Neuroanatomy of Shared Conversational Laughter in Neurodegenerative Disease

Peter S. Pressman, Suzanne Shdo, Michaela Simpson, Kuan-Hua Chen, Clinton Mielke, Bruce L. Miller, Katherine P. Rankin, Robert W. Levenson

Perceiving another person's emotional expression often sparks a corresponding signal in the observer. Shared conversational laughter is a familiar example. Prior studies of shared laughter have made use of task-based functional neuroimaging. While these methods offer insight in a controlled setting, the ecological validity of such controlled tasks has limitations. Here, we investigate the neural correlates of shared laughter in patients with one of a variety of neurodegenerative disease syndromes (N = 75), including Alzheimer's disease (AD), behavioral variant frontotemporal dementia (bvFTD), right and left temporal variants of semantic dementia (rtvFTD, svPPA), nonfluent/agrammatic primary progressive aphasia (nfvPPA), corticobasal syndrome (CBS), and progressive supranuclear palsy (PSP). Patients were recorded in a brief unrehearsed conversation with a partner (e.g., a friend or family member). Laughter was manually labeled, and an automated system was used to assess the timing of that laughter relative to the partner's laughter. The probability of each participant with neurodegenerative disease laughing during or shortly after his or her partners' laughter was compared to differences in brain morphology using voxel-based morphometry, thresholded based on cluster size and a permutation method and including age, sex, magnet strength, disease-specific atrophy and total intracranial volumes as covariates. While no significant correlations were found at the critical T value, at a corrected voxelwise threshold of p < 0.005, a cluster in the left posterior cingulate gyrus demonstrated a trend at p = 0.08 (T = 4.54). Exploratory analysis with a voxelwise threshold of p = 0.001 also suggests involvement of the left precuneus (T = 3.91) and right fusiform gyrus (T = 3.86). The precuneus has been previously implicated in the detection of socially complex laughter, and the fusiform gyrus has a well-described role in the recognition and processing of others' emotional cues. This study is limited by a relatively small sample size given the number of covariates. While further investigation is needed, these results support our understanding of the neural underpinnings of shared conversational laughter.