Human olfactory cortex contributes to emotional and perceptual aspects of aversive associative learning and memory

Abstract

The role of the sensory cortex, beyond the amygdala, has been increasingly recognized in animal associative learning and memory. Here, we examined olfactory cortical plasticity in human olfactory associative learning and memory, while elucidating related changes in emotional and perceptual responses. Psychophysical and neurometric analyses were conducted across an odor-morphing continuum, with the two extreme levels differentially conditioned with aversive and neutral stimuli. Conditioned odors acquired distinct emotional values, tracked by ensemble response patterns in the orbitofrontal (high-level) olfactory cortex. Also observed were enhanced perceptual discrimination and divergent ensemble neuronal response patterns in the anterior and posterior piriform (low-to-intermediate-level) olfactory cortices. Whereas emotional-learning-related changes, both behavioral and neural, maintained 8 days later, perceptual-learning-related changes, also both behavioral and neural, recovered by then, highlighting the human aptitude of forming persistent emotional memory and related sensory cortical plasticity in contrast to transient perceptual alterations of sensory stimuli associated with mild aversive experiences.