Enhanced positive emotional reactivity in frontotemporal dementia reflects left-lateralized atrophy in the temporal and frontal lobes

Suzanne M Shdo; Ashlin R K Roy; Samir Datta; Isabel J Sible; Sladjana Lukic; David C Perry; Katherine P Rankin; Joel H Kramer; Howard J Rosen; Bruce L Miller; William W Seeley; Sarah R Holley; Maria L Gorno-Tempini; Virginia E Sturm

doi:10.1016/j.cortex.2022.02.018

Enhanced positive emotional reactivity in frontotemporal dementia reflects left-lateralized atrophy in the temporal and frontal lobes

Cortex. 2022 Sep:154:405-420. doi: 10.1016/j.cortex.2022.02.018. Epub 2022 Jun 28.

Authors

Affiliations

¹ Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA; University of California, Berkeley, Department of Psychology, Berkeley, CA, USA. Electronic address: shdo@berkeley.edu.
² Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA. Electronic address: ashlin.roy@ucsf.edu.
³ Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA. Electronic address: samir.datta@ucsf.edu.
⁴ Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA. Electronic address: jsible@usc.edu.
⁵ Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA. Electronic address: sladjana.lukic@ucsf.edu.
⁶ Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA. Electronic address: david.perry@ucsf.edu.
⁷ Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA. Electronic address: katherine.rankin@ucsf.edu.
⁸ Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA. Electronic address: joel.kramer@ucsf.edu.
⁹ Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA. Electronic address: howie.rosen@ucsf.edu.
¹⁰ Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA; Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, San Francisco, CA, USA. Electronic address: bruce.miller@ucsf.edu.
¹¹ Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA. Electronic address: bill.seeley@ucsf.edu.
¹² Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, San Francisco, CA, USA; San Francisco State University, Department of Psychology, San Francisco, CA, USA. Electronic address: sholley@sfsu.edu.
¹³ Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA; Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, San Francisco, CA, USA. Electronic address: marialuisa.gornotempini@ucsf.edu.
¹⁴ Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA; Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, San Francisco, CA, USA. Electronic address: virginia.sturm@ucsf.edu.

Abstract

In frontotemporal dementia (FTD), left-lateralized atrophy patterns have been associated with elevations in certain positive emotions. Here, we investigated whether positive emotional reactivity was enhanced in semantic variant primary progressive aphasia (svPPA), an FTD syndrome that targets the left anterior temporal lobe. Sixty-one participants (16 people with svPPA, 24 people with behavioral variant FTD, and 21 healthy controls) viewed six 90-sec trials that were comprised of a series of photographs; each trial was designed to elicit a specific positive emotion, negative emotion, or no emotion. Participants rated their positive emotional experience after each trial, and their smiling behavior was coded with the Facial Action Coding System. Results indicated that positive emotional experience and smiling were elevated in svPPA in response to numerous affective and non-affective stimuli. Voxel-based morphometry analyses revealed that greater positive emotional experience and greater smiling in the patients were both associated with smaller gray matter volume in the left superior temporal gyrus (p_FWE < .05), among other left-lateralized frontotemporal regions. Whereas enhanced positive emotional experience related to atrophy in middle superior temporal gyrus and structures that promote cognitive control and emotion regulation, heightened smiling related to atrophy in posterior superior temporal gyrus and structures that support motor control. Our results suggest positive emotional reactivity is elevated in svPPA and offer new evidence that atrophy in left-lateralized emotion-relevant systems relates to enhanced positive emotions in FTD.

Keywords: Elation; Euphoria; Mood; Neurodegeneration; Semantic dementia.

Publication types

Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural

MeSH terms

Atrophy
Emotions
Frontal Lobe
Frontotemporal Dementia*
Humans
Magnetic Resonance Imaging
Pick Disease of the Brain*

Abstract

Publication types

MeSH terms

Grants and funding