Abstract

Three subregions of the amygdala receive monosynaptic projections from the olfactory bulb, making them part of the primary olfactory cortex. These primary olfactory areas are located at the anterior-medial aspect of the amygdala and include the medial amygdala (MeA), cortical amygdala (CoA), and the periamygdaloid complex (PAC). The vast majority of research on the amygdala has focused on the larger basolateral and basomedial subregions, which are known to be involved in implicit learning, threat responses, and emotion. Fewer studies have focused on the MeA, CoA, and PAC, with most conducted in rodents. Therefore, our understanding of the functions of these amygdala subregions is limited, particularly in humans. Here, we first conducted a review of existing literature on the MeA, CoA, and PAC. We then used resting-state fMRI and unbiased k-means clustering techniques to show that the anatomical boundaries of human MeA, CoA, and PAC accurately parcellate based on their whole-brain resting connectivity patterns alone, suggesting that their functional networks are distinct, relative both to each other and to the amygdala subregions that do not receive input from the olfactory bulb. Finally, considering that distinct functional networks are suggestive of distinct functions, we examined the whole-brain resting network of each subregion and speculated on potential roles that each region may play in olfactory processing. Based on these analyses, we speculate that the MeA could potentially be involved in the generation of rapid motor responses to olfactory stimuli (including fight/flight), particularly in approach/avoid contexts. The CoA could potentially be involved in olfactory-related reward processing, including learning and memory of approach/avoid responses. The PAC could potentially be involved in the multisensory integration of olfactory information with other sensory systems. These speculations can be used to form the basis of future studies aimed at clarifying the olfactory functions of these under-studied primary olfactory areas.

Highlights

  • After being sampled from the air by olfactory sensory neurons in the nose and synapsing through olfactory bulb glomeruli, olfactory stimuli undergo parallel processing in the brain, through at least six cortical regions, all of which receive direct, monosynaptic projections from the olfactory bulb (Carmichael et al, 1994; Lane et al, 2020)

  • We used resting-state functional Magnetic Resonance Imaging (fMRI) and unbiased k-means clustering techniques to show that the anatomical boundaries of human medial amygdala (MeA), cortical amygdala (CoA), and periamygdaloid complex (PAC) can be accurately parcellated based on their whole-brain resting connectivity patterns alone, suggesting that their functional networks are distinct, relative both to each other and to the amygdala subregions that do not receive input from the olfactory bulb

  • Functional neuroimaging studies in humans have found increased amygdala activity in the presence of odor compared to no odor (Royet et al, 2000) and local field potentials recorded from the human amygdala show increased oscillatory activity following odor onset (Hughes and Andy, 1979; Hudry et al, 2001, 2003; Jung et al, 2006)

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Summary

Introduction

After being sampled from the air by olfactory sensory neurons in the nose and synapsing through olfactory bulb glomeruli, olfactory stimuli undergo parallel processing in the brain, through at least six cortical regions, all of which receive direct, monosynaptic projections from the olfactory bulb (Carmichael et al, 1994; Lane et al, 2020) These regions, which include parts of the amygdala, comprise the primary olfactory cortex (Price, 1990, 2009; Wilson and Sullivan, 2003; Illig and Wilson, 2009 Gottfried, 2010; Mainland et al, 2014; Vaughan and Jackson, 2014; Ennis et al, 2015; Porada et al, 2019). Considering that distinct functional networks are suggestive of distinct functions, we examined the whole-brain resting network of each subregion and speculated on potential specific roles that each region may play in olfactory processing

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