Cited by 537Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchSpatial Cognition and Navigation

Increased Attention to Spatial Context Increases Both Place Field Stability and Spatial Memory

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Kentros, Clifford G, Agnihotri, Naveen T, Streater, Samantha, Hawkins, Robert D, Kandel, Eric R·2004·Neuron

Abstract

The hippocampal formation is critical for the acquisition and consolidation of memories. When recorded in freely moving animals, hippocampal pyramidal neurons fire in a location-specific manner: they are "place" cells, comprising a hippocampal representation of the animal's environment. To explore the relationship between place cells and spatial memory, we recorded from mice in several behavioral contexts. We found that long-term stability of place cell firing fields correlates with the degree of attentional demands and that successful spatial task performance was associated with stable place fields. Furthermore, conditions that maximize place field stability greatly increase orientation to novel cues. This suggests that storage and retrieval of place cells is modulated by a top-down cognitive process resembling attention and that place cells are neural correlates of spatial memory. We propose a model whereby attention provides the requisite neuromodulatation to switch short-term homosynaptic plasticity to long-term heterosynaptic plasticity, and we implicate dopamine in this process.

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Crossref · 10.1016/s0896-6273(04)00192-8

Cites

41 of 41 references verified0 citation errors · 0 not checkable

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  • Intermediate fixed points are unstable along a small number of dimensions (saddle fixed points) which funnel neural activity to the appropriate location during a remapping event.

    “In line with observations by Susillo & Barak 31 on a discrete flip-flop task, these intermediate fixed points are unstable along a small number of dimensions (i.e.saddle fixed points; Figure 3D, gold points) which “funnel” neural activity to the appropriate location during a remapping event.”
  • Pharmacological studies have implicated the neurotransmitter dopamine in the stability of hippocampus-dependent memory.

    “Pharmacological studies have implicated the neurotransmitter dopamine in the stability of hippocampus-dependent memory.”
  • Blockade of D1/D5 dopaminergic receptors during exploration of novel environments curtails the stability of new spatial maps.

    “while blockade during exploration of novel environments curtails the stability of new spatial maps8”
  • D1 antagonists prevent the stabilization of place fields in CA1 after the animal enters a new environment.

    “It was found that D1 antagonists prevent this stabilization [20].”

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Authors
Kentros, C. G., Agnihotri, N. T., Streater, S., Hawkins, R. D., & Kandel, E. R.
Affiliations
  • New York State Psychiatric Institute (US)
  • Columbia University (US)
  • Howard Hughes Medical Institute (US)
Corresponding author
Kandel, Eric R
Venue
Neuron
Publisher
Elsevier BV
Published
2004-04
Volume
42
Issue
2
Pages
283-295
ISSN
0896-6273 (ISSN-L)
OpenAlex
W2016985810
Cited by
537
References
41
Citations by year
2026: 29 · 2025: 28 · 2024: 41 · 2023: 32 · 2022: 30 · 2021: 35 · 2020: 25 · 2019: 19 · 2018: 30 · 2017: 28 · 2016: 17 · 2015: 19 · 2014: 22 · 2013: 20 · 2012: 18
FWCI
7.89
Type
journal article
Language
en
Open access
Locations
  • Neuron (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Harvard University
  • National Institutes of Health (NH50733)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
Keywords
place cells, spatial memory, attention, hippocampus, top-down attention, homosynaptic plasticity, heterosynaptic plasticity, dopamine, neuromodulation, mice
MeSH terms
Animals, Attention, Male, Mice, Inbred C57BL, Psychomotor Performance, Spatial Behavior, Pyramidal Cells, Mice

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