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Framing Spatial Cognition: Neural Representations of Proximal and Distal Frames of Reference and Their Roles in Navigation
Open accessAbstract
The most common behavioral test of hippocampus-dependent, spatial learning and memory is the Morris water task, and the most commonly studied behavioral correlate of hippocampal neurons is the spatial specificity of place cells. Despite decades of intensive research, it is not completely understood how animals solve the water task and how place cells generate their spatially specific firing fields. Based on early work, it has become the accepted wisdom in the general neuroscience community that distal spatial cues are the primary sources of information used by animals to solve the water task (and similar spatial tasks) and by place cells to generate their spatial specificity. More recent research, along with earlier studies that were overshadowed by the emphasis on distal cues, put this common view into question by demonstrating primary influences of local cues and local boundaries on spatial behavior and place-cell firing. This paper first reviews the historical underpinnings of the "standard" view from a behavioral perspective, and then reviews newer results demonstrating that an animal's behavior in such spatial tasks is more strongly controlled by a local-apparatus frame of reference than by distal landmarks. The paper then reviews similar findings from the literature on the neurophysiological correlates of place cells and other spatially correlated cells from related brain areas. A model is proposed by which distal cues primarily set the orientation of the animal's internal spatial coordinate system, via the head direction cell system, whereas local cues and apparatus boundaries primarily set the translation and scale of that coordinate system.
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“Such hypothetical memory representations presumably encode the spatial relationships between all the known places and landmarks in a common allocentric reference frame or unitary global map, accessible as a whole, and that can operate to infer the spatial relationships between any of the represented elements.”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [73]
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“Some of these spatial strategies necessarily involve complex learning and memory capabilities and require the concurrence of flexible representational mechanisms, the most remarkable of which probably is allocentric navigation based on map-like spatial memory”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [73]
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“The hippocampus of tetrapods seems to be essential in tasks requiring the formation of a memory of the spatial relationships of multiple elements and cues of the environment and those demanding the flexible expression of previously acquired spatial knowledge [72,73,75,76].”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [73]
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Metadata
- Authors
- Knierim, J. J., & Hamilton, D. A.
- Affiliations
- Johns Hopkins University (US)
- Corresponding author
- Knierim, James J.
- Venue
- Physiological Reviews
- Publisher
- American Physiological Society
- Published
- 2011-10
- Volume
- 91
- Issue
- 4
- Pages
- 1245-1279
- ISSN
- 0031-9333 (ISSN-L)
- 1522-1210
- PMC
- PMC3251945
- OpenAlex
- W2151688688
- Cited by
- 148
- References
- 271
- Citations by year
- 2026: 2 · 2025: 15 · 2024: 13 · 2023: 8 · 2022: 10 · 2021: 11 · 2020: 10 · 2019: 10 · 2018: 13 · 2017: 8 · 2016: 8 · 2015: 14 · 2014: 6 · 2013: 13 · 2012: 4
- FWCI
- 0.71
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Physiological Reviews (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Alcohol Abuse and Alcoholism (R21AA015356, AA-015356, R01AA019462, AA019462)
- National Institute of Neurological Disorders and Stroke (R01NS039456, NS-039456)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- spatial cognition, reference frames, place cells, hippocampus, spatial learning and memory, Morris water task, head direction cells, spatial navigation, local boundaries, spatial coordinate system
- MeSH terms
- Animals, Behavior, Animal, Cognition, Cues, Hippocampus, Learning, Orientation, Spatial Behavior, Models, Animal, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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