Interconnected sub-networks of the macaque monkey gustatory connectome

Renée Hartig; Ali Karimi; Henry C Evrard

doi:10.3389/fnins.2022.818800

Interconnected sub-networks of the macaque monkey gustatory connectome

Front Neurosci. 2023 Feb 16:16:818800. doi: 10.3389/fnins.2022.818800. eCollection 2022.

Authors

Renée Hartig^{1

2

3

4}, Ali Karimi⁵, Henry C Evrard^{1

2

4

6}

Affiliations

¹ Max Planck Institute for Biological Cybernetics, Tübingen, Germany.
² Functional and Comparative Neuroanatomy Laboratory, Werner Reichardt Centre for Integrative Neuroscience, Eberhard Karl University of Tübingen, Tübingen, Germany.
³ Department of Psychiatry and Psychotherapy, University Medical Center, Johannes Gutenberg University Mainz, Mainz, Germany.
⁴ Center for Biomedical Imaging and Neuromodulation, Nathan Kline Institute for Psychiatric Research, Orangeburg, NY, United States.
⁵ Department of Connectomics, Max Planck Institute for Brain Research, Frankfurt, Germany.
⁶ International Center for Primate Brain Research, Center for Excellence in Brain Science and Intelligence Technology, Institute of Neuroscience, Chinese Academy of Sciences, Shanghai, China.

Abstract

Macroscopic taste processing connectivity was investigated using functional magnetic resonance imaging during the presentation of sour, salty, and sweet tastants in anesthetized macaque monkeys. This examination of taste processing affords the opportunity to study the interactions between sensory regions, central integrators, and effector areas. Here, 58 brain regions associated with gustatory processing in primates were aggregated, collectively forming the gustatory connectome. Regional regression coefficients (or β-series) obtained during taste stimulation were correlated to infer functional connectivity. This connectivity was then evaluated by assessing its laterality, modularity and centrality. Our results indicate significant correlations between same region pairs across hemispheres in a bilaterally interconnected scheme for taste processing throughout the gustatory connectome. Using unbiased community detection, three bilateral sub-networks were detected within the graph of the connectome. This analysis revealed clustering of 16 medial cortical structures, 24 lateral structures, and 18 subcortical structures. Across the three sub-networks, a similar pattern was observed in the differential processing of taste qualities. In all cases, the amplitude of the response was greatest for sweet, but the network connectivity was strongest for sour and salty tastants. The importance of each region in taste processing was computed using node centrality measures within the connectome graph, showing centrality to be correlated across hemispheres and, to a smaller extent, region volume. Connectome hubs exhibited varying degrees of centrality with a prominent leftward increase in insular cortex centrality. Taken together, these criteria illustrate quantifiable characteristics of the macaque monkey gustatory connectome and its organization as a tri-modular network, which may reflect the general medial-lateral-subcortical organization of salience and interoception processing networks.

Keywords: functional connectivity; insular cortex; interoception; neuroimaging; non-human primate; taste.

Grants and funding

This work was supported by the Werner Reichardt Centre for Integrative Neuroscience (CIN) at the Eberhard Karls University of Tübingen [CIN is an Excellence Cluster funded by the Deutsche Forschungsgemeinschaft (DFG) within the framework of the Excellence Initiative EXC 307] and by the Max Planck Society. RH was supported by the Focus Program for Translational Neuroscience at the Johannes Gutenberg University Mainz, Germany.