fiber photometry of ventral striatal DA in mice revealed a significant increase in DA following SWRs, peaking ∼0.3 s after SWRs.

Adapt-A-Maze: An Open-Source Adaptable and Automated Rodent Behavior Maze System.

Mazes are a fundamental and widespread tool in behavior and systems neuroscience research in rodents, especially in spatial navigation and spatial memory investigations in behaving animals. However, their form and inflexibility often restrict potential experimental paradigms that involve multiple or adaptive maze designs. Unique layouts often lead to elevated costs, whether financially or in terms of time investment from scientists.

Optogenetic Mapping of Rhythmic Phase-Dependent Excitability in the Mouse Striatum.

The striatum is thought to switch flexibly between multiple converging inputs to support adaptive behavior. The "communication through coherence" (CTC) hypothesis is a potential mechanism to implement such a flexible switching. For CTC to work in the striatum, striatal excitability must show rhythmic fluctuations, such as those related to the phase of the striatal local field potential (LFP).

Awake replay: off the clock but on the job.

Hippocampal replay is widely thought to support two key cognitive functions: online decision-making and offline memory consolidation. In this review, we take a closer look at the hypothesized link between awake replay and online decision-making in rodents, and find only marginal evidence in support of this role. By contrast, the consolidation view is bolstered by new computational ideas and recent data, suggesting that (i) replay performs offline fictive learning for later goal-oriented behavior; and (ii) replay tags memories prior to sleep, prioritizing them for consolidation.

Paradoxical replay can protect contextual task representations from destructive interference when experience is unbalanced.

Experience replay is a powerful mechanism to learn efficiently from limited experience. Despite several decades of compelling experimental results, the factors that determine which experiences are selected for replay remain unclear. A particular challenge for current theories is that on tasks that feature unbalanced experience, rats paradoxically replay the less-experienced trajectory.

Temporal context and latent state inference in the hippocampal splitter signal.

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.

Context coding in the mouse nucleus accumbens modulates motivationally relevant information.

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.

Between-subject prediction reveals a shared representational geometry in the rodent hippocampus.

The rodent hippocampus constructs statistically independent representations across environments ("global remapping") and assigns individual neuron firing fields to locations within an environment in an apparently random fashion, processes thought to contribute to the role of the hippocampus in episodic memory. This random mapping implies that it should be challenging to predict hippocampal encoding of a given experience in one subject based on the encoding of that same experience in another subject. Contrary to this prediction, we find that by constructing a common representational space across rats in which neural activity is aligned using geometric operations (rotation, reflection, and translation; "hyperalignment"), we can predict data of "right" trials (R) on a T-maze in a target rat based on (1) the "left" trials (L) of the target rat and (2) the relationship between L and R trials from a different source rat.

A framework to identify structured behavioral patterns within rodent spatial trajectories.

Animal behavior is highly structured. Yet, structured behavioral patterns-or "statistical ethograms"-are not immediately apparent from the full spatiotemporal data that behavioral scientists usually collect. Here, we introduce a framework to quantitatively characterize rodent behavior during spatial (e.

Progress and issues in second-order analysis of hippocampal replay.

Patterns of neural activity that occur spontaneously during sharp-wave ripple (SWR) events in the hippocampus are thought to play an important role in memory formation, consolidation and retrieval. Typical studies examining the content of SWRs seek to determine whether the identity and/or temporal order of cell firing is different from chance. Such 'first-order' analyses are focused on a single time point and template (map), and have been used to show, for instance, the existence of preplay.

Complementary Control over Habits and Behavioral Vigor by Phasic Activity in the Dorsolateral Striatum.

Despite clear evidence linking the basal ganglia to the control of outcome insensitivity (i.e., habit) and behavioral vigor (i.

Reward revaluation biases hippocampal replay content away from the preferred outcome.

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.

Gamma Oscillations in the Rat Ventral Striatum Originate in the Piriform Cortex.

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.

Internally generated hippocampal sequences as a vantage point to probe future-oriented cognition.

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 Head-Direction Signal Plays a Functional Role as a Neural Compass during Navigation.

