Impaired Interoceptive Accuracy in Semantic Variant Primary Progressive Aphasia

Abstract

Background: Interoception (the perception of internal bodily sensations) is strongly linked to emotional experience and sensitivity to the emotions of others in healthy subjects. Interoceptive impairment may contribute to the profound socioemotional symptoms that characterize frontotemporal dementia (FTD) syndromes, but remains poorly defined.

Methods: Patients representing all major FTD syndromes and healthy age-matched controls performed a heartbeat counting task as a measure of interoceptive accuracy. In addition, patients had volumetric MRI for voxel-based morphometric analysis, and their caregivers completed a questionnaire assessing patients' daily-life sensitivity to the emotions of others.

Results: Interoceptive accuracy was impaired in patients with semantic variant primary progressive aphasia relative to healthy age-matched individuals, but not in behavioral variant frontotemporal dementia and nonfluent variant primary progressive aphasia. Impaired interoceptive accuracy correlated with reduced daily-life emotional sensitivity across the patient cohort, and with atrophy of right insula, cingulate, and amygdala on voxel-based morphometry in the impaired semantic variant group, delineating a network previously shown to support interoceptive processing in the healthy brain.

Conclusion: Interoception is a promising novel paradigm for defining mechanisms of reduced emotional reactivity, empathy, and self-awareness in neurodegenerative syndromes and may yield objective measures for these complex symptoms.

Keywords: autonomic; cardiac; empathy; frontotemporal dementia; interoception; primary progressive aphasia.

Figure 1

Interoceptive accuracy in participant groups: behavioral and voxel-based morphometry data. The plots (above) show individual raw data for accuracy on the heartbeat counting task expressed as an interoceptive accuracy index (see text) in each participant group. Error bars represent SEM. The statistical parametric map of regional gray matter volume associated with interoceptive accuracy in the impaired svPPA group (below) has been overlaid on representative sections of the normalized study-specific T1-weighted group mean brain MR image; the MNI coordinate (millimeters) of the plane of each section is indicated. The color barcodes T values; the SPM is thresholded here at p < 0.001 uncorrected over the whole brain for display purpose. Regional local maxima were significant at p < 0.05_FWE corrected for multiple comparisons over the whole brain (right amygdala, MNI coordinates [18 −15 −21]) or within pre-specified anatomical regions of interest (anterior cingulate cortex [4 0 34]; posterior cingulate cortex [2 −30 28]; right insula [44 −4 −3]). bvFTD, patients with behavioral variant frontotemporal dementia; Control, healthy control group; L, left; nfvPPA, patients with nonfluent variant primary progressive aphasia; svPPA, patients with semantic variant primary progressive aphasia.