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      Differential functions of the dorsal and intermediate regions of the hippocampus for optimal goal-directed navigation in VR space

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      eLife
      eLife Sciences Publications, Ltd
      episodic memory, decision-making, valence learning, virtual environment, inactivation, septotemporal hippocampus, Rat

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          Abstract

          Goal-directed navigation requires the hippocampus to process spatial information in a value-dependent manner, but its underlying mechanism needs to be better understood. Here, we investigated whether the dorsal (dHP) and intermediate (iHP) regions of the hippocampus differentially function in processing place and its associated value information. Rats were trained in a place-preference task involving reward zones with different values in a visually rich virtual reality environment where two-dimensional navigation was possible. Rats learned to use distal visual scenes effectively to navigate to the reward zone associated with a higher reward. Inactivation of both dHP and iHP with muscimol altered the efficiency and precision of wayfinding behavior, but iHP inactivation induced more severe damage, including impaired place preference. Our findings suggest that the iHP is more critical for value-dependent navigation toward higher-value goal locations.

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          Most cited references53

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          CircStat: AMATLABToolbox for Circular Statistics

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            Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat.

            The medial prefrontal cortex (mPFC) has been associated with diverse functions including attentional processes, visceromotor activity, decision making, goal directed behavior, and working memory. Using retrograde tracing techniques, we examined, compared, and contrasted afferent projections to the four divisions of the mPFC in the rat: the medial (frontal) agranular (AGm), anterior cingulate (AC), prelimbic (PL), and infralimbic (IL) cortices. Each division of the mPFC receives a unique set of afferent projections. There is a shift dorsoventrally along the mPFC from predominantly sensorimotor input to the dorsal mPFC (AGm and dorsal AC) to primarily 'limbic' input to the ventral mPFC (PL and IL). The AGm and dorsal AC receive afferent projections from widespread areas of the cortex (and associated thalamic nuclei) representing all sensory modalities. This information is presumably integrated at, and utilized by, the dorsal mPFC in goal directed actions. In contrast with the dorsal mPFC, the ventral mPFC receives significantly less cortical input overall and afferents from limbic as opposed to sensorimotor regions of cortex. The main sources of afferent projections to PL/IL are from the orbitomedial prefrontal, agranular insular, perirhinal and entorhinal cortices, the hippocampus, the claustrum, the medial basal forebrain, the basal nuclei of amygdala, the midline thalamus and monoaminergic nuclei of the brainstem. With a few exceptions, there are few projections from the hypothalamus to the dorsal or ventral mPFC. Accordingly, subcortical limbic information mainly reaches the mPFC via the midline thalamus and basal nuclei of amygdala. As discussed herein, based on patterns of afferent (as well as efferent) projections, PL is positioned to serve a direct role in cognitive functions homologous to dorsolateral PFC of primates, whereas IL appears to represent a visceromotor center homologous to the orbitomedial PFC of primates.
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              Finite scale of spatial representation in the hippocampus.

              To determine how spatial scale is represented in the pyramidal cell population of the hippocampus, we recorded neural activity at multiple longitudinal levels of this brain area while rats ran back and forth on an 18-meter-long linear track. CA3 cells had well-defined place fields at all levels. The scale of representation increased almost linearly from <1 meter at the dorsal pole to approximately 10 meters at the ventral pole. The results suggest that the place-cell map includes the entire hippocampus and that environments are represented in the hippocampus at a topographically graded but finite continuum of scales.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                16 July 2024
                2024
                : 13
                : RP97114
                Affiliations
                [1 ] Department of Brain and Cognitive Sciences, Seoul National University ( https://ror.org/04h9pn542) Seoul Republic of Korea
                [2 ] Department of Psychiatry and Behavioral Sciences, University of Washington ( https://ror.org/00cvxb145) Seattle United States
                University of Texas at Austin ( https://ror.org/00hj54h04) United States
                University of Texas at Austin ( https://ror.org/00hj54h04) United States
                University of Texas at Austin United States
                Seoul National University Seoul Republic of Korea
                University of Washington Seattle United States
                Seoul National University Seoul Republic of Korea
                Author information
                https://orcid.org/0009-0000-7929-6403
                https://orcid.org/0000-0001-5364-5433
                https://orcid.org/0000-0003-3760-4257
                Article
                97114
                10.7554/eLife.97114
                11251721
                39012807
                c18d4082-a770-497a-9363-e91de8db248d
                © 2024, Hwang et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 21 February 2024
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003725, National Research Foundation of Korea;
                Award ID: 2019R1A2C2088799
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003725, National Research Foundation of Korea;
                Award ID: 2021R1A4A2001803
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003725, National Research Foundation of Korea;
                Award ID: 2022M3E5E8017723
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003725, National Research Foundation of Korea;
                Award ID: 2019H1A2A1073456
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                The intermediate region of the hippocampus is critical for strategic goal-directed navigation to the higher-value location, whereas the dorsal hippocampus implements the precise targeting of the goal location.
                prc

                Life sciences
                episodic memory,decision-making,valence learning,virtual environment,inactivation,septotemporal hippocampus,rat

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