The rat limbic system contains head direction (HD) cells that fire according to heading in the horizontal plane, and these cells are thought to provide animals with an internal compass. Previous work has found that HD cell tuning correlates with behavior on navigational tasks, but a direct, causal link between HD cells and navigation has not been demonstrated. Here, we show that pathway-specific optogenetic inhibition of the nucleus prepositus caused HD cells to become directionally unstable under dark conditions without affecting the animals' locomotion.

Optimizing for generalization in the decoding of internally generated activity in the hippocampus.

The decoding of a sensory or motor variable from neural activity benefits from a known ground truth against which decoding performance can be compared. In contrast, the decoding of covert, cognitive neural activity, such as occurs in memory recall or planning, typically cannot be compared to a known ground truth. As a result, it is unclear how decoders of such internally generated activity should be configured in practice.

Low- and high-gamma oscillations deviate in opposite directions from zero-phase synchrony in the limbic corticostriatal loop.

The loop structure of cortico-striatal anatomy in principle enables both descending (cortico-striatal) and ascending (striato-cortical) influences, but the factors that regulate the flow of information in these loops are not known. We report that low- and high-gamma oscillations (∼50 and ∼80 Hz, respectively) in the local field potential of freely moving rats are highly synchronous between the infralimbic region of the medial prefrontal cortex (mPFC) and the ventral striatum (vStr). Strikingly, high-gamma oscillations in mPFC preceded those in vStr, whereas low-gamma oscillations in mPFC lagged those in vStr, with short (∼1 ms) time lags.

Ventral striatal gamma oscillations are highly variable from trial to trial, and are dominated by behavioural state, and only weakly influenced by outcome value.

The human and rodent ventral striatal local field potentials show striking oscillations in the gamma band (~ 40-100 Hz), which have been linked to aspects of behaviour such as reward anticipation and delivery, movement initiation, learning from feedback, and decision-making. These oscillations show a rich temporal organization, whose relationship with behavioural variables is not well understood. Here, we show that, in rats performing a conditioned approach task, low-gamma and high-gamma oscillations during an immobile reward anticipation epoch were largely insensitive to outcome value, even though rats distinguished behaviourally between different outcomes, and single units encoded outcome value.

Internally generated sequences in learning and executing goal-directed behavior.

A network of brain structures including hippocampus (HC), prefrontal cortex, and striatum controls goal-directed behavior and decision making. However, the neural mechanisms underlying these functions are unknown. Here, we review the role of 'internally generated sequences': structured, multi-neuron firing patterns in the network that are not confined to signaling the current state or location of an agent, but are generated on the basis of internal brain dynamics.

Adaptive properties of differential learning rates for positive and negative outcomes.

The concept of the reward prediction error-the difference between reward obtained and reward predicted-continues to be a focal point for much theoretical and experimental work in psychology, cognitive science, and neuroscience. Models that rely on reward prediction errors typically assume a single learning rate for positive and negative prediction errors. However, behavioral data indicate that better-than-expected and worse-than-expected outcomes often do not have symmetric impacts on learning and decision-making.

Risk-responsive orbitofrontal neurons track acquired salience.

Decision making is impacted by uncertainty and risk (i.e., variance).

Theta phase precession beyond the hippocampus.

The spike timing of spatially tuned cells throughout the rodent hippocampal formation displays a strikingly robust and precise organization. In individual place cells, spikes precess relative to the theta local field potential (6-10 Hz) as an animal traverses a place field. At the population level, theta cycles shape repeated, compressed place cell sequences that correspond to coherent paths.

Segmentation of spatial experience by hippocampal θ sequences.

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.

Ventral striatum: a critical look at models of learning and evaluation.

Extensive evidence implicates the ventral striatum in multiple distinct facets of action selection. Early work established a role in modulating ongoing behavior, as engaged by the energizing and directing influences of motivationally relevant cues and the willingness to expend effort in order to obtain reward. More recently, reinforcement learning models have suggested the notion of ventral striatum primarily as an evaluation step during learning, which serves as a critic to update a separate actor.