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

Abstract

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 for maintaining an adaptive level of baseline parasympathetic outflow.

Cardiac responses to viewing facial emotion differentiate frontotemporal dementias

“…The subjective experience of emotion is likely to be integral to the internalization of observed emotional states in others during emotional contagion. Our findings therefore provide a candidate neurobiological mechanism for the blunted emotional reactions and loss of empathy that characterize FTD syndromes38, 39 and amplify previous work linking altered cardiac vagal tone to reduced agreeableness in bvFTD 24. Impaired awareness of heartbeat has also previously been demonstrated in FTD25, 32: taken together with the present findings, this suggests that induction, awareness, and cognitive decoding of embodied emotional responses all contribute to emotional responsiveness and may be separably targeted in FTD syndromes.…”

“…We hypothesized that cardiac modulation would be attenuated in bvFTD and nfvPPA due to degeneration of fronto‐insular networks in these diseases, but relatively preserved (and separable from emotion identification) in syndromes targeting the anterior temporal lobes (svPPA and rtvFTD) 18, 20, 21. We further hypothesized that emotion recognition ability but not cardiac reactivity would be associated with semantic knowledge, while cardiac reactivity would correlate with atrophy in components of the central autonomic regulatory network (ACC, insula, OFC) 15, 16, 24…”

“…In particular, bvFTD has been associated with abnormal autonomic reactivity to affectively charged stimuli,18, 19, 20, 21, 22 alterations of resting skin conductance and heart rate variability,23, 24 and abnormal brain‐heart coupling,24, 25 while nfvPPA has been associated with reduced pupil responses to arousing stimuli 20, 26. Taken together, these findings are consistent with the known targeting of core cerebral autonomic fronto‐cingulo‐insular circuitry in bvFTD and nfvPPA 27, 28, 29, 30.…”

Global and regional brain atrophy is associated with low or retrograde facial vein flow in multiple sclerosis

“…28 The paucity of differences in any of the conventional inflammatory outcome measures may be explained by the recent findings, which suggest that the cortical atrophy, and specifically cortical hemispheric volume loss lateralization, could influence the homeostasis of autonomic nervous system (ANS). 29 For example, autonomic mechanisms related to cardiovascular control are located in the neuronal circuitry of the insular cortex, dorsal anterior cingulate, prefrontal cortex, and hippocampus. 30 It has been reported that dysregulation of the ANS is associated with variability of the heart rate, and fluctuations of the blood pressure, all of which can contribute to reaching a critical closing pressure that leads to the collapse of the cerebral venous system.…”

784. Structural Dysconnectivity of Key Cognitive and Emotional Hubs in Young People at High Genetic Risk for Bipolar Disorder

“…[75][76][77] Indeed, disturbances in this left-right balance may yield the pattern of autonomic disturbances often seen in frontotemporal dementia. 78 In this light, bilateral disturbances speak to a 'balanced' interoceptive and autonomic dysregulation in those at HR of BD.…”