An object's smell in the multisensory brain : how our senses interact during olfactory object processing

Abstract: Object perception is a remarkable and fundamental cognitive ability that allows us to interpret and interact with the world we are living in. In our everyday life, we constantly perceive objects–mostly without being aware of it and through several senses at the same time. Although it might seem that object perception is accomplished without any effort, the underlying neural mechanisms are anything but simple. How we perceive objects in the world surrounding us is the result of a complex interplay of our senses. The aim of the present thesis was to explore, by means of functional magnetic resonance imaging, how our senses interact when we perceive an object’s smell in a multisensory setting where the amount of sensory stimulation increases, as well as in a unisensory setting where we perceive an object’s smell in isolation. In Study I, we sought to determine whether and how multisensory object information influences the processing of olfactory object information in the posterior piriform cortex (PPC), a region linked to olfactory object encoding. In Study II, we then expanded our search for integration effects during multisensory object perception to the whole brain because previous research has demonstrated that multisensory integration is accomplished by a network of early sensory cortices and higher-order multisensory integration sites. We specifically aimed at determining whether there exist cortical regions that process multisensory object information independent of from which senses and from how many senses the information arises. In Study III, we then sought to unveil how our senses interact during olfactory object perception in a unisensory setting. Other previous studies have shown that even in such unisensory settings, olfactory object processing is not exclusively accomplished by regions within the olfactory system but instead engages a more widespread network of brain regions, such as regions belonging to the visual system. We aimed at determining what this visual engagement represents. That is, whether areas of the brain that are principally concerned with processing visual object information also hold neural representations of olfactory object information, and if so, whether these representations are similar for smells and pictures of the same objects. In Study I we demonstrated that assisting inputs from our senses of vision and hearing increase the processing of olfactory object information in the PPC, and that the more assisting input we receive the more the processing is enhanced. As this enhancement occurred only for matching inputs, it likely reflects integration of multisensory object information. Study II provided evidence for convergence of multisensory object information in form of a non-linear response enhancement in the inferior parietal cortex: activation increased for bimodal compared to unimodal stimulation, and increased even further for trimodal compared to bimodal stimulation. As this multisensory response enhancement occurred independent of the congruency of the incoming signals, it likely reflects a process of relating the incoming sensory information streams to each other. Finally, Study III revealed that regions of the ventral visual object stream are engaged in recognition of an object’s smell and represent olfactory object information in form of distinct neural activation patterns. While the visual system encodes information about both visual and olfactory objects, it appears to keep information from the two sensory modalities separate by representing smells and pictures of objects differently. Taken together, the studies included in this thesis reveal that olfactory object perception is a multisensory process that engages a widespread network of early sensory as well higher-order cortical regions, even if we do not encounter ourselves in a multisensory setting but exclusively perceive an object’s smell.