Rapidly acquired multisensory association in the olfactory cortex.

Prasanna R Karunanayaka,Donald A Wilson,Jianli Wang,Qing X Yang,Megha Vasavada,Michael J Tobia,Paul Eslinger,Lan Kong,Brittany Martinez

doi:10.1002/brb3.390

Prasanna R Karunanayaka, Donald A Wilson + Show 7 more

Open Access

https://doi.org/10.1002/brb3.390

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Abstract

The formation of an odor percept in humans is strongly associated with visual information. However, much less is known about the roles of learning and memory in shaping the multisensory nature of odor representations in the brain. The dynamics of odor and visual association in olfaction was investigated using three functional magnetic resonance imaging (fMRI) paradigms. In two paradigms, a visual cue was paired with an odor. In the third, the same visual cue was never paired with an odor. In this experimental design, if the visual cue was not influenced by odor-visual pairing, then the blood-oxygen-level-dependent (BOLD) signal elicited by subsequent visual cues should be similar across all three paradigms. Additionally, intensity, a major dimension of odor perception, was used as a modulator of associative learning which was characterized in terms of the spatiotemporal behavior of the BOLD signal in olfactory structures. A single odor-visual pairing cue could subsequently induce primary olfactory cortex activity when only the visual cue was presented. This activity was intensity dependent and was also detected in secondary olfactory structures and hippocampus. This study provides evidence for a rapid learning response in the olfactory system by a visual cue following odor and visual cue pairing. The novel data and paradigms suggest new avenues to explore the dynamics of odor learning and multisensory representations that contribute to the construction of a unified odor percept in the human brain.

Highlights

Odor perception is highly influenced by knowledge, experience, internal states, and sensory information from other modalities (Wilson and Stevenson 2006)
A striking observation is that the visual-only stimuli elicit nearly identical activation patterns as the odor + visual stimuli in the primary olfactory cortex, insula, hippocampus, and orbitofrontal cortex
When this condition was compared to the odor + visual condition, no significant activation differences were detected in olfactory brain structures except in the dorsal lateral prefrontal cortex (DLPFC)

Summary

Introduction

Odor perception is highly influenced by knowledge, experience, internal states, and sensory information from other modalities (Wilson and Stevenson 2006). FMRI studies of odor–visual association (or integration) have shown that a visual cue previously associated with an odor can, in the absence of odor stimulation, elicit neural activity in the primary olfactory cortex (Gottfried et al 2003, 2004). In this paradigm, stimulus-evoked activity within the hippocampus and orbitofrontal cortex was shown to be experience dependent (Gottfried et al 2003). We demonstrated that a learned odor–visual pairing cue is related to the immediate visual-evoked activity within the primary olfactory cortex, secondary olfactory structures, and hippocampus This effect was intensity dependent and generated no visual-evoked odor perception. The results provide novel data and methods suggesting new avenues to explore odor–visual integration and show how multiple brain regions contribute to the construction of a unified odor percept (Wilson and Stevenson 2006)

Participants

Results

Discussion

Limitations of the study