Effects of age, sex, and puberty on neural efficiency of cognitive and motor control in adolescents

Abstract

Critical changes in adolescence involve brain cognitive maturation of inhibitory control processes that are essential for a myriad of adult functions. Cognitive control advances into adulthood as there is more flexible integration of component processes, including inhibitory control of conflicting information, overwriting inappropriate response tendencies, and amplifying relevant responses for accurate execution. Using a modified Stroop task with fMRI, we investigated the effects of age, sex, and puberty on brain functional correlates of cognitive and motor control in 87 boys and 91 girls across the adolescent age range. Results revealed dissociable brain systems for cognitive and motor control processes, whereby adolescents flexibly adapted neural responses to control demands. Specifically, when response repetitions facilitated planning-based action selection, frontoparietal-insular regions associated with cognitive control operations were less activated, whereas cortical-pallidal-cerebellar motor regions associated with motor skill acquisition, were more activated. Attenuated middle cingulate cortex activation occurred with older adolescent age for both motor control and cognitive control with automaticity from repetition learning. Sexual dimorphism for control operations occurred in extrastriate cortices involved in visuo-attentional selection: While boys enhanced extrastriate selection processes for motor control, girls activated these regions more for cognitive control. These sex differences were attenuated with more advanced pubertal stage. Together, our findings show that brain cognitive and motor control processes are segregated, demand-specific, more efficient in older adolescents, and differ between sexes relative to pubertal development. Our findings advance our understanding of how distributed brain activity and the neurodevelopment of automaticity enhances cognitive and motor control ability in adolescence.

Keywords: Age and gender; Automaticity of behavior; Executive control; Functional MRI; Puberty.

Figure 1. Age and pubertal stage distributions for girls and boys.

Despite similar chronological ages (left panel), boys had on average lower pubertal development scores (PDS) than girls (right upper panel) using the self-assessment Pubertal Development Scale (PDS; Petersen et al. 1988) (Table 1). Age and pubertal development were more strongly correlated in boys than girls (right lower panel).

Figure 2. Stroop Match-to-Sample fMRI paradigm.

Subjects were asked to match the color of a sample to the font color of the Stroop target and press a YES-key for color matches and a NO-key for non-matches. Stroop targets were color words printed in a font color that was either congruent (e.g., the word BLUE printed in blue font) or incongruent (the word BLUE printed in green font) to the word’s meaning. The task had four conditions: congruent-match, incongruent-match, congruent-nonmatch, and incongruent nonmatch, which were presented in blocks of trials requiring response switching (RS), i.e., when match and nonmatch trials were mixed in a block, or response repetitions (RR), i.e., when either match or nonmatch trials were presented in a block.

Figure 3. Stroop Match-to-Sample task: Behavior.

Mean response time (RT) and standard to incongruent (inc) and congruent (con) Stroop words for response switching (RS) and response repetition (RR) blocks of trials in adolescent girls and boys. The Stroop effect (green) is defined as the difference in RT between incongruent and congruent trials (Diff RT_INC-CON). Behavioral Stroop effects were larger for RR than RS in girls and in boys.

Figure 4. Cognitive Control.

Stroop-related activation (upper panels): Incongruent in contrast to congruent Stroop conditions (inc>con: in red-to-yellow; all trials) activated a bilateral fronto-parietal network, also including subcortical (thalamus, striatum, limbic) and cerebellar regions; the opposite contrast (con>inc: in blue-to-green) activated medial prefrontal and parietal regions. Stroop contrasts (inc>con) conducted separately for response switching (Stroop-RS) and response repetition blocks of trials (Stroop-RR). Motor Control. Response mode-related activation (lower panels): Response switching (RS), contrasted to response repetition (RR) blocks of trials (RS>RR, all trials) activated a cerebellar-motor cortical circuitry, also including lateral parietal, temporal, insula, and thalamic regions (in red-to-yellow); the opposite contrast (RR>RS) activated prefrontal, lateral and medial frontal areas, also including supplementary motor area, angular, fusiform, and cerebellar regions (in blue-to-green). Response mode contrasts conducted separately for non-conflict congruent trials showed cerebellar–motor cortical network activation (lower panel).

Figure 5. Age-related Activation.

Correlation graphs depict age effects (Tables 3C, 5C). Cognitive control. With older age, left parietal and occipito-temporal regions were more activated to Stroop-RS (in cyan; left panels) and the middle cingulate cortex (MCC) was less activated to Stroop-RR (in green; middle panels). Motor Control: With older age, the MCC was less activated during RS than RR for non-conflict congruent trials (in green; right panels).

Figure 6. Sex Differences in Activation.

Girls (in pink) activated extrastriate fusiform and lingual areas more than boys (in blue) during cognitive control (Stroop conflict, inc>con, Table 2B). Boys activated the right superior temporal and left lingual gyri more than girls during motor control (RSRR, Table 4B). Relation to Puberty. Pubertal development (PDS) scores correlated with extrastriate activation such that sex differences gradually decreased with more advanced puberty.