Elsevier

Cortex

Volume 134, January 2021, Pages 278-295
Cortex

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

https://doi.org/10.1016/j.cortex.2020.10.022Get rights and content

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 (pFWE<.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.

Introduction

Dyslexia is a common neurodevelopmental disorder characterized by prominent reading difficulties, and approximately 5–17% of children and adults have significant trouble learning to read despite adequate intelligence, effort, and education (S. E. Shaywitz, 1998; Silani et al., 2005). Reading is a complex process during which meaning is extracted from written words via visual and language systems (Gaillard, Balsamo, Ibrahim, Sachs, & Xu, 2003; Wandell & Le, 2017). Dyslexia is a heterogeneous disorder, but a problem with phonological processing—the ability to break words down into smaller sound units and then to associate these sound units with the written word (S. E. Shaywitz, 1998)—is the most common underlying mechanism (Bradley & Bryant, 1983; Frith, 1999; Lyon, Shaywitz, & Shaywitz, 2003; O'Brien, Wolf, & Lovett, 2012).

Neuroanatomical studies of classic phonological dyslexia have revealed altered brain structure and function in predominantly left-lateralized language systems (Goswami, 2008; Norton, Beach, & Gabrieli, 2015; Richlan, 2012; Silani et al., 2005). While post-mortem studies have shown reduced leftward asymmetry of the planum temporale in dyslexia (Galaburda, 1994; Vanderauwera et al., 2016), neuroimaging studies have found smaller gray matter volume in the left fusiform gyrus and left inferior temporal gyrus (Kronbichler et al., 2008; Linkersdorfer, Lonnemann, Lindberg, Hasselhorn, & Fiebach, 2012), smaller gray matter volume and reduced cortical thickness in left occipitotemporal cortex (Krafnick, Flowers, Luetje, Napoliello, & Eden, 2014; Williams, Juranek, Cirino, & Fletcher, 2018), lower fractional anisotropy in white matter tracts (Vandermosten, Boets, Wouters, & Ghesquière, 2012), and enhanced gyrification of left lateral temporal and middle frontal gyri (Caverzasi et al., 2018) in dyslexia. Functional neuroimaging studies that measure brain activity during reading and phonological decision-making tasks have found that individuals with dyslexia exhibit hypoactivation of bilateral temporoparietal and left occipitotemporal structures, regions that support reading (Hoeft et al., 2007; Paulesu, Danelli, & Berlingeri, 2014; Richlan, Kronbichler, & Wimmer, 2011, 2013). Similar patterns have been found in pre-reading children with a family history of dyslexia who also exhibit smaller gray matter volume (Brambati et al., 2004; Raschle, Chang, & Gaab, 2011; Raschle et al., 2017), atypical sulcal patterns (Im, Raschle, Smith, Ellen Grant, & Gaab, 2016), lower functional and structural connectivity (Kuhl et al., 2020; Skeide et al., 2015), white matter alterations (Langer et al., 2017; Vanderauwera, Wouters, Vandermosten, & Ghesquière, 2017; Vandermosten et al., 2015), and lower functional activity during phonological processing (Raschle, Zuk, & Gaab, 2012) in language networks. Taken together, these studies offer convergent evidence that dyslexia is characterized by predominant neural alterations in the left hemisphere. There is some variability across studies, however, with others suggesting the anatomical underpinnings of dyslexia are more diffuse and involve the right hemisphere as well (Beelen, Vanderauwera, Wouters, Vandermosten, & Ghesquière, 2019; Raschle et al., 2011).

