Aversive learning enhances perceptual and cortical odor discrimination of indistinguishable odor cues

In this experiment we combined fMRI with multivariate analytical techniques and sensory psychophysics to assess the impact of aversive olfactory conditioning on perceptual and neural discrimination of predictive odor cues (Li et al., Science 2008). Importantly, the use of perceptually identical odor enantiomers (mirror-image molecules differing only in their chiral properties) enabled us to determine whether humans can acquire the ability to distinguish between odorous stimuli that initially smell the same. Subjects were presented with four enantiomers (two different pairs), one of which (the conditioned stimulus, or CS+) was repetitively paired with an electric shock (the unconditioned stimulus, or US) during a conditioning phase. Its chiral counterpart (chCS+) was never accompanied by shock, and the second pair of odor enantiomers served as non-conditioned control stimuli.

The behavioral effects of aversive conditioning on perceptual discrimination were assessed using a triangular (triple-forced-choice) odor discrimination test. Before conditioning, discrimination accuracy between the CS+ and chCS+ was at chance (33%), but after odor-shock conditioning, discrimination accuracy rose more than twofold, significantly exceeding chance and pre-conditioning performance (in the absence of any improvement in distinguishing between the control enantiomer pair). We next used multivariate (pattern-based) fMRI approaches to clarify the neural mechanisms underlying learning-induced perceptual enhancement of the predictive odor cue. Before conditioning, the spatial activity patterns in posterior piriform cortex strongly correlated for CS+ and chCS+, corresponding closely to the high perceived similarity as estimated by the triangular tests. However, following conditioning, these spatial correlations markedly declined for the CS+ and chCS+ stimuli, in line with the learning-induced behavioral enhancement in odor discrimination.

These results are the first to demonstrate concurrent enhancement of sensory discrimination between initially indistinguishable odor cues, at both perceptual and cortical levels, as a consequence of associative learning. Moreover, given that learning-induced changes in piriform ensemble activity accompanied behavioral gains in olfactory acuity, the findings offer compelling support for spatial coding hypotheses of odor object perception in piriform cortex (akin to the neural arrangement of visual objects in visual association areas of the brain). Finally, the capacity to update perceptual representations of a CS+ should provide a potent neural substrate to guide the behavioral discrimination of predictive cues.

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