Journal Article

FZJ-2018-05155

http://join2-wiki.gsi.de/foswiki/pub/Main/Artwork/join2_logo100x88.png Network architecture underlying basal autonomic outflow: Evidence from frontotemporal dementia

Sturm, V. E. (Corresponding author) ; Brown, J. A. ; Hua, A. Y. ; Lwi, S. J. ; Zhou, J. ; Kurth, F. ; Eickhoff, S.FZJ* ; Rosen, H. J. ; Kramer, J. H. ; Miller, B. L. ; Levenson, R. W. ; Seeley, W. W.

2018
Soc. Washington, DC

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Please use a persistent id in citations: http://hdl.handle.net/2128/19935  doi:10.1523/JNEUROSCI.0347-18.2018

Abstract: The salience network is a distributed neural system that maintains homeostasis by regulating autonomic nervous system activity and social-emotional function. Here we examined how within-network connectivity relates to individual differences in human (including males and females) baseline parasympathetic and sympathetic nervous activity. We measured resting autonomic nervous system physiology in 24 healthy controls and 23 patients with behavioral variant frontotemporal dementia (bvFTD), a neurodegenerative disease characterized by baseline autonomic deficits. Participants also underwent structural and task-free functional magnetic resonance imaging. First, we used voxel-based morphometry to determine whether salience network atrophy was associated with lower baseline respiratory sinus arrhythmia (RSA; a parasympathetic measure) and skin conductance level (SCL; a sympathetic measure) in bvFTD. Next, we examined whether functional connectivity deficits in 21 autonomic-relevant, salience network node-pairs related to baseline autonomic dysfunction. Lower baseline RSA was associated with smaller volume in left ventral anterior insula (vAI), weaker connectivity between bilateral vAI and bilateral anterior cingulate cortex (ACC), and stronger connectivity between bilateral ACC and bilateral hypothalamus/amygdala. Lower baseline SCL, in contrast, was associated with smaller volume in inferior temporal gyrus, dorsal mid-insula, and hypothalamus; weaker connectivity between bilateral ACC and right hypothalamus/amygdala; and stronger connectivity between bilateral dorsal anterior insula and periaqueductal gray. Our results suggest that baseline parasympathetic and sympathetic tone depend on the integrity of lateralized salience network hubs (left vAI for parasympathetic and right hypothalamus/amygdala for sympathetic) and highly calibrated ipsilateral and contralateral network connections. In bvFTD, deficits in this system may underlie resting parasympathetic and sympathetic disruption.SIGNIFICANCE STATEMENTThe salience network maintains homeostasis and regulates autonomic nervous system activity. Whether within-network connectivity patterns underlie individual differences in resting parasympathetic and sympathetic nervous system activity, however, is not well understood. We measured baseline autonomic nervous system activity in healthy controls and patients with behavioral variant frontotemporal dementia, a neurodegenerative disease characterized by resting autonomic deficits, and probed how salience network dysfunction relates to diminished parasympathetic and sympathetic outflow. Our results indicate that baseline parasympathetic and sympathetic tone are the product of complex, opposing intra-network nodal interactions and depend on the integrity of highly tuned, lateralized salience network hubs (i.e., left ventral anterior insula for parasympathetic activity and right hypothalamus/amygdala for sympathetic activity).

Note: This project was supported by grants from the NIH National Institute on Aging (P50AG023501, P01AG019724, R01AG052496, R01AG032306, R01AG057204, 1K23AG040127, and 1K23AG045289), The Larry L. Hillblom Foundation (2013-A-029-SUP and 2005/2T), the John Douglas French Foundation; the Consortium for Frontotemporal Dementia Research, and the Tau Consortium. We are grateful for the patients, healthy controls, and families that have participated in our research studies.

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Contributing Institute(s):

1. Gehirn & Verhalten (INM-7)

Research Program(s):

1. 574 - Theory, modelling and simulation (POF3-574) (POF3-574)

Appears in the scientific report 2018

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