Auditory subcortical pathways to the amygdala using diffusion weighted imaging tractography

Poster No:

609 

Submission Type:

Abstract Submission 

Authors:

Emmanouela Kosteletou Kassotaki1, Martina Trisia Cinca-Tomás1, Federico Varriano2, Guadalupe Soria3, Alberto Prats-Galino2, Judith Domínguez-Borràs1

Institutions:

1Brainlab Cognitive Neuroscience Research Group, Barcelona, Spain, 2Laboratory of Surgical Neuroanatomy, Faculty of Medicine, University of Barcelona, Barcelona, Spain, 3Institute of Neurosciences, University of Barcelona, Barcelona, Spain

First Author:

Emmanouela Kosteletou Kassotaki  
Brainlab Cognitive Neuroscience Research Group
Barcelona, Spain

Co-Author(s):

Martina Trisia Cinca-Tomás  
Brainlab Cognitive Neuroscience Research Group
Barcelona, Spain
Federico Varriano  
Laboratory of Surgical Neuroanatomy, Faculty of Medicine, University of Barcelona
Barcelona, Spain
Guadalupe Soria  
Institute of Neurosciences, University of Barcelona
Barcelona, Spain
Alberto Prats-Galino  
Laboratory of Surgical Neuroanatomy, Faculty of Medicine, University of Barcelona
Barcelona, Spain
Judith Domínguez-Borràs  
Brainlab Cognitive Neuroscience Research Group
Barcelona, Spain

Introduction:

Quick and efficient detection of threat is critical for survival. To serve this ability, a visual subcortical pathway, is believed to function in humans as a shortcut to the amygdala (McFadyen et al., 2019; Wei et al., 2015). Similarly, evidence from non-human animals suggests the existence of a homologous auditory subcortical pathway, though its presence in humans remains underexplored (LeDoux et al., 1990a; Aggleton et al., 1980; Shinonaga et al., 1994, Marsh et al., 2002).

Methods:

To address this, we applied advanced diffusion-weighted imaging (DWI) tractography and Fixel-Based Analysis (FBA) using data from 200 participants of the Human Connectome Project (Dhollander et al., 2021; Raffelt et al., 2017). Specifically, we reconstructed candidate pathways connecting the inferior colliculus (IC) to the basolateral amygdala (BLA) either via the medial geniculate body (MGB) or directly, as well as direct pathways from the auditory and audiovisual pulvinar (auditory PUL) to BLA. To evaluate the functional significance of these pathways, we analyzed their associations with auditory and fear-related behavioral measures from the HCP dataset. For comparison, we examined the thalamocortical auditory pathway between the ventral MGB (vMGB) and the primary auditory cortex (PAC), which bypasses the amygdala, hypothesizing no association with aversive behavioral responses (Andersen et al., 1980).

Results:

Our findings revealed white matter tracts connecting the inferior colliculus (IC) to the basolateral amygdala (BLA) via the medial geniculate body (MGB) of the thalamus, as well as direct projections from the auditory and audiovisual regions of the pulvinar (auditory PUL) to the BLA. Fiber density in the IC–MGB–BLA pathway was associated with both heightened participants´ fear and anxiety levels (F (1, 380) = 13.222, p = 0.0006; Bonferroni corrected) and better hearing ability in noise (F (1, 381) = 5.425, p = 0.02; Bonferroni corrected), while the auditory PUL–BLA pathway showed associations exclusively with fear and anxiety levels (F (1, 381) = 5.12, p = 0.015, Bonferroni corrected). Additionally, the thalamocortical pathway linking the ventral MGB to the primary auditory cortex (PAC) was correlated with auditory perceptual ability (F (1, 382) = 10.6, p = 0.001), but not with affective function. Finally, our results failed to support the existence of a direct connection between IC and BLA in humans.

Conclusions:

In conclusion, our study has established the foundation for verifying the existence and functional role of an auditory subcortical pathway in the human brain. Our neuroimaging approach, applied to a large sample, provides sufficient evidence supporting the existence of an auditory subcortical pathway to the amygdala facilitating and integrating sensory and emotional information.

Emotion, Motivation and Social Neuroscience:

Emotional Perception 1
Emotion and Motivation Other 2

Modeling and Analysis Methods:

Diffusion MRI Modeling and Analysis

Keywords:

Emotions
Sub-Cortical
Thalamus
Tractography
Other - Amygdala, Audition, Pathway, Fear

1|2Indicates the priority used for review

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Please indicate which methods were used in your research:

Diffusion MRI

For human MRI, what field strength scanner do you use?

3.0T

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Provide references using APA citation style.

Andersen, R. A., Knight, P. L., & Merzenich, M. M. (1980). The thalamocortical and corticothalamic conections of AI, AII, and the anteriior auditory field (AFF) in the cat: Evidence ofr two largely sergregarted systems of connections. Journal of Comparative Neurology, 194(3), 663–701.
Aggleton, J. P., Burton, M. J., & Passingham, R. E. (1980). Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Research, 190(2), 347–368.
Dhollander, T., Clemente, A., Singh, M., Boonstra, F., Civier, O., Duque, J. D., Egorova, N., Enticott, P., Fuelscher, I., Gajamange, S., Genc, S., Gottlieb, E., Hyde, C., Imms, P., Kelly, C., Kirkovski, M., Kolbe, S., Liang, X., Malhotra, A., … Caeyenberghs, K. (2021). Fixel-based Analysis of Diffusion MRI: Methods, Applications, Challenges and Opportunities. In NeuroImage (Vol. 241). Academic Press Inc.
LeDoux, J. E., Farb, C., & Ruggiero, D. A. (1990a). Topographic organization of neurons in the acoustic thalamus that project to the amygdala. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 10(4), 1043–1054.
McFadyen, J., Mattingley, J. B., & Garrido, M. I. (2019). An afferent white matter pathway from the pulvinar to the amygdala facilitates fear recognition. ELife, 8.
Marsh, R. A., Fuzessery, Z. M., Grose, C. D., & Wenstrup, J. J. (2002). Projection to the Inferior Colliculus from the Basal Nucleus of the Amygdala.
Raffelt, D., & Connelly, A. (2016). Unsupervised 3-tissue response function estimation from single-shell or multi-shell diffusion MR data without a co-registered T1 image SEE PROFILE. https://www.researchgate.net/publication/307863133
Shinonaga, Y., Takada, M., & Mizuno, N. (1994). Direct projections from the non-laminated divisions of the medial geniculate nucleus to the temporal polar cortex and amygdala in the cat. The Journal of Comparative Neurology, 340(3), 405–426.
Wei, P., Liu, N., Zhang, Z., Liu, X., Tang, Y., He, X., Wu, B., Zhou, Z., Liu, Y., Li, J., Zhang, Y., Zhou, X., Xu, L., Chen, L., Bi, G., Hu, X., Xu, F., & Wang, L. (2015). Processing of visually evoked innate fear by a non-canonical thalamic pathway. Nature Communications 2015 6:1, 6(1), 1–13.

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