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The Journal of Neurophysiology Vol. 86 No. 4 October 2001, pp. 1839-1857
Copyright ©2001 by the American Physiological Society
Department of Cell and Molecular Biology and Institute for Neuroscience, Northwestern University Medical School, Chicago, Illinois 60611
McEchron, Matthew D.,
Aldis P. Weible, and
John F. Disterhoft.
Aging and Learning-Specific Changes in Single-Neuron Activity in
CA1 Hippocampus During Rabbit Trace Eyeblink Conditioning. J. Neurophysiol. 86: 1839-1857, 2001. Rabbit trace eyeblink conditioning is a
hippocampus-dependent task in which the auditory conditioned stimulus
(CS) is separated from the corneal airpuff unconditioned stimulus (US)
by a 500-ms empty trace interval. Young rabbits are able to associate
the CS and US and acquire trace eyeblink conditioned responses (CRs); however, a subset of aged rabbits show poor learning on this task. Several studies have shown that CA1-hippocampal activity is altered by
aging; however, it is unknown how aging affects the interaction of CA1
single neurons within local ensembles during learning. The present
study examined the extracellular activity of CA1 pyramidal neurons
within local ensembles in aged (29-34 mo) and young (3-6 mo) rabbits
during 10 daily sessions (80 trials/session) of trace eyeblink
conditioning. A single surgically implanted nonmovable stereotrode was
used to record ensembles ranging in size from 2 to 12 separated single
neurons. A total of six young and four aged rabbits acquired
significant levels of CRs, whereas five aged rabbits showed very few
CRs similar to a group of five young pseudoconditioned rabbits.
Pyramidal cells (2,159 total) were recorded from these four groups
during training. Increases in CA1 pyramidal cell firing to the CS and
US were diminished in the aged nonlearners. Local ensembles from all
groups contained heterogeneous types of pyramidal cell responses. Some
cells showed increases while others showed decreases in firing during
the trace eyeblink trial. Hierarchical clustering was used to isolate
seven different classes of single-neuron responses that showed unique firing patterns during the trace conditioning trial. The proportion of
cells in each group was similar for six of seven response classes. Unlike the excitatory modeling patterns reported in previous studies, three of seven response types (67% of recorded cells) exhibited some
type of inhibitory decrease to the CS, US, or both. The single-neuron response classes showed different patterns of learning-related activity
across training. Several of the single-neuron types from the aged
nonlearners showed unique alterations in response magnitude to the CS
and US. Cross-correlation analyses suggest that specific single-neuron
types provide more correlated single-neuron activity to the ensemble
processing of information. However, aged nonlearners showed a
significantly lower level of coincident pyramidal cell firing for all
cell types within local ensembles in CA1.
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