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Volume 17, Number 15,
Issue of August 1, 1997
pp. 5900-5920
Copyright ©1997 Society for Neuroscience
Path Integration and Cognitive Mapping in a Continuous Attractor
Neural Network Model
Received Feb. 24, 1997; revised May 14, 1997; accepted May 15, 1997.
Alexei Samsonovich and
Bruce L. McNaughton
Arizona Research Laboratories Division of Neural Systems, Memory
and Aging, The University of Arizona, Tucson, Arizona 85749
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.
Key words:
hippocampus;
CA3;
place cells;
head direction;
dead
reckoning;
path integration;
idiothetic;
allocentric;
spatial learning;
cognitive map;
attractor;
integrate-and-fire
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|
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|
|
|
|
|
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|
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|
|
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|
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|
|
|
|
|
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|
|
|
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|
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|
|
|
|
|
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|
|
|
|
|
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|
|
|
|
|
|
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[Abstract]
[Full Text]
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|
|
|
|
|
|
|
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13(5):
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[Abstract]
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|
|
|
|
|
|
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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105 - 116.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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9298 - 9309.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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20(19):
7463 - 7477.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Doboli, A. A. Minai, and P. J. Best
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1009 - 1043.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
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1(3):
165 - 178.
[Abstract]
[PDF]
|
|
|
|
|
|
|
S. Leutgeb and S. J. Y. Mizumori
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19(15):
6661 - 6672.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. Q. Whishaw and B. Gorny
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J. Neurosci.,
June 1, 1999;
19(11):
4662 - 4673.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. S. Kudrimoti, C. A. Barnes, and B. L. McNaughton
Reactivation of Hippocampal Cell Assemblies: Effects of Behavioral State, Experience, and EEG Dynamics
J. Neurosci.,
May 15, 1999;
19(10):
4090 - 4101.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Matsumura, H. Nishijo, R. Tamura, S. Eifuku, S. Endo, and T. Ono
Spatial- and Task-Dependent Neuronal Responses during Real and Virtual Translocation in the Monkey Hippocampal Formation
J. Neurosci.,
March 15, 1999;
19(6):
2381 - 2393.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. W. Stackman and J. S. Taube
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J. Neurosci.,
November 1, 1998;
18(21):
9020 - 9037.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. E. Skaggs and B. L. McNaughton
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18(20):
8455 - 8466.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. J. Knierim, H. S. Kudrimoti, and B. L. McNaughton
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J Neurophysiol,
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80(1):
425 - 446.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. Q. Whishaw and H. Maaswinkel
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3050 - 3058.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Zhang, I. Ginzburg, B. L. McNaughton, and T. J. Sejnowski
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79(2):
1017 - 1044.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Zinyuk, S. Kubik, Yu. Kaminsky, A. A. Fenton, and J. Bures
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March 28, 2000;
97(7):
3771 - 3776.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
