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J Neurosci. 2018 Oct 17;38(42):8943-8955. doi: 10.1523/JNEUROSCI.0347-18.2018. Epub 2018 Sep 4.

Network Architecture Underlying Basal Autonomic Outflow: Evidence from Frontotemporal Dementia.

Author information

1
Department of Neurology, University of California-San Francisco, Sandler Neurosciences Center, San Francisco, California 94158.
2
Department of Psychology, University of California, Berkeley, California 94720-1650.
3
Center for Cognitive Neuroscience, Neuroscience and Behavioral Disorders Program, Duke-National University of Singapore Medical School, Singapore 169857.
4
Cousins Center for Psychoneuroimmunology, Semel Institute for Neuroscience and Human Behavior, Department of Psychiatry and Biobehavioral Sciences, University of California-Los Angeles School of Medicine, Los Angeles, California 90095.
5
Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine Universität, 40225 Düsseldorf, Germany.
6
Institute of Neuroscience and Medicine, Brain and Behaviour, Research Centre Jülich, Jülich, 52425, Germany, and.
7
Department of Neurology, University of California-San Francisco, Sandler Neurosciences Center, San Francisco, California 94158, bill.seeley@ucsf.edu.
8
Department of Pathology, University of California, San Francisco, California 94143.

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 fMRI. First, we used voxel-based morphometry to determine whether salience network atrophy was associated with lower baseline respiratory sinus arrhythmia (a parasympathetic measure) and skin conductance level (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 respiratory sinus arrhythmia 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 skin conductance level, 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 depends 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 STATEMENT The 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 intranetwork 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).

KEYWORDS:

autonomic nervous system; frontotemporal dementia; parasympathetic; salience network; sympathetic

PMID:
30181137
PMCID:
PMC6191520
[Available on 2019-04-17]
DOI:
10.1523/JNEUROSCI.0347-18.2018

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