Parallel Pathways Provide Hippocampal Spatial Information to Prefrontal Cortex

Messanvi, Fany; Berkun, Kathleen; Perkins, Aster; Chudasama, Yogita

doi:10.1523/jneurosci.0846-22.2022

Cited by 5 publications

(4 citation statements)

References 102 publications

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“…Further studies are required to determine the mechanisms of this DH-OFC interaction (what is the direction of this interaction, what pathways are involved, and when in the acquisition or consolidation process are these pathways involved?). Note that direct connections between the OFC and DH are extremely sparse/nonexistent, therefore DH-OFC interactions likely involve a complex, multisynaptic circuit 11,[40][41][42][43][44][45] . Questions also remain regarding the degree of abstraction of the cognitive map acquired by rats in our tasks (does prior contextual knowledge promote context-dependent learning only within the training context and for cues/outcomes of the same modality/valence as in training, or is context-dependent learning promoted more generally?)…”

Section: Discussionmentioning

confidence: 99%

Partially dissociable roles of the Orbitofrontal cortex and dorsal Hippocampus in context-dependent (hierarchical) reward prediction and contextual inference in learning

Peterson,

Chavira,

Arango

et al. 2024

Preprint

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Reward cues are often ambiguous; what is good in one context is not necessarily good in another context. To solve this ambiguity, animals form hierarchical associations in which the context acts as a gatekeeper in the retrieval of the appropriate cue-evoked memory, ensuring context-appropriate behavior. These hierarchical associative structures also influence future learning by promoting the formation of new context-dependent associations (leading to the inference of context-dependency for new associations). The orbitofrontal cortex (OFC) and the dorsal hippocampus (DH) are both proposed to encode a “cognitive map” that includes the representation of hierarchical, context-dependent, associations. However the causal role of the OFC and DH in the different functional properties of hierarchical associations remains controversial. Here we used chemogenetic inactivations, in rats, to examine the role of OFC and DH in 1) the contextual regulation of performance, and 2) the contextual learning bias conferred by hierarchical associations. We show that OFC is required for both manifestations of hierarchical associations. In contrast, DH contribution appears limited to the contextual learning bias. This study provides novel insight into the different functional properties of context-dependent hierarchical associations, and establishes the OFC as a critical orchestrator of these different contextual effects.

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Section: Discussionmentioning

confidence: 99%

Partially dissociable roles of the Orbitofrontal cortex and dorsal Hippocampus in context-dependent (hierarchical) reward prediction and contextual inference in learning

Peterson,

Chavira,

Arango

et al. 2024

Preprint

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“…PFC and hippocampus are strongly connected by direct and indirect pathways. Indeed, monosynaptic projections from the ventral hippocampus as well as two multi-synaptic pathways via the thalamus and via the perirhinal and lateral entorhinal cortex 34 connect these two regions. Moreover, a discrete monosynaptic projection from the PFC to dorsal CA1 in mice was recently reported by Malik et al (2022) 35 whereas involvement of both these structures in spatial memory consolidation in mice has been documented by Tuscher et al (2018) 36 .…”

Section: Discussionmentioning

confidence: 99%

Effect of learning on slow gamma propagation between hippocampus and cortex in the wild-type and AD mice

Blinowska

Kamiński

Macrez

et al. 2022

Sci Rep

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Slow gamma oscillations (20–50 Hz) have been suggested to coordinate information transfer between brain structures involved in memory formation. Whereas the involvement of slow gamma in memory processing was studied by means of correlation between the gamma power and the occurrence of a given event (sharp wave ripples (SWRs), cortical transients), our approach consists of the analysis of the transmission of slow gamma itself. We use the method based on Granger causality principle—direct Directed Transfer Function, which allows to determine directed propagation of brain activity, including bidirectional flows. Four cortical sites along with CA1 ipsi- and contralateral were recorded in behaving wild-type and APP/PS1 mice before and after learning session of a spatial memory task. During slow wave sleep propagation of slow gamma was bidirectional, forming multiple loops of interaction which involved both CA1 and some of cortical sites. In episodes coincident with SWRs the number and strength of connectivity pathways increased in both groups compared to episodes without SWRs. The effect of learning was expressed only in APP/PS1 mice and consisted in strengthening of the slow gamma transmission from hippocampus to cortex as well as between both CA1 which may serve more efficient transmission of information from impaired CA1.

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“…This finding is interesting because the CEAc receives substantial inputs from the CA1 ( Cenquizca & Swanson, 2007 ) and the SUBv ( Canteras & Swanson, 1992 ). In addition, contextual information could reach the CEA via multiple relays from the HF ( Canteras & Swanson, 1992 ; Cenquizca & Swanson, 2007 ), most notably, via inputs from the medial PFC ( Hurley et al, 1991 ; Messanvi et al, 2023 ) and BLA.…”

Section: Novel Contextmentioning

confidence: 99%

“…Both medial prefrontal cortical regions analyzed, the PL and ILA, had increased Fos induction in the novel context condition. Both regions receive heavy inputs from the HF ( Hoover & Vertes, 2007 ; Cenquizca & Swanson, 2007 ; Messanvi et al, 2023 ) and can impact the HF via the RE ( McKenna & Vertes, 2004 ; Vertes 2002 ; Hallock et al, 2016 ). In addition, the mPFC is well positioned to control feeding behavior.…”

Section: Novel Contextmentioning

confidence: 99%

Activation patterns in male and female forebrain circuitries during food consumption under novelty

Greiner,

Witt,

Moran

et al. 2023

Preprint

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The influence of novelty on feeding behavior is significant and can override both homeostatic and hedonic drives due to the uncertainty of potential danger. Previous work found that novel food hypophagia is enhanced in a novel environment and that males habituate faster than females. The current study’s aim was to identify the neural substrates of separate effects of food and context novelty. Adult male and female rats were tested for consumption of a novel or family food in either a familiar or in a novel context. Test-induced Fos expression was measured in the amygdalar, thalamic, striatal, and prefrontal cortex regions that are important for appetitive responding, contextual processing, and reward motivation. Food and context novelty induced strikingly different activation patterns. Novel context induced Fos robustly in almost every region analyzed, including the central (CEA) and basolateral complex nuclei of the amygdala, the thalamic paraventricular (PVT) and reuniens nuclei, the nucleus accumbens (ACB), the medial prefrontal cortex prelimbic and infralimbic areas, and the dorsal agranular insular cortex (AI). Novel food induced Fos in a few select regions: the CEA, anterior basomedial nucleus of the amygdala, anterior PVT, and posterior AI. There were also sex differences in activation patterns. The capsular and lateral CEA had greater activation for male groups and the anterior PVT, ACB ventral core and shell had greater activation for female groups. These activation patterns and correlations between regions, suggest that distinct functional circuitries control feeding behavior when food is novel and when eating occurs in a novel environment.

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Parallel Pathways Provide Hippocampal Spatial Information to Prefrontal Cortex

Cited by 5 publications

References 102 publications

Partially dissociable roles of the Orbitofrontal cortex and dorsal Hippocampus in context-dependent (hierarchical) reward prediction and contextual inference in learning

Partially dissociable roles of the Orbitofrontal cortex and dorsal Hippocampus in context-dependent (hierarchical) reward prediction and contextual inference in learning

Effect of learning on slow gamma propagation between hippocampus and cortex in the wild-type and AD mice

Activation patterns in male and female forebrain circuitries during food consumption under novelty

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