Developmental Sex Differences in Negative Emotion Decision-Making Dynamics: Computational Evidence and Amygdala-Prefrontal Pathways

Abstract

Sex differences in human emotion and related decision-making behaviors are recognized, which can be traced back early in development. However, our understanding of their underlying neurodevelopmental mechanisms remains elusive. Using developmental functional magnetic resonance imaging and computational approach, we investigated developmental sex differences in latent decision-making dynamics during negative emotion processing and related neurocognitive pathways in 243 school-aged children and 78 young adults. Behaviorally, girls exhibit higher response caution and more effective evidence accumulation, whereas boys show more impulsive response to negative facial expression stimuli. These effects parallel sex differences in emotion-related brain maturity linking to evidence accumulation, along with age-related decrease in emotional response in the basolateral amygdala and medial prefrontal cortex (MPFC) in girls and an increase in the centromedial amygdala (CMA) in boys. Moreover, girls exhibit age-related decreases in BLA–MPFC coupling linked to evidence accumulation, but boys exhibit increases in CMA–insula coupling associated with response caution. Our findings highlight the neurocomputational accounts for developmental sex differences in emotion and emotion-related behaviors and provide important implications into the neurodevelopmental mechanisms of sex differences in latent emotional decision-making dynamics. This informs the emergence of sex differences in typical and atypical neurodevelopment of children’s emotion and related functions.

Age‐related change in task‐evoked amygdala—prefrontal circuitry: A multiverse approach with an accelerated longitudinal cohort aged 4–22 years

“…Though a number of studies have examined age‐related changes from childhood to young adulthood in amygdala responses and amygdala—mPFC functional connectivity (FC) associated with emotional face stimuli, findings have varied widely (likely due in part to differences in sample composition and task design; see Table S1 for details). Several studies have found age‐related change in amygdala reactivity, including decreases as a function of age in response to emotional faces (Gee et al, 2013 ; Guyer et al, 2008 ; Killgore, Oki, & Yurgelun‐Todd, 2001 ; Passarotti, Sweeney, & Pavuluri, 2009 ; Swartz, Carrasco, Wiggins, Thomason, & Monk, 2014 ; Telzer et al, 2015 ) as well as other images (Decety, Michalska, & Kinzler, 2012 ; Silvers et al, 2017b ; Vink, Derks, Hoogendam, Hillegers, & Kahn, 2014 ), increases in amygdala reactivity with age (Joseph et al, 2015 ; Todd, Evans, Morris, Lewis, & Taylor, 2011 ), developmental sex differences (Xu et al, 2021 ) or peaks during adolescence (Hare et al, 2008 ; Vijayakumar, Pfeifer, Flournoy, Hernandez, & Dapretto, 2019 ). Others have observed no age‐related changes (Kujawa et al, 2016 ; Pfeifer et al, 2011 ; Pine et al, 2001 ; Wu et al, 2016 ; Yurgelun‐Todd & Killgore, 2006 ; Zhang, Padmanabhan, Gross, & Menon, 2019 ).…”

“…With task‐evoked amygdala—mPFC FC, several studies have found age‐related decreases from childhood to young adulthood (Gee et al, 2013 ; Kujawa et al, 2016 ; Silvers et al, 2017a ; Wu et al, 2016 ), while others have found increases (Decety et al, 2012 ; Perlman & Pelphrey, 2011 ; Vink et al, 2014 ), developmental sex differences (Xu et al, 2021 ), or little age‐related change (Zhang et al, 2019 ). While some investigations have found differing age‐related change for faces displaying different emotions (Killgore & Yurgelun‐Todd, 2007 ; Swartz et al, 2014 ; Vijayakumar et al, 2019 ), even investigations of fearful faces specifically have varied in their developmental findings for both amygdala reactivity and amygdala—mPFC FC (Forbes et al, 2011 ; Gee et al, 2013 ; Killgore et al, 2001 ; Wu et al, 2016 ; Zhang et al, 2019 ).…”

Correlations Between Psychological Status and Perception of Facial Expression

“…In addition to emotional factors, difficulties in facial affect recognition are associated with cognitive impairments, including attention and impulsivity. [16][17][18][19][20] In a review of facial emotional recognition in adolescents with attention deficit hyperactivity disorder (ADHD), Dan 16 reported that adolescents with ADHD found the recognition of facial expressions difficult due to differences in their brain activity. Löytömäki et al 17 stated that a delay in emotional recognition in patients with ADHD is associated with the linguistic and cognitive skills required for selective intervention procedures.…”

Age-related change in task-evoked amygdala—prefrontal circuitry: a multiverse approach with an accelerated longitudinal cohort aged 4-22 years

“…With task-evoked amygdala-mPFC FC, several studies have found age-related decreases from childhood to young adulthood (Gee et al, 2013;Kujawa et al, 2016;Silvers et al, 2017a;Wu et al, 2016), while others have found increases (Decety et al, 2012;Perlman & Pelphrey, 2011;Vink et al, 2014), developmental sex differences (Xu et al, 2021), or little age-Running head: AMYGDALA-MPFC AGE-RELATED CHANGE related change (Zhang et al, 2019). While some investigations have found differing agerelated change for faces displaying different emotions (Killgore & Yurgelun-Todd, 2007;Swartz et al, 2014;Vijayakumar et al, 2019), even investigations of fearful faces specifically have varied in their developmental findings for both amygdala reactivity and amygdala-mPFC functional connectivity (Forbes et al, 2011;Gee et al, 2013;Killgore et al, 2001;Wu et al, 2016Wu et al, , 2016Zhang et al, 2019).…”

“…Though a number of studies have examined age-related changes from childhood to young adulthood in amygdala responses and amygdala–mPFC functional connectivity (FC) associated with emotional face stimuli, findings have varied widely (likely due in part to differences in sample composition and task design; see sTable 1 for details). Several studies have found age-related change in amygdala reactivity, including decreases as a function of age in response to emotional faces (Gee et al, 2013; Guyer et al, 2008; Killgore et al, 2001; Passarotti et al, 2009; Swartz et al, 2014; Telzer et al, 2015) as well as other images (Decety et al, 2012; Silvers et al, 2017b; Vink et al, 2014), increases in amygdala reactivity with age (Joseph et al, 2015; Todd et al, 2011), developmental sex differences (Xu et al, 2021) or peaks during adolescence (Hare et al, 2008; Vijayakumar et al, 2019). Others have observed no age-related changes (Kujawa et al, 2016; Pfeifer et al, 2011; Pine et al, 2001; Wu et al, 2016; Yurgelun-Todd & Killgore, 2006; Zhang et al, 2019).…”