Orbitofrontal cortex neurons: Role in olfactory and visual association learning

1. The orbitofrontal cortex is implicated in the rapid learning of new associations between visual stimuli and primary reinforcers such as taste. It is also the site of convergence of information from olfactory, gustatory, and visual modalities. To investigate the neuronal mechanisms underlying the formation of odor-taste associations, we made recordings from olfactory neurons in the orbitofrontal cortex during the performance of an olfactory discrimination task and its reversal in macaques. 2. It was found that 68% of odor-responsive neurons modified their responses after the changes in the taste reward associations of the odorants. Full reversal of the neuronal responses was seen in 25% of these neurons. Extinction of the differential neuronal responses after task reversal was seen in 43% of these neurons. 3. For comparison, visually responsive orbitofrontal neurons were tested during reversal of a visual discrimination task. Seventy-one percent of these visual cells showed rapid full reversal of the visual stimulus to which they responded, when the association of the visual stimulus with taste was reversed in the reversal task. 4. These findings demonstrate that the responses of many orbitofrontal cortex olfactory neurons are modified by and depend on the taste with which the odor is associated. 5. This modification is likely to be important for setting the motivational value of olfactory stimuli for feeding and other rewarded behavior. However, it is less complete, and much slower, than the modifications found for orbitofrontal visual neurons during visual-taste reversal. This relative inflexibility of olfactory responses is consistent with the need for some stability in odor-taste associations to facilitate the formation and perception of flavors.