Appetitive and aversive olfactory learning in humans studied using event-related functional magnetic resonance imaging.
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.
Gottfried
Jay A
JA
Wellcome Department of Imaging Neuroscience, Institute of Neurology, London, WC1N 3BG, United Kingdom. j.gottfried@fil.ion.ucl.ac.uk
O'Doherty
John
J
Dolan
Raymond J
RJ
D000328:Adult; D000679:Amygdala / Q000033:anatomy & histology / Q000502:physiology; D001069:Appetite Regulation; D001245:Association Learning; D001519:Behavior; D003214:Conditioning, Classical; D004644:Emotions; D005071:Evoked Potentials; D005260:Female; D006801:Humans; D007700:Kinetics; D008279:Magnetic Resonance Imaging / Q000379:methods*; D008297:Male; D009714:Nucleus Accumbens / Q000033:anatomy & histology / Q000502:physiology; D009812:Odorants; D009833:Olfactory Pathways / Q000033:anatomy & histology* / Q000502:physiology*; D012903:Smell