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The Journal of Neuroscience, December 15, 1999, 19(24):10869-10876
Amygdala-Hippocampal Involvement in Human Aversive Trace
Conditioning Revealed through Event-Related Functional Magnetic
Resonance Imaging
Christian
Büchel1,
Raymond J.
Dolan1, 2,
Jorge
L.
Armony1, 3, and
Karl J.
Friston1
1 The Wellcome Department of Cognitive Neurology,
Institute of Neurology, London, UK WC1N 3BG, 2 The Royal
Free School of Medicine, London, UK NW3 2QG, and
3 Institute of Cognitive Neuroscience, University College
London, UK WC1E 6BT
Previous functional neuroimaging studies have characterized brain
systems mediating associative learning using classical delay conditioning paradigms. In the present study, we used event-related functional magnetic resonance imaging to characterize neuronal responses mediating aversive trace conditioning. During conditioning, neutral auditory tones were paired with an aversive sound
[unconditioned stimulus (US)]. We compared neuronal responses evoked
by conditioned (CS+) and nonconditioned (CS ) stimuli in which a 50%
pairing of CS+ and the US enabled us to limit our analysis to responses evoked by the CS+ alone. Differential responses (CS+ vs CS), related
to conditioning, were observed in anterior cingulate and anterior
insula, regions previously implicated in delay fear conditioning. Differential responses were also observed in the amygdala and hippocampus that were best characterized with a time × stimulus interaction, indicating rapid adaptation of
CS+-specific responses in medial temporal lobe. These results are
strikingly similar to those obtained with a previous delay conditioning
experiment and are in accord with a preferential role for medial
temporal lobe structures during the early phase of conditioning.
However, an additional activation of anterior hippocampus in the
present experiment supports a view that its role in trace conditioning is to maintain a memory trace between the offset of the CS+ and the
delayed onset of the US to enable associative learning in trace conditioning.
Key words:
associative learning; fear; medial temporal lobe; memory; functional neuroimaging; emotional learning
Copyright © 1999 Society for Neuroscience 0270-6474/99/192410869-08$05.00/0
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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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[Full Text]
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|
|
|
|
|
|
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|
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