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 Previous Article
Volume 17, Number 5,
Issue of March 1, 1997
pp. 1880-1890
Copyright ©1997 Society for Neuroscience
Selective Roles for Hippocampal, Prefrontal Cortical, and Ventral
Striatal Circuits in Radial-Arm Maze Tasks With or Without a Delay
Received Oct. 10, 1996; revised Dec. 17, 1996; accepted Dec. 18, 1996.
Stan B. Floresco,
Jeremy K. Seamans, and
Anthony G. Phillips
Department of Psychology, University of British Columbia,
Vancouver, British Columbia, Canada V6T 1Z4
The hippocampus, the prefrontal cortex, and the ventral striatum
form interconnected neural circuits that may underlie aspects of
spatial cognition and memory. In the present series of experiments, we
investigated functional interactions between these areas in rats during
the performance of delayed and nondelayed spatially cued radial-arm
maze tasks. The two-phase delayed task consisted of a training phase
that provided rats with information about where food would be located
on the maze 30 min later during a test phase. The single-phase
nondelayed task was identical to the test phase of the delayed task,
but in the absence of a training phase rats lacked previous knowledge
of the location of food on the maze. Transient inactivation of the
ventral CA1/subiculum (vSub) by a bilateral injection of lidocaine
disrupted performance on both tasks. Lidocaine injections into the vSub
on one side of the brain and the prefrontal cortex on the other
transiently disconnected these two brain regions and significantly
impaired foraging during the delayed task but not the nondelayed task. Transient disconnections between the vSub and the nucleus accumbens produced the opposite effect, disrupting foraging during the nondelayed task but not during the delayed task. These data suggest that serial
transmission of information between the vSub and the prefrontal cortex
is required when trial-unique, short-term memory is used to guide
prospective search behavior. In contrast, exploratory goal-directed
locomotion in a novel situation not requiring previously acquired
information about the location of food is dependent on serial
transmission between the hippocampus and the nucleus accumbens. These
results indicate that different aspects of spatially mediated behavior
are subserved by separate, distributed limbic-cortical-striatal networks.
Key words:
ventral CA1/subiculum;
prelimbic cortex;
nucleus
accumbens;
spatial memory;
neural networks;
lidocaine-induced
reversible lesions;
rats
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[Full Text]
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[PDF]
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18(18):
7588 - 7598.
[Abstract]
[Full Text]
[PDF]
|
|
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J. Neurosci.,
February 15, 1998;
18(4):
1613 - 1621.
[Abstract]
[Full Text]
[PDF]
|
|
|
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|
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[Abstract]
[Full Text]
[PDF]
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RC106 - RC106.
[Abstract]
[Full Text]
[PDF]
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