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The Journal of Neuroscience, July 15, 2002, 22(14):6254-6264
Dynamic Interactions between Local Surface Cues, Distal
Landmarks, and Intrinsic Circuitry in Hippocampal Place Cells
James J.
Knierim
Department of Neurobiology and Anatomy, W. M. Keck Center for
the Neurobiology of Learning and Memory, University of
Texas-Houston Medical School, Houston, Texas 77030
A number of computational models of hippocampal place cells
incorporate attractor neural network architecture to simulate key
findings in the place cell literature, including the properties of
pattern completion, firing in the absence of visual input, and
nonlinear responses to environmental manipulations. To test for
evidence of attractor dynamics, ensembles of place cells were recorded
using multiple-tetrode techniques. After many days of experience in an
environment with salient local surface cues on a circular track and
salient distal landmarks on the wall, the local surface cues were
rotated as a set in opposition to the distal landmarks. The amount of
mismatch between the local and distal sets of cues varied from 45 to
180°. If place cells were parts of strong attractors, then their
place fields should follow either the local cues or the distal cues as
an integrated ensemble. Instead, in single recording sessions, some
place cells were controlled by the distal landmarks, other cells were
controlled by the local cues, and other cells became silent or gained
new fields. In some cases, individual place fields split in half,
following both the local and distal cues. If place cells are indeed
parts of attractor networks in the hippocampus, then the attractors may
be weak relative to the inputs from external sources, such as
representations of the sensory environment and representations of
heading direction, in a familiar, well explored environment.
Key words:
place cells; attractor neural networks; single-unit; ensemble recording; navigation; spatial orientation
Copyright © 2002 Society for Neuroscience 0270-6474/02/22146254-11$05.00/0
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