The Phoenix from the Ashes: Cardiovascular Autonomic Dysfunction in Behavioral Variant of Frontotemporal Dementia

Struhal, Walter; Javor, Andrija; Brunner, Cornelia; Benesch, Thomas; Schmidt, Verena; Voško, Milan R.; Ransmayr, Gerhard

doi:10.3233/jad-140531

Cited by 19 publications

(29 citation statements)

References 17 publications

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“…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. svPPA has also been associated with deficits in afferent interoceptive signal processing 20, 26, 31, 32.…”

Section: Introductionsupporting

confidence: 70%

Cardiac responses to viewing facial emotion differentiate frontotemporal dementias

Marshall

Hardy

Allen

et al. 2018

Ann Clin Transl Neurol

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ObjectiveTo establish proof‐of‐principle for the use of heart rate responses as objective measures of degraded emotional reactivity across the frontotemporal dementia spectrum, and to demonstrate specific relationships between cardiac autonomic responses and anatomical patterns of neurodegeneration.MethodsThirty‐two patients representing all major frontotemporal dementia syndromes and 19 healthy older controls performed an emotion recognition task, viewing dynamic, naturalistic videos of facial emotions while ECG was recorded. Cardiac reactivity was indexed as the increase in interbeat interval at the onset of facial emotions. Gray matter associations of emotional reactivity were assessed using voxel‐based morphometry of patients’ brain MR images.ResultsRelative to healthy controls, all patient groups had impaired emotion identification, whereas cardiac reactivity was attenuated in those groups with predominant fronto‐insular atrophy (behavioral variant frontotemporal dementia and nonfluent primary progressive aphasia), but preserved in syndromes focused on the anterior temporal lobes (right temporal variant frontotemporal dementia and semantic variant primary progressive aphasia). Impaired cardiac reactivity correlated with gray matter atrophy in a fronto‐cingulo‐insular network that overlapped correlates of cognitive emotion processing.InterpretationAutonomic indices of emotional reactivity dissociate from emotion categorization ability, stratifying frontotemporal dementia syndromes and showing promise as novel biomarkers. Attenuated cardiac responses to the emotions of others suggest a core pathophysiological mechanism for emotional blunting and degraded interpersonal reactivity in these diseases.

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Section: Introductionsupporting

confidence: 70%

Cardiac responses to viewing facial emotion differentiate frontotemporal dementias

Marshall

Hardy

Allen

et al. 2018

Ann Clin Transl Neurol

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Section: Relationship Of Present Findings To Previous Work On Autonomicmentioning

confidence: 99%

“…Although bvFTD-related damage to cortical autonomic centers such as the ACC and FI has been welldocumented, few studies have directly assessed autonomic functions in these patients (12,13). A recent study performed clinical autonomic function tests and reported a high prevalence of parasympathetic and sympathetic dysfunction in bvFTD without exploring the anatomical correlates of these deficits (13). In the context of emotion processing, several studies examined physiological reactivity to emotional stimuli and found that patients with bvFTD retained physiological responses to many stimuli (27,71,72) but that response amplitudes were diminished to emotional stimuli, such as those designed to elicit self-conscious emotions (71).…”

Section: Relationship Of Present Findings To Previous Work On Autonomicmentioning

confidence: 99%

“…The autonomic nervous system exerts direct control over bodily states via its two major branches: the sympathetic system, associated with energy mobilization, and the parasympathetic system, whose peripheral efferent signals are conveyed chiefly via the vagus nerve and are associated with energy conservation at the whole organism level (8). Perturbations in one or both of these systems are associated with homeostatic instability and diverse pathological feeling states (1,(9)(10)(11)(12)(13)(14). Therefore, elucidating the neural mechanisms of autonomic integration represents an important biomedical research priority.…”

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confidence: 99%

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

Guo

Sturm

Zhou

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

110

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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.

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“…Autonomic dysregulation, which is associated with altered responses to hunger and satiety, 29 has been found to be increased in bvFTD. 30,31 In addition, the hypothalamus has functional projections to the striatum, thalamus, brainstem, orbitofrontal cortex, middle and posterior cingulum, and temporal brain regions. 32 Recent animal studies have also shown that the lateral hypothalamus connects to the reward centers in the ventral tegmental area, which may mediate sucrose preference.…”

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confidence: 99%

Eating behavior in frontotemporal dementia

et al. 2015

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Objective: To contrast the relationships of hormonal eating peptides and hypothalamic volumes to eating behavior and metabolic changes (body mass index [BMI]) in behavioral variant frontotemporal dementia (bvFTD) and semantic variant primary progressive aphasia (svPPA).Methods: Seventy-five patients with dementia (19 bvFTD, 26 svPPA, and 30 Alzheimer disease dementia) and 23 controls underwent fasting blood analyses of leptin, ghrelin, cholecystokinin, peptide tyrosine tyrosine (PYY), and agouti-related peptide (AgRP) levels. On brain MRI anterior, posterior, and total hypothalamic volumes were measured. Relationships between endocrine measures, hypothalamic volumes, eating behaviors, and BMI were investigated.Results: Levels of AgRP were higher in patients with bvFTD (69 6 89 pg/mL) and svPPA (62 6 81 pg/mL) compared with controls (23 6 19 pg/mL, p , 0.01). No differences were found for leptin, oxytocin, cholecystokinin, ghrelin, and PYY levels. Patients with bvFTD and svPPA had higher scores on questionnaires measuring eating behaviors. Atrophy of the posterior and total hypothalamus was observed in the bvFTD group only. Linear regression modeling revealed that leptin and AgRP levels predicted BMI. Conclusion:Eating abnormalities are multifactorial in FTD. In bvFTD, they are in part related to hypothalamic degeneration, with potential disintegration of the network connections between the hypothalamus and orbitofrontal cortex/reward pathways. In svPPA, although hypothalamic volumes are preserved, this group experiences elevated AgRP levels similar to bvFTD, which predicts BMI in both groups. This finding highlights the potential key role of AgRP in eating and metabolic changes and provides a potential target for treatment to modify disease progression. Alterations in eating behavior are one of the diagnostic criteria for behavioral variant frontotemporal dementia (bvFTD).

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The Phoenix from the Ashes: Cardiovascular Autonomic Dysfunction in Behavioral Variant of Frontotemporal Dementia

Abstract: This is the first prospective study to elucidate autonomic dysfunction in bvFTD patients. There is a considerable higher frequency of cardiovascular dysfunction and OH in bvFTD. History taking may be not conclusive thus cannot exclude cardiovascular dysautonomia.

Cited by 19 publications

References 17 publications

Cardiac responses to viewing facial emotion differentiate frontotemporal dementias

Cardiac responses to viewing facial emotion differentiate frontotemporal dementias

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

Eating behavior in frontotemporal dementia

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