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Link to original content: http://pubmed.ncbi.nlm.nih.gov/34955769/
Human Primary Olfactory Amygdala Subregions Form Distinct Functional Networks, Suggesting Distinct Olfactory Functions - PubMed Skip to main page content
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. 2021 Dec 9:15:752320.
doi: 10.3389/fnsys.2021.752320. eCollection 2021.

Human Primary Olfactory Amygdala Subregions Form Distinct Functional Networks, Suggesting Distinct Olfactory Functions

Torben Noto  1 , Guangyu Zhou  1 , Qiaohan Yang  1 , Gregory Lane  1 , Christina Zelano  1
Affiliations

Human Primary Olfactory Amygdala Subregions Form Distinct Functional Networks, Suggesting Distinct Olfactory Functions

Torben Noto et al. Front Syst Neurosci. .

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.

Keywords: amygdala; cortical amygdala; fMRI; medial amygdala; olfaction; periamygdaloid complex; resting connectivity.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Human brain atlas with subregions of the amygdala labeled. Subregions that receive olfactory bulb input are labeled in red; others are labeled in black. Olfactory subregions include the medial amygdala (MeA), cortical amygdala (CoA), and the periamygdaloid complex (PAC). Other amygdala subregions listed for reference: the lateral amygdala (LA), ventromedial part of the basolateral amygdala (BLVM), basomedial amygdala (BM), central amygdala (Ce), and the dorsolateral part of the lateral amygdala (LaDL) (adapted from Mai et al., 2015).
Figure 2
Figure 2
Olfactory and non-olfactory areas of the amygdala are delineated using resting state connectivity. (A) Results of k-means (k = 2) clustering of the amygdala based on resting state connectivity. Each color (red and blue) in panel (A) indicates one cluster. The data are shown on the FSL’s MNI152_T1_1 mm_brain. (B) Bar plots indicate the distribution of permuted difference of the percentage of the olfactory subregions within each parcellation. The red vertical line indicates real value. Data are shown for the right and left hemispheres separately. R, right hemisphere.
Figure 3
Figure 3
Parcellation of the olfactory amygdala subregions based on resting state connectivity. K-means (k = 3) clustering analysis was performed for the right hemisphere (A), left hemisphere (B), and combined left and right (C) hemispheres. Each color (red, blue, and green) in (A–C) indicates one cluster. Results are shown on the FSL’s MNI152_T1_1 mm_brain. Parcellation accuracy of each subregion is shown on the right. Top right: proportion of voxels from each parcellation subdivision located within each anatomical subregion. Bottom right: z score of the proportion maps. *Indicates P < 0.05 (Bonferroni corrected). L, left hemisphere; R, right hemisphere; MeA, medial amygdala; CoA, cortical amygdala; PAC, periamygdaloid complex.
Figure 4
Figure 4
Whole-brain resting connectivity of the MeA. Regions of interest include the insula, motor cortex, anterior cingulate cortex, and raphe nuclei. The connectivity map was thresholded at threshold-free cluster enhancement corrected P < 0.05. Results are overlaid on FSL’s MNI152_T1_1 mm_brain.
Figure 5
Figure 5
Whole-brain resting connectivity of the CoA. Regions of interest include the hypothalamus, substantia nigra, periaqueductal gray area, and medial dorsal thalamus. The connectivity map was thresholded at threshold-free cluster enhancement corrected P < 0.05. Results are overlaid on FSL’s MNI152_T1_1 mm_brain.
Figure 6
Figure 6
Whole-brain resting connectivity of the PAC. Regions of interest include the fusiform gyrus, anterior olfactory nucleus, pontine nucleus, and orbitofrontal cortex. The connectivity map was thresholded at threshold-free cluster enhancement corrected P < 0.05. Results are overlaid on FSL’s MNI152_T1_1 mm_brain.
Figure 7
Figure 7
Whole-brain resting connectivity is common to MeA, CoA, and PAC. Regions of interest include the piriform cortex, entorhinal cortex, olfactory tubercle, temporal pole, basal forebrain, and other areas of the amygdala. The connectivity maps were thresholded at threshold-free cluster enhancement corrected P < 0.05. Results are overlaid on FSL’s MNI152_T1_1 mm_brain.
Figure 8
Figure 8
Whole-brain resting connectivity common to two of the three olfactory amygdala subregions. (A) Intersections of resting state networks of olfactory amygdala subregion pairs. Results are overlaid on FSL’s MNI152_T1_1 mm_brain. (B) Bar plot of the number of voxels that shows significant connectivity with each (Figures 4–6) and combination (panel A and Figure 7) of the olfactory subregions. (C) Venn Diagram of panel (B). The connectivity maps were thresholded at threshold-free cluster enhancement corrected P < 0.05.
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