Cited by 989Memory and Neural MechanismsSpatial Cognition and NavigationNeural dynamics and brain function

Path integration and cognitive mapping in a continuous attractor neural network model

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Samsonovich, Alexei, McNaughton, Bruce L.·1997·The Journal of Neuroscience

Abstract

A minimal synaptic architecture is proposed for how the brain might perform path integration by computing the next internal representation of self-location from the current representation and from the perceived velocity of motion. In the model, a place-cell assembly called a “chart” contains a two-dimensional attractor set called an “attractor map” that can be used to represent coordinates in any arbitrary environment, once associative binding has occurred between chart locations and sensory inputs. In hippocampus, there are different spatial relations among place fields in different environments and behavioral contexts. Thus, the same units may participate in many charts, and it is shown that the number of uncorrelated charts that can be encoded in the same recurrent network is potentially quite large. According to this theory, the firing of a given place cell is primarily a cooperative effect of the activity of its neighbors on the currently active chart. Therefore, it is not particularly useful to think of place cells as encoding any particular external object or event. Because of its recurrent connections, hippocampal field CA3 is proposed as a possible location for this “multichart” architecture; however, other implementations in anatomy would not invalidate the main concepts. The model is implemented numerically both as a network of integrate-and-fire units and as a “macroscopic” (with respect to the space of states) description of the system, based on a continuous approximation defined by a system of stochastic differential equations. It provides an explanation for a number of hitherto perplexing observations on hippocampal place fields, including doubling, vanishing, reshaping in distorted environments, acquiring directionality in a two-goal shuttling task, rapid formation in a novel environment, and slow rotation after disorientation. The model makes several new predictions about the expected properties of hippocampal place cells and other cells of the proposed network.

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Crossref · 10.1523/jneurosci.17-15-05900.1997

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  • Remapping mechanisms have been modeled using multistable attractor dynamics for several decades.

    “The mechanisms of remapping in biological circuits are still poorly understood, but have been modeled using multistable attractor dynamics for several decades (Samsonovich and McNaughton, 1997)”

    From Remapping in a recurrent neural network model of navigation and context inference (2023) · cites this paper as Samsonovich and McNaughton, 1997

  • Classical multistable attractor models typically store completely decorrelated spatial maps.

    “Classical models typically store completely decorrelated spatial maps (Samsonovich and McNaughton, 1997)”

    From Remapping in a recurrent neural network model of navigation and context inference (2023) · cites this paper as Samsonovich and McNaughton, 1997

  • Classical models typically store completely decorrelated spatial maps, while our RNNs produce distinct maps that are, by construction, perfectly correlated in the position readout dimensions.

    “Classical models typically store completely decorrelated spatial maps (Samsonovich and McNaughton, 1997), while our RNNs produce distinct maps that are, by construction, perfectly correlated in the position readout dimensions.”

    From Remapping in a recurrent neural network model of navigation and context inference (2023) · cites this paper as Samsonovich and McNaughton, 1997

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Cites

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Research works printed but not linked: 13

  1. Amaral DG, Witter M P (1995) Hippocampal formation. In: The rat nervous system, 2nd edition (Paxinos G, ed), pp 443-493. San Diego: Academic.
  2. Blair HT (1996) Simulation of a thalamocortical circuit for computing directional heading in the rat. In: Advances in neural information processing systems, Vol 8 (Touretzky DS, Moser MC, Hasselmo M E, eds), pp 152-158.
  3. Knierim JJ, Kudrimoti HS, Skaggs W E, McNaughton BL (1996) The interaction between vestibular cues and visual landmark learning in spatial navigation. In: Perception, memory, and emotion: frontiers in neuroscience (Ono T, McNaughton B, Molotchnikoff S, Rolls E, Nishijo H, eds), pp 343-357. New York: Elsevier Science.
  4. Maurer R, Se ´guinot V (1995) What is modeling for? A critical review of the models of path integration. J Theor Biol 175:457-475.
  5. Mehta M, Barnes CA, McNaughton BL (1997) E xperience-dependent, asymmetric expansion of hippocampal place fields. Proc Natl Acad Sci USA, in press.
  6. O'Keefe J (1979) A review of the hippocampal place cells. Prog Neuro- biol 13:419 -439.
  7. Samsonovich A (1997) Attractor-map theory of the hippocampal repre- sentation of space. PhD thesis, The University of Arizona.
  8. Samsonovich A, McNaughton BL (1997) A model of formation of the hippocampal spatial code. Soc Neurosci Abstr, in press.
  9. Shepherd GM (1990) The synaptic organization of the brain, 3rd edi- tion. New York: Oxford UP.
  10. Skaggs WE (1995) Relations between the theta rhythm and activity patterns of hippocampal neurons. PhD thesis, The University of Arizona.
  11. Skaggs WE, Knierim JJ, Kudrimoti HS, McNaughton BL (1995) A model of the neural basis of the rat's sense of direction. In: Advances in neural information processing systems (Tesauro G, Touretzky D, Leen T, eds), pp 130 -180.
  12. Sparks DL, Lee C, Rohrer W H (1990) Population coding of the direc- tion, amplitude and velocity of saccadic eye movements by neurons in the superior colliculus. Cold Spring Harbor Symposium on Quantita- tive Biology, Vol LV, pp 805-811. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  13. Strogatz SH (1994) Nonlinear dynamics and chaos. Reading, MA: Addison-Wesley.

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Authors
Samsonovich, A., & McNaughton, B. L.
Affiliations
University of Arizona (US)
Venue
The Journal of Neuroscience
Published
1997-08-01
Volume
17
Issue
15
Pages
5900-5920
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2149422514
Cited by
989
References
5
Citations by year
2026: 33 · 2025: 46 · 2024: 47 · 2023: 49 · 2022: 34 · 2021: 34 · 2020: 30 · 2019: 48 · 2018: 27 · 2017: 35 · 2016: 32 · 2015: 43 · 2014: 36 · 2013: 43 · 2012: 30
FWCI
13.63
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Office of Naval Research
  • National Institute of Neurological Disorders and Stroke (R37NS020331, R01NS020331, NS-20331)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
path integration, cognitive mapping, continuous attractor networks, place cells, hippocampus, CA3, integrate-and-fire neurons, stochastic differential equations, recurrent neural networks
MeSH terms
Animals, Brain Mapping, Hippocampus, Neural Networks, Computer, Rats

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