Over the river, through the woods: cognitive maps in the hippocampus and orbitofrontal cortex

Wikenheiser, Andrew M.; Schoenbaum, Geoffrey

doi:10.1038/nrn.2016.56

Cited by 306 publications

(274 citation statements)

References 176 publications

(164 reference statements)

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“…In the present experiments, analyses were focused on HPC and DLS memory systems; components of broader networks known to mediate goal-directed and habit behavioral learning (Redish, 2016;Wikenheiser & Schoenbaum, 2016). The mPFC is reciprocally connected with both the HPC and striatum.…”

Section: Discussionmentioning

confidence: 99%

Hippocampal BDNF regulates a shift from flexible, goal‐directed to habit memory system function following cocaine abstinence

2019

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The transition from recreational drug use to addiction involves pathological learning processes that support a persistent shift from flexible, goal‐directed to habit behavioral control. Here, we examined the molecular mechanisms supporting altered function in hippocampal (HPC) and dorsolateral striatum (DLS) memory systems following abstinence from repeated cocaine. After 3 weeks of cocaine abstinence (experimenter‐ or self‐administered), we tested new behavioral learning in male rats using a dual‐solution maze task, which provides an unbiased approach to assess HPC‐ versus DLS‐dependent learning strategies. Dorsal hippocampus (dHPC) and DLS brain tissues were collected after memory testing to identify transcriptional adaptations associated with cocaine‐induced shifts in behavioral learning. Our results demonstrate that following prolonged cocaine abstinence rats show a bias toward the use of an inflexible, habit memory system (DLS) in lieu of a more flexible, easily updated memory system involving the HPC. This memory system bias was associated with upregulation and downregulation of brain‐derived neurotrophic factor (BDNF) gene expression and transcriptionally permissive histone acetylation (acetylated histone H3, AcH3) in the DLS and dHPC, respectively. Using viral‐mediated gene transfer, we overexpressed BDNF in the dHPC during cocaine abstinence and new maze learning. This manipulation restored HPC‐dependent behavioral control. These findings provide a system‐level understanding of altered plasticity and behavioral learning following cocaine abstinence and inform mechanisms mediating the organization of learning and memory more broadly.

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Section: Discussionmentioning

confidence: 99%

Hippocampal BDNF regulates a shift from flexible, goal‐directed to habit memory system function following cocaine abstinence

2019

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“…When presented with a stimulus to be assigned to a concept, hippocampus—mPFC interactions may trigger reactivation of similar, concept-relevant learning experiences. Medial PFC also influences hippocampal encoding by compressing memory representations to emphasize features that capture commonalities across events [21], consistent with its hypothesized role in forming mental models of latent structures that are not directly observable [13, 14, 68]. The retrieved memories may then be used to predict a concept label for the current experience.…”

Section: Integrated Maps Of Conceptual Spacementioning

confidence: 99%

Memory integration constructs maps of space, time, and concepts

Morton

Sherrill

Preston³

2017

Current Opinion in Behavioral Sciences

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Recent evidence demonstrates that new events are learned in the context of their relationships to existing memories. Within the hippocampus and medial prefrontal cortex, related memories are represented by integrated codes that connect events experienced at different times and places. Integrated codes form the basis of spatial, temporal, and conceptual maps of experience. These maps represent information that goes beyond direct experience and support generalization behaviors that require knowledge be used in new ways. The degree to which an individual memory is integrated into a coherent map is determined by its spatial, temporal, and conceptual proximity to existing knowledge. Integration is observed over a wide range of scales, suggesting that memories contain information about both broad and fine-grained contexts.

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“…While hippocampus is best known as a cognitive map of space (O’Keefe and Nadel, 1978; Redish, 1999), the OFC has recently been cast in similar terms, as a map of abstract concepts such as task state (Schuck et al, 2016; Wilson et al, 2014). These ideas share an emphasis on the flexible use of previous learning to guide behavior when the reward structure of the world is unknown, ambiguous, or changing (Wikenheiser and Schoenbaum, 2016). Despite this convergence, few studies have examined how perturbing interactions between OFC and hippocampus affects behavior or neural activity in either region.…”

Section: Introductionmentioning

confidence: 99%

“…Such trial blocks have been argued to constitute “abstract contexts” or states (Saez et al, 2015), the use of which has been proposed to depend on OFC (Wilson et al, 2014). Here we test whether such outcome-relevant block or state representations depend on output from hippocampus (Wikenheiser and Schoenbaum, 2016). …”

Section: Introductionmentioning

confidence: 99%

Suppression of Ventral Hippocampal Output Impairs Integrated Orbitofrontal Encoding of Task Structure

Wikenheiser¹,

Marrero-Garcia²,

Schoenbaum

2017

Neuron

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Summary The hippocampus and orbitofrontal cortex (OFC) both make important contributions to decision making and other cognitive processes. However, despite anatomical links between the two, few studies have tested the importance of hippocampal–OFC interactions. Here, we recorded OFC neurons in rats performing a decision making task while suppressing activity in a key hippocampal output region, the ventral subiculum. OFC neurons encoded information about expected outcomes and rats’ responses. With hippocampal output suppressed, rats were slower to adapt to changes in reward contingency, and OFC encoding of response information was strongly attenuated. In addition, ventral subiculum inactivation prevented OFC neurons from integrating information about features of outcomes to form holistic representations of the outcomes available in specific trial blocks. These data suggest that the hippocampus contributes to OFC encoding of both concrete, low-level features of expected outcomes, and abstract, inferred properties of the structure of the world, such as task state.

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Over the river, through the woods: cognitive maps in the hippocampus and orbitofrontal cortex

Cited by 306 publications

References 176 publications

Hippocampal BDNF regulates a shift from flexible, goal‐directed to habit memory system function following cocaine abstinence

Hippocampal BDNF regulates a shift from flexible, goal‐directed to habit memory system function following cocaine abstinence

Memory integration constructs maps of space, time, and concepts

Suppression of Ventral Hippocampal Output Impairs Integrated Orbitofrontal Encoding of Task Structure

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