Appetitive and aversive olfactory learning in humans studied using event-related functional magnetic resonance imaging

Jay A. Gottfried*, John O'Doherty, Raymond J. Dolan

*Corresponding author for this work

Research output: Contribution to journalArticle

334 Scopus citations

Abstract

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 capp) 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.

Original languageEnglish (US)
Pages (from-to)10829-10837
Number of pages9
JournalJournal of Neuroscience
Volume22
Issue number24
DOIs
StatePublished - Dec 15 2002

Keywords

  • Amygdala
  • Associative learning
  • Conditioning
  • Emotion
  • Neuroimaging
  • Nucleus accumbens
  • Odor
  • Olfaction
  • Orbitofrontal cortex
  • Piriform cortex
  • fMRI

ASJC Scopus subject areas

  • Neuroscience(all)

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