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The Journal of Neuroscience, December 15, 2002, 22(24):10829-10837
Appetitive and Aversive Olfactory Learning in Humans Studied
Using Event-Related Functional Magnetic Resonance Imaging
Jay A.
Gottfried,
John
O'Doherty, and
Raymond J.
Dolan
Wellcome Department of Imaging Neuroscience, Institute of
Neurology, London, WC1N 3BG, United Kingdom
We combined event-related functional magnetic resonance imaging
(fMRI) with olfactory classical conditioning to differentiate the
neural responses evoked during appetitive and aversive olfactory learning. Three neutral faces [the conditioned stimuli (CS+)] were
repetitively paired with pleasant, neutral, or unpleasant odors [the
unconditioned stimuli (UCS)] in a partial reinforcement schedule. A
fourth face was never paired to odor [the nonconditioned stimulus
(CS )]. Learning-related neural activity, comparing unpaired (face
only) CS+ stimuli with CS, showed valence-independent activations in
rostral and caudal orbitofrontal cortex (OFC). Medial OFC responded to
the appetitive (app) CS+, whereas lateral OFC responded to the aversive
(av) CS+. Within nucleus accumbens, neural responses showed divergent
activation profiles that increased with time in response to the appCS+
but decreased in response to the avCS+. In posterior amygdala,
responses were elicited by the appCS+, which habituated over time. In
temporal piriform cortex, neural responses were evoked by the avCS+,
which progressively increased with time. These results highlight
regional and temporal dissociations during olfactory learning and imply
that emotionally salient odors can engender cross-modal associative
learning. Moreover, the findings suggest that the role of human primary
(piriform) and secondary olfactory cortices transcends their function
as mere intermediaries of chemosensory information processing.
Key words:
olfaction; odor; emotion; conditioning; associative
learning; neuroimaging; fMRI; orbitofrontal cortex; nucleus accumbens; amygdala; piriform cortex
Copyright © 2002 Society for Neuroscience 0270-6474/02/222410829-09$05.00/0
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