Hippocampus-dependent emergence of spatial sequence coding in retrosplenial cortex

D, Mao; Neumann, Adam; Sun, Jianjun; Bonin, Vincent; Mohajerani, Majid H.; McNaughton, Bruce L.

doi:10.1073/pnas.1803224115

Cited by 104 publications

(114 citation statements)

References 40 publications

(46 reference statements)

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“…RSC spatial responses have been primary examined during track running paradigms (Smith and Mizumori, 2012; Alexander and Nitz, 2015; Alexander and Nitz, 2017; Vedder et al, 2016; Mao et al, 2017; Mao et al, 2018; Miller et al, 2019). Accordingly, we questioned whether there was any relationship between stable firing correlates in free exploration and route running.…”

Section: Resultsmentioning

confidence: 99%

“…Despite possessing dense reciprocal connectivity with numerous regions known to support spatial cognition, few reports have examined spatial response properties of neurons within the RSC. Most assessments of functional properties of RSC neurons have occurred in rodents performing track running tasks (Smith and Mizumori, 2012; Alexander and Nitz, 2015; Alexander and Nitz, 2017; Vedder et al, 2016; Mao et al, 2017; Mao et al, 2018; Miller et al, 2019). Track running experiments have revealed that RSC neurons exhibit spatial correlates with conjunctive sensitivity to allocentric and egocentric coordinate systems (among others) simultaneously (Alexander and Nitz, 2015).…”

Section: Introductionmentioning

confidence: 99%

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Egocentric boundary vector tuning of the retrosplenial cortex

Alexander

Carstensen

Hinman

et al. 2019

Preprint

121

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31The retrosplenial cortex is reciprocally connected with a majority of structures implicated in 32 spatial cognition and damage to the region itself produces numerous spatial impairments. 33However, in many ways the retrosplenial cortex remains understudied. Here, we sought to 34 characterize spatial correlates of neurons within the region during free exploration in two-35 dimensional environments. We report that a large percentage of retrosplenial cortex neurons 36 have spatial receptive fields that are active when environmental boundaries are positioned at a 37 specific orientation and distance relative to the animal itself. We demonstrate that this vector-38 based location signal is encoded in egocentric coordinates, localized to the dysgranular 39 retrosplenial sub-region, independent of self-motion, and context invariant. Further, we identify a 40 sub-population of neurons with this response property that are synchronized with the 41 hippocampal theta oscillation. Accordingly, the current work identifies a robust egocentric spatial 42 code in retrosplenial cortex that can facilitate spatial coordinate system transformations and 43 support the anchoring, generation, and utilization of allocentric representations. 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 108 From a connectivity standpoint, the retrosplenial cortex (RSC) is an excellent candidate to 109 examine egocentric representations during navigation. Further, theoretical work has posited that 110 RSC forms a computational hub for supporting coordinate transformations (Byrne et al., 2007;111 Clark et al., 2018; Rounds et al., 2018; Bicankski and Burgess, 2018). RSC is composed of two 112 interconnected sub-regions, dysgranular (dRSC) and granular (gRSC), which have slightly 113 different connectivity with cortical and subcortical regions (Shibata et al., 2009). dRSC (in mice 114 agranular RSC) is positioned along the dorsal surface of the brain and possesses biased 115 interconnectivity with association, sensory, and motor processing regions that code in 116

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Egocentric boundary vector tuning of the retrosplenial cortex

Alexander

Carstensen

Hinman

et al. 2019

Preprint

121

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“…This latter mechanism fits well into our conceptualization of systems consolidation; we contend that this is a feature, rather than a side effect, of replay. Although more work is needed for full confidence in this contention -such as experiments that carefully track and manipulate the influence of the hippocampus on cortical representations 15 -we think the evidence already points to replay having a critical and active role in driving consolidation across memory systems.…”

Section: Comparing Integration and Contextual Binding Accounts Of Memmentioning

confidence: 99%

Active and effective replay: systems consolidation reconsidered again

Antony

Schapiro

2019

Nat Rev Neurosci

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“…Older adults have been found to be 6 slower in learning novel environments and have problems to retrieve this newly learnt information 7 later, even when the results are controlled for their slower learning rate ( the first to be affected during the progression from healthy aging to Alzheimer's disease (AD; Braak & 16 Del Tredici, 2015), the neural mechanisms for age-related deficits in spatial learning are still poorly 17 understood, even in healthy older adults. Studies in rodents and non-human primates showed that 18 place cells in the CA3 subfield of the hippocampus exhibit higher firing rates in aged animals during 19 navigation, and they fail to encode new information when rats encounter novel environments (Thomé,20 Gray O'Mara, 2012). In humans, in contrast, there is evidence for an age-related activity reduction in the 24 hippocampus and medial parietal areas during spatial navigation (Konishi et al, 2013;Moffat, Elkins, 25 & Resnick, 2006).…”

Section: Introductionmentioning

confidence: 99%

Increased hippocampal excitability and altered learning dynamics mediate cognitive mapping deficits in human aging

Diersch

Valdés-Herrera

Tempelmann

et al. 2019

Preprint

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1Learning the spatial layout of a novel environment is associated with dynamic activity changes in the 2 hippocampus and in medial parietal areas. With advancing age, the ability to learn spatial 3 environments deteriorates substantially but the underlying neural mechanisms are unknown. Here, 4 we report findings from a behavioral and a fMRI experiment where older and younger adults 5 performed a spatial learning task in a photorealistic virtual environment. We modeled individual 6 learning states using a Bayesian state-space model and found that activity in retrosplenial 7 cortex/parieto-occipital sulcus and anterior hippocampus did not change systematically as a function 8 learning in older compared to younger adults across repeated episodes in the environment. 9Moreover, effective connectivity analyses revealed that the age-related learning deficits are linked to 10 an increase in hippocampal excitability. Together, these results provide important insights into how 11 human aging affects computations in the brain's navigation system, highlighting the critical role of the 12 hippocampus. 13 unknown whether this effect also pertains to age-related problems in retrieving the layout of spatial 1 environments. 2

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Hippocampus-dependent emergence of spatial sequence coding in retrosplenial cortex

Cited by 104 publications

References 40 publications

Egocentric boundary vector tuning of the retrosplenial cortex

Egocentric boundary vector tuning of the retrosplenial cortex

Active and effective replay: systems consolidation reconsidered again

Increased hippocampal excitability and altered learning dynamics mediate cognitive mapping deficits in human aging

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