How distinct functional insular subdivisions mediate interacting neurocognitive systems

Author:

Zhao Haichao1234ORCID,Turel Ofir5678,Bechara Antoine56,He Qinghua129101112ORCID

Affiliation:

1. Faculty of Psychology and MOE Key Laboratory of Cognition and Personality , , Chongqing, China

2. Southwest University , , Chongqing, China

3. School of Biological Science and Medical Engineering , , Beijing, China

4. Beihang University , , Beijing, China

5. Department of Psychology , and Brain and Creativity Institute, , Los Angeles, CA, United States

6. University of Southern California , and Brain and Creativity Institute, , Los Angeles, CA, United States

7. Computing Information Systems , , Parkville, Victoria, Australia

8. The University of Melbourne , , Parkville, Victoria, Australia

9. Chongqing Collaborative Innovation Center for Brain Science , Chongqing, China

10. Southwest University Branch , , Chongqing, China

11. Collaborative Innovation Center of Assessment Toward Basic Education Quality at Beijing Normal University , , Chongqing, China

12. State Key Laboratory of Cognitive Neuroscience and Learning , Beijing Normal University, Beijing, China

Abstract

Abstract Recent neurocognitive models propose that the insula serves as a hub of interoceptive awareness system, modulating 2 interplaying neurocognitive systems: The posterior insula (PI) receives and integrates various interoceptive signals; these signals are then transmitted to the anterior insula for processing higher-order representations into awareness, where the dorsal anterior insula (dAI) modulates the prefrontal self-control system and the ventral anterior insula (vAI) modulates the amygdala (AMG)-striatal reward-seeking circuit. We sought to test this view using a multimodal approach. We first used a resting-state functional magnetic resonance imaging (fMRI) approach with a sample of 120 undergraduate students. Then, we unpacked the neuro-cognitive association between insular connectivity and cognitive performance during an Iowa gambling fMRI task. Lastly, an independent Open Southwest University Longitudinal Imaging Multimodal dataset was used to validate the results. Findings suggested that the dAI was predominantly connected to the prefrontal regions; the vAI was primarily connected to the AMG–ventral–striatum system; and the PI was mainly connected to the visceral-sensorimotor system. Moreover, cognitive scores were positively correlated with FC between dAI and the self-control process of ventrolateral prefrontal cortex and were negatively correlated with FC between vAI and the reward-seeking process of orbitofrontal cortex and subgenual anterior cingulate cortex. The findings highlight the roles of our theorized subinsular functionality in the overall operation of the neural cognitive systems.

Funder

National Natural Science Foundation of China

Natural Science Foundation of Chongqing

Fundamental Research Funds for the Central Universities

High-end Foreign Expert Introduction Program

Open Research Fund of the State Key Laboratory of Cognitive Neuroscience and Learning

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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