Dominant hemisphere lateralization of cortical parasympathetic control as revealed by frontotemporal dementia

The brain continuously influences and perceives the physiological condition of the body. Related cortical representations have been proposed to shape emotional experience and guide behavior. Although previous studies have identified brain regions recruited during autonomic processing, neurological l...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 113; no. 17; pp. E2430 - E2439
Main Authors Guo, Christine C., 郭聪, Sturm, Virginia E., Zhou, Juan, Gennatas, Efstathios D., Trujillo, Andrew J., Hua, Alice Y., Crawford, Richard, Stables, Lara, Kramer, Joel H., Rankin, Katherine, Levenson, Robert W., Rosen, Howard J., Miller, Bruce L., Seeley, William W.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 26.04.2016
National Acad Sciences
SeriesPNAS Plus
Subjects
Adult
Aged
Asymmetry
Biological Sciences
Brain
Case-Control Studies
Dementia
Emotions
Female
Frontotemporal Dementia - physiopathology
Functional Laterality - physiology
Functional Neuroimaging
Gyrus Cinguli - physiology
Heart - physiopathology
Heart Rate - physiology
Humans
Magnetic Resonance Imaging
Male
Middle Aged
Nerve Net - physiology
Parasympathetic Nervous System - physiology
PNAS Plus
lateralization
frontotemporal dementia
emotion
salience network
autonomic neuroscience
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Summary:The brain continuously influences and perceives the physiological condition of the body. Related cortical representations have been proposed to shape emotional experience and guide behavior. Although previous studies have identified brain regions recruited during autonomic processing, neurological lesion studies have yet to delineate the regions critical for maintaining autonomic outflow. Even greater controversy surrounds hemispheric lateralization along the parasympathetic–sympathetic axis. The behavioral variant of frontotemporal dementia (bvFTD), featuring progressive and often asymmetric degeneration that includes the frontoinsular and cingulate cortices, provides a unique lesion model for elucidating brain structures that control autonomic tone. Here, we show that bvFTD is associated with reduced baseline cardiac vagal tone and that this reduction correlates with left-lateralized functional and structural frontoinsular and cingulate cortex deficits and with reduced agreeableness. Our results suggest that networked brain regions in the dominant hemisphere are critical formaintaining an adaptive level of baseline parasympathetic outflow.
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Author contributions: V.E.S., J.Z., J.H.K., K.R., R.W.L., H.J.R., B.L.M., and W.W.S. designed research; C.C.G., J.Z., E.D.G., A.J.T., A.Y.H., R.C., and L.S. performed research; C.C.G. contributed new reagents/analytic tools; C.C.G., V.E.S., and A.J.T. analyzed data; and C.C.G., V.E.S., R.W.L., and W.W.S. wrote the paper.
Edited by Marcus E. Raichle, Washington University in St. Louis, St. Louis, MO, and approved March 10, 2016 (received for review May 12, 2015)
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1509184113