In various clinical disorders, lateralized dysfunction in one hemisphere may facilitate function in the other, an imbalance that can lead to strengths as well as vulnerabilities (Kapur, 1996; B. L. Miller, Ponton, Benson, Cummings, & Mena, 1996; Seeley, Matthews, et al., 2008; Zhou et al., 2010). Language and emotions have long been associated with opposing hemispheres of the brain: while the left hemisphere is crucial for language, the right hemisphere plays a dominant role in emotion generation and recognition (Blonder, Bowers, & Heilman, 1991; Borod et al., 1998; Demaree, Everhart, Youngstrom, & Harrison, 2005; Gainotti, 1972; Tucker, 1981). Emotions are adaptive, multisystem responses that are accompanied by coordinated changes in autonomic nervous system activity and facial expression (i.e., herein, “visceromotor” activities), rapid bursts of activity that sweep across the body and move an individual from rest to action (Levenson, 2003). In clinical studies, individuals with predominant right hemisphere damage often have diminished emotional expression and impaired recognition of emotional faces, prosody, and gestures (Blonder et al., 1991; Borod et al., 1998; Sturm, Ascher, Miller, & Levenson, 2008). In dyslexia, there is some indication that diminished functioning in language systems in the left hemisphere is accompanied by accentuated functioning in emotion systems in the right. In addition to hypoactivity in left hemisphere language systems during phonological processing tasks, for example, individuals with dyslexia exhibit hyperactivity in right hemisphere regions that promote emotions including the anterior insula and thalamus (Maisog, Einbinder, Flowers, Turkeltaub, & Eden, 2008; Richlan, Kronbichler, & Wimmer, 2009).

The salience network, an intrinsic connectivity network anchored by structures in the right hemisphere, plays a central role in emotion generation and sensation (Seeley et al., 2007; Seeley, Zhou, & Kim, 2012). Intrinsic connectivity networks are comprised of spatially distributed brain regions that exhibit synchronous blood oxygen level-dependent (BOLD) fluctuations in task-free settings and support various cognitive, motor, sensory, social, and affective processes (Beckmann, DeLuca, Devlin, & Smith, 2005; Fox et al., 2005). The salience network has primary hubs in the right ventral anterior insula (vAI) and right anterior cingulate cortex (ACC), regions that typically coactivate during a wide range of functional neuroimaging studies including those that elicit emotions, empathy, pain, and reward (Craig, 2009, 2011). Through projections to subcortical structures (i.e., hypothalamus, central nucleus of the amygdala, periaqueductal gray, and brainstem nuclei), the ACC and vAI play critical roles in visceromotor emotion generation and interoception, triggering and sensing the physiological and motor changes that arise during emotions (Craig, 2002; Critchley & Harrison, 2013; Levenson, 1994; Ongur & Price, 2000; Saper, 2002; Seeley et al., 2012; Vogt, 2005). Salience network connectivity, which is reliable over time and considered to be trait-like, varies in strength across people (C. C. Guo et al., 2012) and relates to variability in socioemotional sensitivity (Toller et al., 2018) such that individuals with stronger salience network connectivity are inclined to have more intense physiological and experiential reactions to affectively charged contexts than those with lower salience network connectivity (Hermans et al., 2011; Seeley et al., 2007; Xia, Touroutoglou, Quigley, Feldman Barrett, & Dickerson, 2017). Although the salience network is detectable in infancy and has a spatial topography that resembles adults (Gao, Alcauter, Smith, Gilmore, & Lin, 2015), its connections may expand and get stronger during childhood and adolescence (Uddin, Supekar, Ryali, & Menon, 2011; Zielinski, Gennatas, Zhou, & Seeley, 2010).

