Head Direction Cell Representations Maintain Internal Coherence during Conflicting Proximal and Distal Cue Rotations: Comparison with Hippocampal Place Cells
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Place cells of the hippocampal formation encode a spatial representation of the environment, and the orientation of this representation is apparently governed by the head direction cell system. The representation of a well explored environment by CA1 place cells can be split when there is conflicting information from salient proximal and distal cues, because some place fields rotate to follow the distal cues, whereas others rotate to follow the proximal cues (Knierim, 2002a). In contrast, the CA3 representation is more coherent than CA1, because the place fields in CA3 tend to rotate in the same direction (Lee et al., 2004). The present study tests whether the head direction cell network produces a split representation or remains coherent under these conditions by simultaneously recording both CA1 place cells and head direction cells from the thalamus. In agreement with previous studies, split representations of the environment were observed in ensembles of CA1 place cells in ∼75% of the mismatch sessions, in which some fields followed the counterclockwise rotation of proximal cues and other fields followed the clockwise rotation of distal cues. However, of 225 recording sessions, there was not a single instance of the head direction cell ensembles revealing a split representation of head direction. Instead, in most of the mismatch sessions, the head direction cell tuning curves rotated as an ensemble clockwise (94%) and in a few sessions rotated counterclockwise (6%). The findings support the notion that the head direction cells may be part of an attractor network bound more strongly to distal landmarks than proximal landmarks, even under conditions in which the CA1 place representation loses its coherence.
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Mammalian PCs are notable for their representational flexibility, while other spatial cells exhibit more coherent shifts across environments.
“Mammalian PCs are notable for their representational flexibility10,40,41, while other spatial cells exhibit more coherent shifts across environments42–44.”
From A population code for spatial representation in the zebrafish telencephalon (2024) · cites this paper as [43]
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“However, unlike place fields, split head direction representations of the mismatch environment were never observed (Taube and Burton, 1995; Zugaro et al., 2001).”
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“Experimentally, the head direction circuitry has been shown to be anchored to distal cues, retaining its internal cardinal axes when an environment is rotated [32].”
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Schøyen (2022) · doi:10.1101/2022.08.18.504379 · Cited by 27 · see citing works
- Authors
- Yoganarasimha, D., Yu, X., & Knierim, J. J.
- Affiliations
- The University of Texas Health Science Center at Houston (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-01-11
- Volume
- 26
- Issue
- 2
- Pages
- 622-631
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC1388189
- OpenAlex
- W1979697475
- Cited by
- 149
- References
- 4
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 9 · 2023: 9 · 2022: 5 · 2021: 9 · 2020: 12 · 2019: 6 · 2018: 11 · 2017: 7 · 2016: 4 · 2015: 7 · 2014: 13 · 2013: 8 · 2012: 8
- FWCI
- 2.91
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Public Health Service
- National Institute of Mental Health (KO2 MH63297, K02MH063297)
- National Institute of Neurological Disorders and Stroke (R01 NS39456, R01NS039456)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
- Keywords
- head direction cells, place cells, CA1, CA3, hippocampus, spatial representation, landmark-based navigation, attractor networks, thalamus, internal coherence
- MeSH terms
- Animals, Cues, Electrodes, Implanted, Hippocampus, Male, Memory, Nerve Net, Orientation, Rotation, Space Perception, Spatial Behavior, Thalamus, Head Movements, Rats, Long-Evans, Rats
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