Cited by 540Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeural dynamics and brain function

Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons

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Bittner, Katie C, Grienberger, Christine, Vaidya, Sachin P, Milstein, Aaron D, Macklin, John J, Suh, Junghyup, Tonegawa, Susumu, Magee, Jeffrey C·2015·Nature Neuroscience

Abstract

Feature-selective firing allows networks to produce representations of the external and internal environments. Despite its importance, the mechanisms generating neuronal feature selectivity are incompletely understood. In many cortical microcircuits the integration of two functionally distinct inputs occurs nonlinearly through generation of active dendritic signals that drive burst firing and robust plasticity. To examine the role of this processing in feature selectivity, we recorded CA1 pyramidal neuron membrane potential and local field potential in mice running on a linear treadmill. We found that dendritic plateau potentials were produced by an interaction between properly timed input from entorhinal cortex and hippocampal CA3. These conjunctive signals positively modulated the firing of previously established place fields and rapidly induced new place field formation to produce feature selectivity in CA1 that is a function of both entorhinal cortex and CA3 input. Such selectivity could allow mixed network level representations that support context-dependent spatial maps.

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  • Plateau potentials on their own do not change synaptic strength.

    “These plateau potentials on their own do not change synaptic strength.”

    From Synaptic memory and CaMKII (2023) · cites this paper as [424]

    The Results section, “Plateau increase the amplitude of incoming input” (page unavailable), says plateau-induced place fields are consistent with increased EPSP amplitude—evidence of strengthened synaptic input. The Discussion (page unavailable) also describes plasticity produced by plateau potentials. The paper therefore makes the contrary point, although it does not isolate a plateau from all concurrent synaptic input. (LLM, conf=0.88)

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  • The data establish a causal relationship between spike-burst activity observed during awake immobility-related behaviors and place field plasticity mechanisms.

    “Thus, our data establish a causal relationship between spike-burst activity observed during awake immobility-related behaviors10,16 and place field plasticity mechanisms.”

    From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [16]

    The Results section, “Impact on sharp wave/ripple related activity” (page unavailable), reports neuronal activity during non-exploratory periods and increased action-potential firing during ripples after place fields were induced. It does not establish that spike bursts during awake immobility cause place-field plasticity; the reported sequence runs from place-field induction during active running to later ripple-related activity. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • Place field formation in CA1 neurons is thought to occur via rapid synaptic plasticity mechanisms at distal entorhinal inputs.

    “Place field formation in CA1 neurons is thought to occur via rapid synaptic plasticity mechanisms at distal entorhinal inputs16,17.”

    From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [16]

    The Discussion (page unavailable) says dendritic plateau potentials can rapidly induce CA1 place fields, likely by strengthening active synaptic inputs. The Introduction (page unavailable) places EC3 inputs on distal dendrites, but the Discussion does not establish that plasticity occurs specifically at those inputs; it says the plasticity should also involve CA3 inputs. (LLM, conf=0.87)

    Experimental — accuracy not yet measured
  • When plateau potentials are coincident with or preceded by several hundreds of milliseconds by a series of subthreshold EPSPs, these EPSPs are potentiated.

    “However, when these plateau potentials are coincident with or are preceded by several hundreds of milliseconds by a series of subthreshold excitatory postsynaptic potentials (EPSPs), these EPSPs are potentiated.”

    From Synaptic memory and CaMKII (2023) · cites this paper as [424]

    The Results section, “Plateau increase the amplitude of incoming input” (page unavailable), reports changes consistent with increased EPSP amplitude after plateau-induced place-field formation. The Discussion (page unavailable) describes strengthening of synaptic inputs active around plateau generation as likely. Neither passage establishes potentiation of a series of subthreshold EPSPs specifically preceding a plateau by several hundred milliseconds. (LLM, conf=0.85)

    Experimental — accuracy not yet measured
  • Input to CA1 from entorhinal cortex provides an instructive signal in the form of large Ca2+-dependent dendritic plateau potentials.

    “Input to CA1 from entorhinal cortex provides an instructive signal in the form of large Ca2+-dependent dendritic plateau potentials (424, 426).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [424]

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Authors
Bittner, K. C., Grienberger, C., Vaidya, S. P., Milstein, A. D., Macklin, J. J., Suh, J., Tonegawa, S., & Magee, J. C.
Affiliations
Howard Hughes Medical Institute (US)
Corresponding author
Magee, Jeffrey C
Venue
Nature Neuroscience
Published
2015-07-13
Volume
18
Issue
8
Pages
1133-1142
ISSN
  • 1097-6256 (ISSN-L)
  • 1546-1726
OpenAlex
W954230352
Cited by
540
References
50
Citations by year
2026: 53 · 2025: 59 · 2024: 57 · 2023: 40 · 2022: 52 · 2021: 49 · 2020: 41 · 2019: 64 · 2018: 52 · 2017: 37 · 2016: 26 · 2015: 9
FWCI
24.87
Type
journal article
Language
en
Open access
Locations
  • Nature Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
  • PMC
Funders
Howard Hughes Medical Institute
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
feature selectivity, hippocampal CA1, place fields, entorhinal cortex, hippocampal CA3, pyramidal neurons, spatial maps, entorhinal-hippocampal circuit, local field potentials
MeSH terms
Animals, Behavior, Animal, Membrane Potentials, Nerve Net, Neurons, Pyramidal Cells, Entorhinal Cortex, Mice, CA1 Region, Hippocampal, CA3 Region, Hippocampal, Spatial Navigation

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