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

J Neurosci. 2002 Dec 15;22(24):10829-37. doi: 10.1523/JNEUROSCI.22-24-10829.2002.

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 (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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Amygdala / anatomy & histology
  • Amygdala / physiology
  • Appetite Regulation*
  • Association Learning*
  • Behavior
  • Conditioning, Classical
  • Emotions
  • Evoked Potentials
  • Female
  • Humans
  • Kinetics
  • Magnetic Resonance Imaging / methods*
  • Male
  • Nucleus Accumbens / anatomy & histology
  • Nucleus Accumbens / physiology
  • Odorants
  • Olfactory Pathways / anatomy & histology*
  • Olfactory Pathways / physiology*
  • Smell*