A 4-year longitudinal neuroimaging study of cognitive control using latent growth modeling: developmental changes and brain-behavior associations

Abstract

Despite theoretical models suggesting developmental changes in neural substrates of cognitive control in adolescence, empirical research has rarely examined intraindividual changes in cognitive control-related brain activation using multi-wave multivariate longitudinal data. We used longitudinal repeated measures of brain activation and behavioral performance during the multi-source interference task (MSIT) from 167 adolescents (53% male) who were assessed annually over four years from ages 13 to 17 years. We applied latent growth modeling to delineate the pattern of brain activation changes over time and to examine longitudinal associations between brain activation and behavioral performance. We identified brain regions that showed differential change patterns: (1) the fronto-parietal regions that involved bilateral insula, bilateral middle frontal gyrus, left pre-supplementary motor area, left inferior parietal lobule, and right precuneus; and (2) the rostral anterior cingulate cortex (rACC) region. Longitudinal confirmatory factor analyses of the fronto-parietal regions revealed strong measurement invariance across time implying that multivariate functional magnetic resonance imaging data during cognitive control can be measured reliably over time. Latent basis growth models indicated that fronto-parietal activation decreased over time, whereas rACC activation increased over time. In addition, behavioral performance data, age-related improvement was indicated by a decreasing trajectory of intraindividual variability in response time across four years. Testing longitudinal brain-behavior associations using multivariate growth models revealed that better behavioral cognitive control was associated with lower fronto-parietal activation, but the change in behavioral performance was not related to the change in brain activation. The current findings suggest that reduced effects of cognitive interference indicated by fronto-parietal recruitment may be a marker of a maturing brain that underlies better cognitive control performance during adolescence.

Neural cognitive control moderates the longitudinal link between hedonia and substance use across adolescence

“…Regarding cognitive control as a moderating factor for the effect of hedonia, we found that higher hedonia was significantly associated with higher substance use, only for adolescents with higher activation in frontoparietal regions during cognitive control. Research suggests that higher frontoparietal activation during cognitive control reflects less efficient neural functioning ( Crone and Steinbeis, 2017 , Kim-Spoon et al, 2021 , Luna et al, 2010 ) and individuals with substance use dependence show inefficiency of frontoparietal cortical activity during delay discounting ( Monterosso et al, 2007 ). Importantly, our results demonstrate that hedonia can be a risk factor, particularly when it is coupled with inefficient cognitive processing.…”

“…In a previous study, Kim-Spoon and colleagues (2021) reported that as adolescents’ behavioral cognitive control improves with age, frontoparietal activation decreased and rACC activation increased, suggesting that lower frontoparietal activation and higher rACC activation may implicate better cognitive control. In addition, they demonstrated measurement invariance in longitudinal confirmatory factor analysis based on the multiple ROIs in the frontoparietal regions across four years, implying longitudinal reliability of ROI indicators during the MSIT task ( Kim-Spoon et al, 2021 ).…”

“…Research suggests that earlier initiation of substance use in adolescence leads to poorer adjustment outcomes and further increases risk for substance use disorders and addiction ( Castellanos-Ryan et al, 2017 , Squeglia and Gray, 2016 ). Further, substance use during adolescence may increase vulnerability to the neurotoxic effects of these substances, especially in neurocognitive functioning related to risky decision making ( Kim-Spoon et al, 2021 , Schweinsburg et al, 2008 ). As such, it is important to understand risk and protective factors contributing to the development of substance use to inform prevention and intervention approaches during this developmentally salient period.…”

“…Though previous research has demonstrated that substance use during adolescence affects brain development and is associated with poorer cognitive functioning ( Lees et al, 2020 , Squeglia and Gray, 2016 ), it remains unclear whether cognitive control functions as a risk or protective factor for later substance use during this period. Recent longitudinal studies found that better performance during cognitive control is a protective factor against adolescent substance use ( Kim-Spoon et al, 2021 ), whereas impaired performance during cognitive control is a risk factor to adolescent substance use ( Morin et al, 2019 ). Prospective longitudinal studies that involve both behavioral and neuroimaging assessments are needed to enhance mechanistic understanding of the role that cognitive control plays in the development of substance use.…”

“…Previous research has established that brain regions within the prefrontal cortex are important for cognitive control development during childhood and adolescence ( Crone and Steinbeis, 2017 ). Longitudinal studies examining trajectories of cognitive control-related brain activation across adolescence have found developmental changes in frontoparietal regions (involved in interference inhibition), the dorsal and rostral anterior cingulate cortex (involved in error-processing), and the dorsolateral prefrontal cortex (involved in executive control; Kim-Spoon et al, 2021 ; Ordaz et al, 2013 ; Sebastian et al, 2013 ; Van Leijenhorst et al, 2010 ). Our conceptual framework focuses on the interaction between the reactive system (i.e., reward sensitivity) and the regulatory system (i.e., cognitive control) to understand the etiology of individual differences in adolescent risk-taking behaviors (see Kim-Spoon, Kahn et al, 2017 for a review).…”