Attentive scanning behavior drives one-trial potentiation of hippocampal place fields
Open accessAbstract
The hippocampus is thought to have a critical role in episodic memory by incorporating the sensory input of an experience onto a spatial framework embodied by place cells. Although the formation and stability of place fields requires exploration, the interaction between discrete exploratory behaviors and the specific, immediate and persistent modifications of neural representations required by episodic memory has not been established. We recorded place cells in rats and found that increased neural activity during exploratory head-scanning behaviors predicted the formation and potentiation of place fields on the next pass through that location, regardless of environmental familiarity and across multiple testing days. These results strongly suggest that, during the attentive behaviors that punctuate exploration, place cell activity mediates the one-trial encoding of ongoing experiences necessary for episodic memory.
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Numerous exploratory behaviors linked to episodic learning occur in stationary animals, such as interactions with objects or conspecifics, rearing, and head-scanning behavior.
“Numerous exploratory behaviors linked to episodic learning occur in stationary animals (i.e., at a fixed spatial location), such as interactions with objects or conspecifics, rearing, and head-scanning behavior10–12.”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [10]
The Discussion (page unavailable) describes head scanning during pauses as an investigatory behavior and links scan-related place-field changes to episodic memory. It also calls rearing an investigatory behavior, but says rearing was not analyzed. Our copy does not establish the claimed link for interactions with objects or conspecifics. (LLM, conf=0.86)
Experimental — accuracy not yet measuredRecent studies have shown that head-scanning behavior and rearing are associated with rapid reorganizations of the hippocampal spatial map.
“Indeed, recent studies have shown that head-scanning behavior and rearing are associated with rapid reorganizations of the hippocampal spatial map10,11.”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [10]
The Abstract reports that activity during head scanning was strongly associated with abrupt formation or potentiation of hippocampal place fields. The Discussion says rearing was not analyzed because rats rarely performed it in this task, so this source does not support the rearing part of the claim. Page numbers are not available in our copy. (LLM, conf=0.94)
Experimental — accuracy not yet measuredThe 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 [10]
New place fields can emerge in correspondence with awake immobility-related behaviors such as head scanning and rearing.
“Recent behavioral and electrophysiological studies have shown that new place fields can also emerge in correspondence with awake immobility-related behaviors (e.g., head scanning10, rearing11); however, the underlying plasticity mechanisms have remained unresolved.”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [10]
Spontaneous spike bursts during head-scanning behavior have been shown to precede the rapid emergence of place fields, indicating that place cell spiking alone might be sufficient for engaging plasticity mechanisms during immobility.
“Interestingly, spontaneous spike bursts during head-scanning behavior have been shown to precede the rapid emergence of place fields10, indicating that place cell spiking alone might be sufficient for engaging plasticity mechanisms during immobility.”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [10]
Active exploratory behaviors occurring in stationary animals, like head-scanning behavior or rearing, are associated with fast Type-1-like theta oscillations.
“It is noteworthy that active exploratory behaviors occurring in stationary animals—like head-scanning behavior10 or rearing11—are associated with fast (Type-1-like) theta oscillations.”
From Place and behavioral modulation of hippocampal neurons during immobility (2026) · cites this paper as [10]
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References 53 · Cited by 163
- Authors
- Monaco, J. D., Rao, G., Roth, E. D., & Knierim, J. J.
- Affiliations
- Johns Hopkins University (US)
- University of Delaware (US)
- Corresponding author
- Knierim, James J
- Venue
- Nature Neuroscience
- Published
- 2014-03-30
- Volume
- 17
- Issue
- 5
- Pages
- 725-731
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC4036486
- OpenAlex
- W2133427628
- Cited by
- 163
- References
- 53
- Citations by year
- 2026: 11 · 2025: 14 · 2024: 18 · 2023: 8 · 2022: 15 · 2021: 13 · 2020: 13 · 2019: 15 · 2018: 17 · 2017: 14 · 2016: 10 · 2015: 12 · 2014: 3
- FWCI
- 7.19
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (5p01ns038310-10)
- National Institute of Mental Health (R01MH094146)
- National Institute of Neurological Disorders and Stroke (P01 NS-038310, R01NS039456)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- place cells, hippocampus, exploratory behavior, one-trial learning, episodic memory, spatial memory, rats, environmental familiarity, neural representations
- MeSH terms
- Action Potentials, Animals, Association Learning, Cues, Exploratory Behavior, Hippocampus, Male, Models, Neurological, Neurons, ROC Curve, Rotation, Space Perception, Theta Rhythm, Rats, Long-Evans, Rats
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