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Mind the gap: binding experiences across space and time in the human hippocampus.

ABSTRACT: A fundamental goal in memory research is to understand what class of learning problem the hippocampus is uniquely designed to solve. While much controversy surrounds the particular types of memories the hippocampus is thought to support, one hypothesized function possibly linking divergent frameworks is the capacity to bind mnemonic representations across spatial and temporal gaps in our experience. In our current functional magnetic resonance imaging (fMRI) study, we systematically controlled the extent to which a target and an event detail have to be integrated across spatiotemporal discontiguities during associative memory formation. Although the encoding task, the type of association, and subsequent memory performance were held constant, engagement of the hippocampus during successful associative binding was directly modulated by increases in spatial and temporal discontiguities across episodic elements. These results suggest that a core mnemonic function of the hippocampus is to bridge representational gaps in our experience.

SUBMITTER: Staresina BP

PROVIDER: S-EPMC2726251 | biostudies-literature | 2009 Jul

REPOSITORIES: biostudies-literature

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Mind the gap: binding experiences across space and time in the human hippocampus.

Staresina Bernhard P BP Davachi Lila L

Neuron 20090701 2

A fundamental goal in memory research is to understand what class of learning problem the hippocampus is uniquely designed to solve. While much controversy surrounds the particular types of memories the hippocampus is thought to support, one hypothesized function possibly linking divergent frameworks is the capacity to bind mnemonic representations across spatial and temporal gaps in our experience. In our current functional magnetic resonance imaging (fMRI) study, we systematically controlled t ...[more]

PMID: 19640484

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Project description:The vertebrate hippocampus is believed to use recurrent connectivity in area CA3 to support episodic memory recall from partial cues. This brain area also contains place cells, whose location-selective firing fields implement maps supporting spatial memory. Here we show that place cells emerge in networks trained to remember temporally continuous sensory episodes. We model CA3 as a recurrent autoencoder that recalls and reconstructs sensory experiences from noisy and partially occluded observations by agents traversing simulated arenas. The agents move in realistic trajectories modeled from rodents and environments are modeled as continuously varying, high-dimensional, sensory experience maps (spatially smoothed Gaussian random fields). Training our autoencoder to accurately pattern-complete and reconstruct sensory experiences with a constraint on total activity causes spatially localized firing fields, i.e., place cells, to emerge in the encoding layer. The emergent place fields reproduce key aspects of hippocampal phenomenology: a) remapping (maintenance of and reversion to distinct learned maps in different environments), implemented via repositioning of experience manifolds in the network's hidden layer, b) orthogonality of spatial representations in different arenas, c) robust place field emergence in differently shaped rooms, with single units showing multiple place fields in large or complex spaces, and d) slow representational drift of place fields. We argue that these results arise because continuous traversal of space makes sensory experience temporally continuous. We make testable predictions: a) rapidly changing sensory context will disrupt place fields, b) place fields will form even if recurrent connections are blocked, but reversion to previously learned representations upon remapping will be abolished, c) the dimension of temporally smooth experience sets the dimensionality of place fields, including during virtual navigation of abstract spaces.

Dataset Information

Mind the gap: binding experiences across space and time in the human hippocampus.

Publications

Mind the gap: binding experiences across space and time in the human hippocampus.

Similar Datasets

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