The Statistical Structure of the Hippocampal Code for Space as a Function of Time, Context, and Value

Lee, Jae Sung; Briguglio, John; Cohen, Jack B.; Romani, Sandro; Lee, Albert K.

doi:10.1016/j.cell.2020.09.024

Cited by 113 publications

(160 citation statements)

References 87 publications

(182 reference statements)

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“…at the collection port) would provide a useful representation for learning about the target in the context of these foraging tasks. Moreover, unlike tasks that deliver reward at a variable target location(s) [71][72][73] , we did not find clear evidence for an enrichment of place fields nor enhanced decoding resolution 71 in the vicinity of the target location. dCA1 inactivation during foraging trajectories had no clear effect on performance (Fig.…”

contrasting

confidence: 95%

“…One of the most robust features that determines dCA1 activity is an animal's allocentric position in space 2 . The performance of a task, depending upon its demands, can enhance [71][72][73] or reduce 49,77 the relative contribution of spatial position to hippocampal and entorhinal activity 71 . In addition, population activity of dCA1 also represents non-navigational information, such as task events and elapsed intervals 10,14,44,45,78,79 .…”

Section: Discussionmentioning

confidence: 99%

“…Hippocampal representations, specifically in CA1, are thought to allow for conjunctive coding of a reward location ( i.e. , spatial position ⋂ reward probability [71][72][73] ). The reward is in a constant location in our tasks and thus it is also not clear how a pure reward representation 73 ( i.e.…”

mentioning

confidence: 99%

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Construction of a hippocampal cognitive map depends upon spatial context

Jiang¹,

Xu²,

Dudman³

2021

Preprint

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The hippocampus encodes both spatial and non-spatial features of an environment thought to be critical to guide navigational trajectories and associative learning, respectively. These seemingly dichotomous roles have been reconciled in a proposed cognitive map - a representation of environment structure abstracted away from specific behavioral demands. However, the extent to which a cognitive map is independent of behavioral demands remains unclear because direct comparisons across environments with common structure but different spatial/behavioral context is lacking. Here we compare behaviors in mice trained to navigate to a hidden target in a physical arena and manipulate a joystick to a virtual target to collect a delayed reward. Comparison of behaviors with an artificial agent revealed a common algorithmic basis for learned foraging trajectories in both contexts. Imaging CA1 neural activity revealed a similar map-like encoding of active foraging; however, detailed analysis of ensemble activity, optogenetic inactivation, and modeling revealed a context-specific functional dissociation. In a navigational context, CA1 was critical for retrospective evaluation of spatial trajectories, but dispensable for initiation. In a non-navigational context, CA1 activity was critical for initiation and planning foraging trajectories. This work highlights how construction of a cognitive map to facilitate idiosyncratic behavioral demands7 is critical for foraging in diverse spatial contexts.

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confidence: 95%

Section: Discussionmentioning

confidence: 99%

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Construction of a hippocampal cognitive map depends upon spatial context

Jiang¹,

Xu²,

Dudman³

2021

Preprint

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“…Based on the proportion of reward coding neurons reported previously ( Gauthier and Tank, 2018 ), the number of cells recorded in our task and the percentage of stimulation responsive cells, we estimate that on average only one or two reward coding neurons may have been activated during our Reward-PC stimulations. In addition, recent experiments report an increased field density of neurons encoding conjunctively the reward and the location rather than a purely reward location-specific sub-population ( Lee et al., 2019 ). Future experiments will be required to fully dissociate these populations and assess their functional roles independently.…”

Section: Discussionmentioning

confidence: 99%

Targeted Activation of Hippocampal Place Cells Drives Memory-Guided Spatial Behavior

Robinson

Descamps

Russell

et al. 2020

Cell

200

105

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“…Another possible explanation of differences that we have observed in Arc expression across the CA1 longitudinal axis could be related to cellular excitability and intrinsic recruitment propensity. In dorsal CA1, several studies have reported that cellular recruitment does not follow a Poisson process (random draw with replacement), but instead is gamma or log-normally distributed [29, 30, 42]. Recently, Lee et al (2020) found that most cells in CA1 are virtually “silent” and have no place fields across multiple, large environments, while some cells have single fields, and a minority of cells have multiple fields in multiple environments – in keeping with recruitment statistics of hippocampal cells in multi-room IEG studies [42].…”

Section: Resultsmentioning

confidence: 99%

Behaviour-drivenArcexpression is greater in dorsal than ventral CA1 regardless of task or sex differences

Lee

McHugh

Morgan

et al. 2021

Preprint

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Evidence from genetic, behavioural, anatomical, and physiological study suggests that the hippocampus functionally differs across its longitudinal (dorsoventral or septotemporal) axis. Although, how to best characterize functional and representational differences in the hippocampus across its long axis remains unclear. While some suggest that the hippocampus can be divided into dorsal and ventral subregions that support distinct cognitive functions, others posit that these regions vary in their granularity of representation, wherein spatial-temporal resolution decreases in the ventral (temporal) direction. Importantly, the cognitive and granular hypotheses make distinct predictions on cellular recruitment dynamics under conditions when animals perform tasks with qualitatively different cognitive-behavioural demands. The cognitive function account implies that dorsal and ventral cellular recruitment differs depending on relevant behavioural demands, while the granularity account suggests similar recruitment dynamics regardless of the nature of the task performed. Here, we quantified cellular recruitment with the immediate early gene (IEG) Arc across the entire longitudinal CA1 axis in female and male rats performing spatial-and fear-guided memory tasks. Our results show that recruitment is greater in dorsal than ventral CA1 regardless of task or sex. This experimentum crucis leads to the strong inference that the granularity hypothesis for functional differences across the longitudinal axis in the rodent hippocampus is correct.

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The Statistical Structure of the Hippocampal Code for Space as a Function of Time, Context, and Value

Cited by 113 publications

References 87 publications

Construction of a hippocampal cognitive map depends upon spatial context

Construction of a hippocampal cognitive map depends upon spatial context

Targeted Activation of Hippocampal Place Cells Drives Memory-Guided Spatial Behavior

Behaviour-drivenArcexpression is greater in dorsal than ventral CA1 regardless of task or sex differences

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