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Cited by 148Memory and Neural MechanismsSpatial Cognition and NavigationNeurogenesis and neuroplasticity mechanisms

Framing Spatial Cognition: Neural Representations of Proximal and Distal Frames of Reference and Their Roles in Navigation

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Knierim, James J., Hamilton, Derek A.·2011·Physiological Reviews
DOI 10.1152/physrev.00021.2010PMC PMC3251945
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Abstract

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 known places and landmarks in a common allocentric reference frame or unitary global map, accessible as a whole, and can operate to infer spatial relationships between any represented elements.

    “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 teleost spatial strategies necessarily involve complex learning and memory capabilities and require flexible representational mechanisms, the most remarkable of which is allocentric navigation based on map-like spatial memory.

    “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]

    Section II.C, “What is Learned?” (page not provided), describes cognitive maps that guide flexible navigation, including novel shortcuts. Section IV, “Summary and Concluding Comments” (page not provided), says animals can use cognitive mapping strategies and track locations in multiple reference frames. These passages support the map-based navigation component, but they do not establish the claim about teleost strategies or that those strategies necessarily require complex learning and memory capabilities. (LLM, conf=0.84)

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  • The hippocampus of tetrapods is 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.

    “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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3 of the 271 references couldn’t be matched to a known paper.

Research works printed but not linked: 10

  1. [23]Carr H Maze studies with the white rat. Journal of Animal Behavior 1917 7 259 275
  2. [33]Cressant A Muller RU Poucet B Further study of the control of place cell firing by intra-apparatus objects. Hippocampus 1999 9 423 431 10495023
  3. [82]Hartley T Burgess N Lever C Cacucci F O'Keefe J Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 2000 10 369 379 10985276
  4. [95]Hubbert HB Lashley KS Retroactive association and the elimination of errors in the maze. Journal of Animal Behavior 1917 7 130 138
  5. [112]Knierim JJ Wiener SI Taube JS Coupling between head direction cells and place cells: Influences of landmarks, self-motion, and intrinsic circuitry. Head Direction Cells and the Neural Mechanisms Underlying Directional Orientation 2004 MIT Press Cambridge, MA
  6. [191]Rolls ET A theory of hippocampal function in memory. Hippocampus 1996 6 601 620 9034849
  7. [196]Save E Nerad L Poucet B Contribution of multiple sensory information to place field stability in hippocampal place cells. Hippocampus 2000 10 64 76 10706218
  8. [203]Shapiro ML Tanila H Eichenbaum H Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 1997 7 624 642 9443059
  9. [221]Steele RJ Morris RGM Delay-dependent impairment of a matching-to-place task with chronic and intrahippocampal infusion of the NMDA-antagonist D-AP5. Hippocampus 1999 9 118 136 10226773
  10. [239]Touretzky DS Redish AD Theory of rodent navigation based on interacting representations of space. Hippocampus 1996 6 247 270 8841825

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Authors
Knierim, J. J., & Hamilton, D. A.
Affiliations
Johns Hopkins University (US)
Corresponding author
Knierim, James J.
ORCID
Venue
Physiological Reviews
Publisher
American Physiological Society
Published
2011-10
Volume
91
Issue
4
Pages
1245-1279
ISSN
  • 0031-9333 (ISSN-L)
  • 1522-1210
DOI
10.1152/physrev.00021.2010
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
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
  • Physical Sciences › Engineering › Automotive Engineering › 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

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