Enhanced visceromotor emotional reactivity in dyslexia and its relation to salience network connectivity

Virginia E Sturm; Ashlin R K Roy; Samir Datta; Cheng Wang; Isabel J Sible; Sarah R Holley; Christa Watson; Eleanor R Palser; Nathaniel A Morris; Giovanni Battistella; Esther Rah; Marita Meyer; Mikhail Pakvasa; Maria Luisa Mandelli; Jessica Deleon; Fumiko Hoeft; Eduardo Caverzasi; Zachary A Miller; Kevin A Shapiro; Robert Hendren; Bruce L Miller; Maria Luisa Gorno-Tempini

doi:10.1016/j.cortex.2020.10.022

Enhanced visceromotor emotional reactivity in dyslexia and its relation to salience network connectivity

Cortex. 2021 Jan:134:278-295. doi: 10.1016/j.cortex.2020.10.022. Epub 2020 Nov 20.

Authors

Virginia E Sturm¹, Ashlin R K Roy², Samir Datta³, Cheng Wang⁴, Isabel J Sible⁵, Sarah R Holley⁶, Christa Watson⁷, Eleanor R Palser⁸, Nathaniel A Morris⁹, Giovanni Battistella¹⁰, Esther Rah¹¹, Marita Meyer¹², Mikhail Pakvasa¹³, Maria Luisa Mandelli¹⁴, Jessica Deleon¹⁵, Fumiko Hoeft¹⁶, Eduardo Caverzasi¹⁷, Zachary A Miller¹⁸, Kevin A Shapiro¹⁹, Robert Hendren²⁰, Bruce L Miller²¹, Maria Luisa Gorno-Tempini²²

Affiliations

¹ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA; Department of Psychiatry, University of California, San Francisco, CA, USA. Electronic address: virginia.sturm@ucsf.edu.
² Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: ashlin.roy@ucsf.edu.
³ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: samir.datta@ucsf.edu.
⁴ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: cwang.neurosci@outlook.com.
⁵ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: ijsible@gmail.com.
⁶ Department of Psychology, San Francisco State University, San Francisco, CA, USA. Electronic address: sholley@sfsu.edu.
⁷ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: christa.watson@ucsf.edu.
⁸ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: eleanor.palser@ucsf.edu.
⁹ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: nathaniel.morris@ucsf.edu.
¹⁰ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: giovanni.battistella@ucsf.edu.
¹¹ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: estherrah30@gmail.com.
¹² Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: meyerm77@gmail.com.
¹³ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: mkpakvasa@gmail.com.
¹⁴ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: marialuisa.mandelli@ucsf.edu.
¹⁵ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: jessica.deleon@ucsf.edu.
¹⁶ Department of Psychiatry, University of California, San Francisco, CA, USA. Electronic address: fumiko.hoeft@ucsf.edu.
¹⁷ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: eduardo.caverzasi@ucsf.edu.
¹⁸ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: zachary.miller2@ucsf.edu.
¹⁹ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: kevin.shapiro@gmail.com.
²⁰ Department of Psychiatry, University of California, San Francisco, CA, USA. Electronic address: robert.hendren@ucsf.edu.
²¹ Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA. Electronic address: bruce.miller@ucsf.edu.
²² Department of Neurology, University of California, UCSF Memory and Aging Center, Sandler Neurosciences Center, San Francisco, CA, USA; Department of Psychiatry, University of California, San Francisco, CA, USA. Electronic address: marialuisa.gornotempini@ucsf.edu.

Abstract

Dyslexia is a neurodevelopmental disorder mainly defined by reading difficulties. During reading, individuals with dyslexia exhibit hypoactivity in left-lateralized language systems. Lower activity in one brain circuit can be accompanied by greater activity in another, and, here, we examined whether right-hemisphere-based emotional reactivity may be elevated in dyslexia. We measured emotional reactivity (i.e., facial behavior, physiological activity, and subjective experience) in 54 children ages 7-12 with (n = 32) and without (n = 22) dyslexia while they viewed emotion-inducing film clips. Participants also underwent task-free functional magnetic resonance imaging. Parents of children with dyslexia completed the Behavior Assessment System for Children, which assesses real-world behavior. During film viewing, children with dyslexia exhibited significantly greater reactivity in emotional facial behavior, skin conductance level, and respiration rate than those without dyslexia. Across the sample, greater emotional facial behavior correlated with stronger connectivity between right ventral anterior insula and right pregenual anterior cingulate cortex (p_FWE<.05), key salience network hubs. In children with dyslexia, greater emotional facial behavior related to better real-world social skills and higher anxiety and depression. Our findings suggest there is heightened visceromotor emotional reactivity in dyslexia, which may lead to interpersonal strengths as well as affective vulnerabilities.

Keywords: Autonomic nervous system; Development; Emotion generation; Laterality; Reading.

Publication types

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

MeSH terms

Brain Mapping
Child
Dyslexia*
Emotions
Humans
Language
Magnetic Resonance Imaging
Reading

Abstract

Publication types

MeSH terms

Grants and funding