By guiding behavior and coloring subjective experience, emotions play an important role in everyday life and are critical for physical survival and social harmony (Levenson, 1994). Emotions not only help people to stay safe from physical threats but also encourage them to form and maintain close interpersonal bonds (Griskevicius, Shiota, & Neufeld, 2010; Lerner & Keltner, 2000). Individuals who manage their emotions with ease are better equipped to navigate complex interpersonal situations and to develop meaningful social connections (Eisenberg, Spinrad, & Eggum, 2010; Lopes, Mestre, Guil, Kremenitzer, & Salovey, 2012; Lopes, Salovey, Côté, Beers, & Petty, 2005). In children and adolescents, those who express their emotions in adaptive ways are more socially adept, more likable, and less anxious in everyday life (Denham, McKinley, Couchoud, & Holt, 1990; Lopes et al., 2012; A. L.; Miller et al., 2006), whereas those who tend to express high-intensity emotions have poorer mental health, lower social skills, and less robust relationships with teachers, parents, and peers (Eisenberg et al., 1993, 2010; Frick & Morris, 2004). While some prior research suggests children with dyslexia have poorer social skills than those without dyslexia (Parhiala et al., 2015), this finding is not consistent, and other studies have found that children and adults with dyslexia are rated as socially competent (Frederickson & Jacobs, 2001; Hellendoorn & Ruijssenaars, 2000). Although experiencing emotions is often advantageous, emotions that are too frequent or too intense can be problematic and lead to affective symptoms (Cole, Michel, & Teti, 1994, pp. 73–100; Kring & Sloan, 2009). Affective symptoms, which are associated with alterations in gray matter volume and functional connectivity in salience network structures (Davis, Margolis, Thomas, Huo, & Marsh, 2018; Goodkind et al., 2015; Sha, Wager, Mechelli, & He, 2019), are common in dyslexia (Carroll & Iles, 2006; Haft, Duong, Ho, Hendren, & Hoeft, 2019; Hendren, Haft, Black, White, & Hoeft, 2018; Novita, 2016). Children with dyslexia and reading disorders often report feelings of anxiety and depression (Mugnaini, Lassi, La Malfa, & Albertini, 2009; Willcutt & Pennington, 2000), and even mild reading deficits in children ages 8–12 are associated with lower mood and self-esteem (Casey, Levy, Brown, & Brooks-Gunn, 1992).

In the present study, we investigated whether children with phonological dyslexia have enhanced emotional reactivity. Children with and without dyslexia underwent a laboratory-based assessment of emotion and “resting state,” task-free functional magnetic resonance imaging (tf-fMRI). Parents of children with dyslexia also reported on their child's real-world social behavior, mood, and anxiety. To measure emotional reactivity, participants viewed five film clips that elicited specific positive and negative emotions while facial behavior and physiological activity were recorded continuously. Subjective experience was also assessed after each film clip by asking participants to rate how much they felt various specific emotions. We hypothesized that children with dyslexia would show accentuated emotional reactivity while viewing the film clips and that greater emotional reactivity would relate to stronger intrinsic connectivity between right vAI and right ACC, key salience network hubs. Given that emotional reactivity has been associated with social advantages (Lopes et al., 2005) as well as affective vulnerabilities (Cole et al., 1994, pp. 73–100; Kring & Sloan, 2009), we expected that higher emotional reactivity in dyslexia may be associated with greater interpersonal strengths as well as greater symptoms of anxiety and depression.

Section snippets

Materials and methods

We report how we determined our sample size, all data exclusions, all inclusion and exclusion criteria, whether inclusion/exclusion criteria were established prior to data analysis, all manipulations, and all measures included in the present study.

Participant demographics and clinical information

The groups of children with and without dyslexia included approximately equal numbers of girls and boys and had a similar mean age, which was 10 years old (see Table 1). The groups did not differ in handedness, and both were comprised of children of comparable ethnic backgrounds and socioemotional statuses (as measured by the mean annual income of the families). In general, both groups were predominantly white and had annual family income levels that ranged from the low average to above average

Discussion

We found evidence for elevated visceromotor emotional reactivity in dyslexia. While viewing emotion-eliciting film clips, children with dyslexia exhibited greater reactivity in emotional facial behavior, skin conductance level, and respiration rate than children without dyslexia. The groups did not differ in heart rate reactivity during the film-viewing task. There was no significant difference between the groups in subjective emotional experience, even when accounting for lower emotion word

Funding

This work was supported by the University of California, San Francisco Dyslexia Center; the Charles and Helen Schwab Foundation; the National Institute of Neurological Disorders and Stroke (R01NS050915); and the National Institutes of Health (K24DC015544).

CRediT author statement

Virginia E. Sturm: Conceptualization, Methodology, Writing-Original Draft, Writing-Review & Editing, Visualization, Supervision, Funding acquisition.

Ashlin R.K. Roy: Writing-Original Draft, Writing-Review & Editing, Visualization, Formal analysis, Data Curation, Methodology.

Samir Datta: Writing-Original Draft, Writing-Review & Editing, Visualization, Formal analysis, Data Curation, Methodology.

Cheng Wang: Formal analysis, Visualization.

Isabel J. Sible: Investigation, Methodology, Project

Declaration of competing interest

The authors report no competing interests.

Acknowledgements

We are grateful to the children and their families for participating in this research.

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