A three‐wave longitudinal study of subcortical–cortical resting‐state connectivity in adolescence: Testing age‐ and puberty‐related changes

Abstract

Adolescence is the transitional period between childhood and adulthood, characterized by substantial changes in reward‐driven behavior. Although reward‐driven behavior is supported by subcortical‐medial prefrontal cortex (PFC) connectivity, the development of these circuits is not well understood. Particularly, while puberty has been hypothesized to accelerate organization and activation of functional neural circuits, the relationship between age, sex, pubertal change, and functional connectivity has hardly been studied. Here, we present an analysis of resting‐state functional connectivity between subcortical structures and the medial PFC, in 661 scans of 273 participants between 8 and 29 years, using a three‐wave longitudinal design. Generalized additive mixed model procedures were used to assess the effects of age, sex, and self‐reported pubertal status on connectivity between subcortical structures (nucleus accumbens, caudate, putamen, hippocampus, and amygdala) and cortical medial structures (dorsal anterior cingulate, ventral anterior cingulate, subcallosal cortex, frontal medial cortex). We observed an age‐related strengthening of subcortico‐subcortical and cortico‐cortical connectivity. Subcortical–cortical connectivity, such as, between the nucleus accumbens—frontal medial cortex, and the caudate—dorsal anterior cingulate cortex, however, weakened across age. Model‐based comparisons revealed that for specific connections pubertal development described developmental change better than chronological age. This was particularly the case for changes in subcortical–cortical connectivity and distinctively for boys and girls. Together, these findings indicate changes in functional network strengthening with pubertal development. These changes in functional connectivity may maximize the neural efficiency of interregional communication and set the stage for further inquiry of biological factors driving adolescent functional connectivity changes.

Dopamine-related striatal neurophysiology is associated with specialization of frontostriatal reward circuitry through adolescence

“…Adolescence. Our results showing significant developmental decreases in vmPFC -NAcc coupling, evident in both reward and rest contexts, are in agreement with previous resting state and task-based fMRI studies showing developmental decreases in PFC -NAcc connectivity Fareri et al, 2015;Porter et al, 2015;Supekar et al, 2009;Van Duijvenvoorde et al, 2016;Van Duijvenvoorde et al, 2019, but see Van Den Bos et al, 2012 who showed increases in task-related connectivity between late childhood and early adolescence). These changes may be influenced by changes in DAergic processing and may contribute to known changes in adolescent reward processing.…”

Developmental Maturation of the Precuneus as a Functional Core of the Default Mode Network

“…Data at the second longitudinal time point (T2) were collected approximately 2 years later from 254 of the original participants (mean age = 16.07 years, age range = 9.92-26.62 years; 131 female). Although previous articles have published findings from the BrainTime study's restingstate data (van Duijvenvoorde, Westhoff, de Vos, Wierenga, & Crone, 2019;Peters, Peper, van Duijvenvoorde, Braams, & Crone, 2017;Peters, Jolles, van Duijvenvoorde, Crone, & Peper, 2015;van Duijvenvoorde, Achterberg, Braams, Peters, & Crone, 2015) and data from its two tasks separately (Schreuders et al, 2018;Braams & Crone, 2017a, 2017bPeters, Van der Meulen, Zanolie, & Crone, 2017;Braams, Peper, Van Der Heide, Peters, & Crone, 2016;Peters, van Duijvenvoorde, Koolschijn, & Crone, 2016;Braams, van Duijvenvoorde, Peper, & Crone, 2015;Braams, Peters, Peper, Güroğlu, & Crone, 2014;Peters, Braams, Raijmakers, Koolschijn, & Crone, 2014;Peters, Koolschijn, Crone, van Duijvenvoorde, & Raijmakers, 2014), this is the first study integrating all of the functional task and rest data from BrainTime's first two longitudinal time points.…”

Development of the Brain Functional Connectome Follows Puberty-Dependent Nonlinear Trajectories

“…Pubertal status showed a faster growth rate in females compared to males. Although self-reported questionnaires are sensitive to inaccuracies (Dorn et al, 2006), the pattern observed has been replicated in other populations (Braams et al, 2015;Wierenga et al, 2018;van Duijvenvoorde et al, 2019). Pubertal scale scores showed a faster growth rate in females around level 2 and 12 years of age compared to males.…”

“…This scale allows to take into account sex-specific patterns of puberty development even at the same chronological age. Children under 10 years old were set to level 1 of the PDS, as previous studies have shown similar values at these ages (Hibberd et al, 2015;van Duijvenvoorde et al, 2019). Missing values corresponding to 8 time-points (4 females) were estimated with two age-smooth splines by sex with a Generalized Additive Mixed Model (GAMM) following van Duijvenvoorde et al (2019).…”

“…Besides, the pubertal spurt is an important source of variability in adolescence when considering developmental trajectories based on chronological age, but it is rarely considered (Blakemore et al, 2010;Vijayakumar et al, 2018). A pair of recent studies have taken an important step in this direction, by fitting the developmental trajectories of fronto-subcortical connectivity with the pubertal stage (Spielberg et al, 2014;van Duijvenvoorde et al, 2019). However, the relationship between the pubertal stage and the developmental of the brain functional organization still remains largely unexplored.…”