Increased functional selectivity over development in rostrolateral prefrontal cortex

Abstract

Relational reasoning, or the ability to identify and consider relationships between multiple mental representations, is a fundamental component of high-level cognition (Robin and Holyoak, 1995). The capacity to reason with relations enables abstract thought and may be at the core of what makes human cognition unique (Penn et al., 2008). This capacity improves throughout childhood and adolescence (Ferrer et al., 2009). Here, we sought to better understand the neural mechanisms that support its emergence. We have hypothesized previously, based on fMRI research in adults, that (1) inferior parietal lobe (IPL) plays a central role in representing relationships between mental representations (first-order relations) and (2) rostrolateral prefrontal cortex (RLPFC) integrates inputs from IPL to build second-order relational structures (i.e., relations between relations). In the present study, we examined fMRI and cortical thickness data from 85 children and adolescents (ages 6-18 years). Participants performed a relational matching task in which they viewed arrays of four visual stimuli and determined whether two stimuli shared a particular feature (a first-order relational judgment) or whether two pairs of stimuli matched according to the same feature (a second-order relational judgment). fMRI results provide evidence for increased functional selectivity across ages 6-18 years in RLPFC and IPL. Specifically, young children engaged RLPFC and IPL indiscriminately for first-order and second-order relational judgments, and activation for first-order relations diminished with age whereas activation for second-order relations stayed elevated. Examination of cortical thickness revealed that increased functional selectivity in RLPFC could be partly accounted for by cortical thinning in IPL.

Figure 1.

Task illustration. Each trial consisted of a yes/no judgment based on a stimulus array that contained four patterned shapes. On Shape trials, participants determined whether there was a shape match in either pair. On Pattern trials, participants determined whether there was a pattern match in either pair. On Match trials, participants decided whether the bottom pair of stimuli matched along the same dimension (i.e., Shape or Pattern) as the top pair of stimuli. Shape and Pattern trials require first-order relational processing, whereas Match trials require second-order relational integration.

Figure 2.

Behavioral performance on the relational matching task. Scatter plots show accuracy (top) and response time (bottom) versus age for the first-order and second-order conditions.

Figure 3.

Functional activation versus age for left RLPFC. A significant decrease with age is observed for first-order (left plot) but not for second-order (right plot).

Figure 4.

Functional activation by age group for six ROIs, including left and right RLPFC, DLPFC, and IPL. Data are plotted for younger children (ages 7–10 years), middle-aged children (ages 11–14 years), and older children (ages 15–18 years).

Figure 5.

Whole-brain activation for the second-order > first-order contrast, for younger children (red), middle children (green), and older children (blue). Areas of overlap between the younger and middle children are shown in yellow.

Figure 6.

Cortical thinning in RLPFC, DLPFC, and IPL. Results are shown for the left side only but were similar on the right.

Figure 7.

Structured equation model relating age, cortical thickness, and fMRI activation in left RLPFC and IPL. Only connections that yielded standardized parameter estimated >0.1 are depicted, with line thickness corresponding approximately to the magnitude of the parameter estimate and color indicating the direction of the relationship (solid/green for positive, dashed/red for negative).