INVESTIGATION OF AN INNATE OLFACTORY-VISUAL FUNCTIONAL CONNECTION IN THE HUMAN BRAIN USING FMRI

Open Access
Author:
Martinez, Brittany Elizabeth
Graduate Program:
Neuroscience
Degree:
Doctor of Philosophy
Document Type:
Dissertation
Date of Defense:
March 31, 2017
Committee Members:
  • Qing X. Yang, Dissertation Advisor
  • Qing X. Yang, Committee Chair
  • Mark David Meadowcroft, Committee Member
  • Prasanna Rasika Karunanayaka, Committee Member
  • Paul Eslinger, Outside Member
  • Patricia Sue Grigson-Kennedy, Committee Member
Keywords:
  • olfaction
  • fMRI
  • vision
Abstract:
We are constantly bombarded with stimuli from multiple sensory sources in the environment of our natural world. The innate behavioral responses to the environment, therefore, are based on our brains’ ability to integrate distinct and complex sensory information into a comprehensive and understandable percept (1). Therefore, multisensory integration is a phenomenon that involves combining multimodal sensory information from a target stimulus into a coherent signal. Despite substantial knowledge of the fundamental processes involved in multisensory integration, there is still much to be learned because majority of studies have focused on one sensory modality at a time (2). One particular aspect that is largely overlooked is the interplay between the visual and olfactory systems (3). Despite olfaction being a vestigial sense, landmark studies have consistently demonstrated, strong behavioral and physiological responses to olfactory stimuli even at levels below conscious perception, (4-7). Behavioral, anatomical, and neurofunctional evidence exists supporting the likelihood of an innate olfactory-visual functional connection in the human brain (8-43). Furthermore, pioneering research on the topic of olfactory-visual interactions has utilized fMRI to delineate the neural networks underlying the interplay between these two sensory systems (44-55). However, many of these studies employed fMRI paradigms to better understand the influence of visual information over olfactory processing. This dissertation aimed to utilize olfactory-visual association fMRI paradigms to better elucidate the reciprocal relationship between the olfactory and visual systems in the human brain. The overall goal was to develop a more comprehensive model of the neural networks underlying the human olfactory function. Olfaction is the most studied chemosensory system, however, the functioning of this network is still not well understood because of its complicated neuroanatomical organization (56). This dissertation, therefore, sought to elucidate several unknown aspects of the functional connection between the olfactory and visual systems by testing several hypotheses about this innate connection. First, Chapter 2 of this dissertation focused on investigating the role of congruence during the formation of olfactory-visual associations. It was hypothesized that olfactory-visual associations could be rapidly formed by a neutral, non-lexical abstract visual symbols, as evidenced by significant olfactory system activation during testing conditions consisting of presenting a visual cue that was previously paired with an odor compared to an unpaired visual cue. It was also hypothesized that a lexical, semantically congruent visual cue, would produce greater olfactory-visual activation during both the acquisition and testing phases compared to a lexical, semantically incongruent visual cue or a neutral, non-lexical symbol. The results reinforced that rapid olfactory-visual associations could be formed by neutral, non-lexical visual cues, via modulation of visual activation by visual information. This indicated that olfactory-visual associations could be formed innately, in a reflexively manner to facilitate the odor naming process. Furthermore, lexical, semantically congruent, multisensory visual cues were found to elicit patterns of greater visual and language-related activation, mostly likely subserving an olfactory-visual-lexical integrative process that may be responsible for odor identification and naming in the human brain (57-59). Chapter 3 of this dissertation tested the hypothesis that an odor-attention task, involving higher-order cognitive decision-making and attentional processes to an olfactory stimulus, will elicit significantly stronger olfactory-visual associative neural activation compared to less complex visual-attention task that requires only detection of a visual stimulus. The findings here indicated that rapid olfactory-visual associations may be formed via modulation of the visual system by olfactory information, regardless of the task context. This suggests a unique, intrinsic mechanism between the olfactory and visual systems that provides odors an avenue to influence visual processing of stimuli, regardless of which sensory cue is selectively attended to. Chapter 4 of this dissertation consisted of an investigation of the effect of age on neural activity in response to an olfactory-visual association paradigm in an older, cognitively normal participant cohort. Based on previous findings, it was hypothesized that a significant age-related decline would be observed in neural activity in response to this paradigm and that male subjects would display significantly greater deficits on olfactory-visual associative activation compared to female subjects. The results highlighted a significant effect of normal aging on the olfactory-visual functional connection and differential patterns of decline were observed in men and women, with women appearing to be more resilient to this effect. In summary, this dissertation made significant strides in elucidating several unknown aspects of this under-researched piece of brain function. Overall, the results support the existence of an innate olfactory-visual functional connection, in that rapid olfactory-visual associations can be formed using non-lexical, neutral symbols, but that a lexical, semantically congruent visual cue “Smell” appears to elicit stronger associations between olfactory and visual stimuli, leading to increased activation in visual brain regions. Furthermore, higher order cognitive tasks also appear to influence this effect by increasing activation in visual and olfactory regions, thus likely enhancing the strength of the olfactory-visual association. Finally, it was also observed that there is a significant, negative effect of age of the innate functional connection between the olfactory and visual systems and that women may be more resilient to this effect due to improved connectivity between olfactory structures. Taken together, these findings not only provide evidence of an innate olfactory-visual functional connection, but also offer valuable insight into modulating factors of this connection.