Behavior determines the hippocampal spatial mapping of a multisensory environment

Radvansky, Brad A.; Oh, Jee Young; Climer, Jason R.; Dombeck, Daniel A.

doi:10.1016/j.celrep.2021.109444

Cited by 40 publications

(41 citation statements)

References 78 publications

(100 reference statements)

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“…It is possible that, rather than encoding non-spatial “what” information ( O’Keefe and Krupic, 2021 ), “cue cells” in our study could actually be place cells encoding “where” information within a different reference frame ( van Dijk and Fenton, 2018 ; Radvansky et al, 2021 ). However, we observed robust responses in the same cue cells even to an odor cue administered randomly in each lap ( Figures 4A – 4C ).…”

Section: Discussionmentioning

confidence: 96%

Parallel processing of sensory cue and spatial information in the dentate gyrus

et al. 2022

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During exploration, animals form an internal map of an environment by combining information about landmarks and the animal's movement, a process that depends on the hippocampus. The dentate gyrus (DG) is the first stage of the hippocampal circuit where self-motion (''where'') and sensory cue information (''what'') are integrated, but it remains unknown how DG neurons encode this information during cognitive map formation. Using two-photon calcium imaging in mice running on a treadmill along with online cue manipulation, we identify robust sensory cue responses in DG granule cells. Cue cell responses are stable, stimulus-specific, and accompanied by inhibition of nearby neurons. This demonstrates the existence of ''cue cells'' in addition to better characterized ''place cells'' in the DG. We hypothesize that the DG supports parallel channels of spatial and non-spatial information that contribute distinctly to downstream computations and affect roles of the DG in spatial navigation and episodic memory.

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Section: Discussionmentioning

confidence: 96%

Parallel processing of sensory cue and spatial information in the dentate gyrus

et al. 2022

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“…Therefore, our observation of concurrent cue-specific and cue-independent spatial representations could not have been confounded by factors like task requirement or reward setup. Moreover, our findings suggest that previous studies reporting cue-independent spatial representations might have missed parallel cue-specific representations reflected in a different form of neural activity 13, 14, 16 . For this reason, the current study highlights the importance of investigating complementary neural phenomena to obtain a more complete understanding of the neural representations underlying cognitive maps.…”

Section: Discussionmentioning

confidence: 59%

“…When the sensory inputs for encoding the same physical space changed, previous studies have observed either cue-specific spatial representations in the hippocampus 9 , or cue-independent spatial representations in RSC 14 and in the brain-wide functional connectivity pattern 16 . A recent study found that whether altering spatial inputs invoked cue-specific or cue-independent spatial representations in the hippocampus depended on whether different cue types were congruent in defining the reward location 13 . Taken together, previous studies have observed either cue-specific or cue-independent spatial representations but not both at the same time in the same spatial context.…”

Section: Discussionmentioning

confidence: 99%

“…Studies in rodents usually manipulated the availability of visual information by switching a light on and off, but the results are mixed as to whether this manipulation would induce hippocampal remapping [10][11][12] . Recently, Radvansky and colleagues (2021) showed that whether a common map or distinct maps were recruited for visual and odor cues depended on the behavioral relevance of these cues, i.e., whether different cue types were congruent or incongruent in defining a reward location 13 . In RSC, researchers have also observed neurons exhibiting positionselective firing 14,15 ; these place-cell-like cells maintained the same firing patterns when the environment was illuminated vs. dark 14 , suggesting cue-independent spatial representations.…”

Section: Introdctionmentioning

confidence: 99%

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Coexistence of Cue-specific and Cue-independent Spatial Representations for Landmarks and Self-motion Cues in Human Retrosplenial Cortex

Chen

Wei

Wolbers

2022

Preprint

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Landmark-based and self-motion-based navigation are two fundamental forms of spatial navigation, which involve distinct cognitive mechanisms. A critical question is whether these two navigation modes invoke common or distinct spatial representations for a given environment in the brain. While a number of electrophysiological studies in non-human animals have investigated this question but yielded inconsistent results, it still awaits rigorous investigation in humans. In the current study, we combined ultra-high field fMRI at 7T and desktop virtual reality with state-of-the-art fMRI data analysis techniques. Using a novel linear track navigation task, we dissociated the use of landmarks and self-motion cues, so that participants used different spatial cues to encode and retrieve the same set of spatial locations. Focusing on the retrosplenial cortex (RSC) and the hippocampus, we observed that RSC contained both cue-specific and cue-independent spatial representations, which were driven by objective location (where the participant was actually located) and subjective location (the participant’s self-reported location), respectively. The hippocampus showed strong functional coupling with RSC and exhibited a similar spatial coding scheme, but with reduced effect sizes. Taken together, the current study demonstrated for the first time concurrent cue-specific and cue-independent spatial representations in RSC in the same spatial context, suggesting that this area might transform cue-specific spatial inputs into coherent cue-independent spatial representations to guide navigation behavior.

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“…Statistical comparisons for CPFE studies were performed using one-way ANOVA followed by Dunnett’s multiple comparisons tests, and dose dependence was assessed by fitting data to a logistic equation (GraphPad Prism v9.3.1). Comparisons for calcium imaging data were made by fitting linear mixed effects models, with statistical significance derived from Kenward-Roger type III & likelihood ratio tests (Bates et al, 2015) using RStudio, 2021.09.0 Build 351 (R Core Team (2021). R: A language and environment for statistical computing.…”

Section: Methodsmentioning

confidence: 99%

Dose-dependent suppression of hippocampal contextual memory formation, place cells, and spatial engrams by the NMDAR antagonist (R)-CPP

Zhu¹,

Perkins²,

Lennertz³

et al. 2022

Preprint

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A common way to study the functional importance of N-methyl-D-aspartate receptors (NMDARs) in hippocampal memory-encoding circuits is by administering NMDAR antagonists. We recently compared the effects of (R,S)-3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid (CPP), a competitive NMDAR antagonist, on suppression of memory in vivo versus suppression of NMDAR-mediated field EPSPs (fEPSPNMDA) and long-term potentiation (LTP) in vitro. Surprisingly, we found that concentrations that block contextual conditioning in vivo are ineffective at blocking the fEPSPNMDA or LTP in vitro. Here we tested one possible explanation for the mismatch—that the hippocampus is relatively resistant to CPP compared to other brain structures engaged in contextual fear conditioning. We used the context pre-exposure facilitation effect (CPFE) paradigm to isolate the hippocampal component of contextual learning, and in-vivo calcium imaging of place cells and spatial engrams to directly assess hippocampal spatial coding. We found that, by both measures, the active enantiomer (R)-CPP did interfere with hippocampal function at concentrations below those that block fEPSPs or LTP. We conclude that the alternative—that CPP interferes with memory by targeting NMDARs in interneurons rather than pyramidal neurons—is the more likely explanation.

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Behavior determines the hippocampal spatial mapping of a multisensory environment

Cited by 40 publications

References 78 publications

Parallel processing of sensory cue and spatial information in the dentate gyrus

Parallel processing of sensory cue and spatial information in the dentate gyrus

Coexistence of Cue-specific and Cue-independent Spatial Representations for Landmarks and Self-motion Cues in Human Retrosplenial Cortex

Dose-dependent suppression of hippocampal contextual memory formation, place cells, and spatial engrams by the NMDAR antagonist (R)-CPP

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