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Journal of Neuroscience, Vol 10, 3093-3105, Copyright © 1990 by Society for Neuroscience
Firing properties of hippocampal neurons in a visually symmetrical environment: contributions of multiple sensory cues and mnemonic processes
PE Sharp, JL Kubie and RU Muller
Department of Physiology, SUNY Health Sciences Center, Brooklyn 11203.
The location-specific firing of hippocampal place cells can easily be
brought under the control of experimenter-defined cues. Nevertheless, there
is evidence that these firing fields are not determined just by immediate
sensory input, but also by earlier states of the nervous system (O'Keefe
and Speakman, 1987). Here, we report further on the roles of multiple
visual cues and mnemonic processes in determining the firing of place
cells. Rats were trained to chase food pellets in a cylinder with
homogeneous gray walls and 1 white cue card. After a cell's field was
recorded in this "standard" condition, probe sessions were conducted in
which a second card was placed 180 degrees away from the first. This
configuration created a diametrically symmetrical environment in which
pairs of locations 180 degrees apart were identical with respect to views
of the wall and cards. If place cells are strongly controlled by these
immediately available views, firing in the 2-card configuration should be
diametrically symmetrical. Alternatively, because the rat moves freely in
the cylinder, information is available that pairs of visually identical
places are not truly the same. If some mnemonic process stores and updates
information about the rat's paths during the session, it is possible that
the firing pattern will be different in 2 such places, especially because
the original training was conducted in the 1-card, asymmetrical
environment. Thirteen of 18 cells had a single, asymmetric firing pattern
after the second card was introduced; the field was the same size and shape
as in the 1-card configuration and in the same spatial relation to 1 of the
2 cards. The field position during 2-card sessions could be rotated 180
degrees by starting the rat by one card or the other. In further probe
sessions in which the cue cards, entry location, and background cues were,
in various combinations, rotated in relation to each other, these cells
always showed a single field, similar in size and shape to that in the
standard, and in the same relationship as in the standard to as many cues
as possible. The remaining 5 cells showed complex changes over repeated
2-card sessions, and 3 of these showed paired fields, 180 degrees apart for
at least some of the sessions. In one case, the second field disappeared
with repeated exposures to 2 cards; in another, the second field persisted
when only 1 card was used. We conclude that place cells are influenced both
by the immediate sensory configuration and by internal neural states
related to earlier experience in the environment.
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