Spatial representation in the hippocampal formation: a history

Moser, Edvard I; Moser, May‐Britt; McNaughton, Bruce L.

doi:10.1038/nn.4653

Cited by 428 publications

(374 citation statements)

References 290 publications

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“…The cooperative spiking of hippocampal PYRs underpins the computation of information-representing assemblies thought to subsequently serve memory-guided behavior (Buzsáki, 2010, Moser et al., 2017). This important idea could lead to the assumption that the circuit-level expression of a memory representation and its behavioral manifestation are the same process.…”

Section: Discussionmentioning

confidence: 99%

A Hippocampus-Accumbens Tripartite Neuronal Motif Guides Appetitive Memory in Space

Trouche

Koren

Doig

et al. 2019

Cell

121

125

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SummaryRetrieving and acting on memories of food-predicting environments are fundamental processes for animal survival. Hippocampal pyramidal cells (PYRs) of the mammalian brain provide mnemonic representations of space. Yet the substrates by which these hippocampal representations support memory-guided behavior remain unknown. Here, we uncover a direct connection from dorsal CA1 (dCA1) hippocampus to nucleus accumbens (NAc) that enables the behavioral manifestation of place-reward memories. By monitoring neuronal ensembles in mouse dCA1→NAc pathway, combined with cell-type selective optogenetic manipulations of input-defined postsynaptic neurons, we show that dCA1 PYRs drive NAc medium spiny neurons and orchestrate their spiking activity using feedforward inhibition mediated by dCA1-connected parvalbumin-expressing fast-spiking interneurons. This tripartite cross-circuit motif supports spatial appetitive memory and associated NAc assemblies, being independent of dorsal subiculum and dispensable for both spatial novelty detection and reward seeking. Our findings demonstrate that the dCA1→NAc pathway instantiates a limbic-motor interface for neuronal representations of space to promote effective appetitive behavior.

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Section: Discussionmentioning

confidence: 99%

A Hippocampus-Accumbens Tripartite Neuronal Motif Guides Appetitive Memory in Space

Trouche

Koren

Doig

et al. 2019

Cell

121

125

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“…[110] Aquatic vertebrates, such as tadpoles and lampreys, also display the same bilateral action of CNs as observed in mammals. As sensorimotor networks evolve, interneurons allow computation of multimodal sensory integration, as evidenced in the nematode, [68,77,114,115] while in the fly, [79,80,100,101,116] rodent, [117] and mammalian brain, [50][51][52][53][118][119][120][121] the presence of layers of network structures demonstrates a hierarchical organization. Sensorimotor control loops are observed in the fly, where navigation is achieved via a combination of path integration (tracking position relative to a reference point) and known visual landmarks.…”

Section: Independent Of the Evolutionary Age Of The Organism Inhibitmentioning

confidence: 99%

“…[100,102] Ultimately, reciprocal inhibition is a computation common to all organisms throughout evolution, and inhibitory neurons remain central to the performance of such networks. As sensorimotor networks evolve, interneurons allow computation of multimodal sensory integration, as evidenced in the nematode, [68,77,114,115] while in the fly, [79,80,100,101,116] rodent, [117] and mammalian brain, [50][51][52][53][118][119][120][121] the presence of layers of network structures demonstrates a hierarchical organization. Within this circuit, excitatory and inhibitory pathways create bidirectional circuits and contribute to sensorimotor control loops [83] as convergent projections targeting the circuit enable the integration of multimodal bottom-up and top-down information while divergent projections enable modulation of a broad range of sensorimotor circuits throughout the brain.…”

Section: Independent Of the Evolutionary Age Of The Organism Inhibitmentioning

confidence: 99%

Prominent Inhibitory Projections Guide Sensorimotor Computation: An Invertebrate Perspective

Hughes

Celikel

2019

BioEssays

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From single-cell organisms to complex neural networks, all evolved to provide control solutions to generate context-and goal-specific actions. Neural circuits performing sensorimotor computation to drive navigation employ inhibitory control as a gating mechanism as they hierarchically transform (multi)sensory information into motor actions. Here, the focus is on this literature to critically discuss the proposition that prominent inhibitory projections form sensorimotor circuits. After reviewing the neural circuits of navigation across various invertebrate species, it is argued that with increased neural circuit complexity and the emergence of parallel computations, inhibitory circuits acquire new functions. The contribution of inhibitory neurotransmission for navigation goes beyond shaping the communication that drives motor neurons, and instead includes encoding of emergent sensorimotor representations. A mechanistic understanding of the neural circuits performing sensorimotor computations in invertebrates will unravel the minimum circuit requirements driving adaptive navigation.

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“…Downstream regions like the entorhinal cortex and the hippocampus use this information to derive a stable representation of the world and one's own position, direction and speed in it (Hartley et al, 2014;Moser et al, 2017). Together, such spatial representations are often referred to as 'cognitive map' and are thought to fundamentally shape our memories and guide behavior (O'Keefe and Nadel, 1978).…”

Section: Introductionmentioning

confidence: 99%

Behavior-dependent directional tuning in the human visual-navigation network

Nau

Schröder²,

Frey

et al. 2019

Preprint

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The brain derives cognitive maps from sensory experience to guide memory formation and behavior. Despite extensive efforts, it still remains unclear how the underlying population activity relates to active behavior and memory performance. Here, we combined 7T-fMRI with a kernelbased encoding model of virtual navigation to map world-centered directional tuning across the human cortex. First, we present an in-depth analysis of directional tuning in visual, retrosplenial and parahippocampal cortices and the hippocampus. Second, we show that tuning strength, width and topology of this directional code during memory-guided navigation depend on successful encoding of the environment. Finally, we show that participants' locomotory state influences this tuning in sensory and mnemonic regions such as the hippocampus. We demonstrate a direct link between neural population tuning and human cognition and show that high-level memory processing interacts with network-wide environmental coding in the service of behavior.

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Spatial representation in the hippocampal formation: a history

Cited by 428 publications

References 290 publications

A Hippocampus-Accumbens Tripartite Neuronal Motif Guides Appetitive Memory in Space

A Hippocampus-Accumbens Tripartite Neuronal Motif Guides Appetitive Memory in Space

Prominent Inhibitory Projections Guide Sensorimotor Computation: An Invertebrate Perspective

Behavior-dependent directional tuning in the human visual-navigation network

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