fNIRS evidence of prefrontal regulation of frustration in early childhood

Abstract

The experience of frustration is common in early childhood, yet some children seem to possess a lower tolerance for frustration than others. Characterizing the biological mechanisms underlying a wide range of frustration tolerance observed in early childhood may inform maladaptive behavior and psychopathology that is associated with this construct. The goal of this study was to measure prefrontal correlates of frustration in 3-5-year-old children, who are not readily adaptable for typical neuroimaging approaches, using functional near infrared spectroscopy (fNIRS). fNIRS of frontal regions were measured as frustration was induced in children through a computer game where a desired and expected prize was "stolen" by an animated dog. A fNIRS general linear model (GLM) was used to quantify the correlation of brain regions with the task and identify areas that were statistically different between the winning and frustrating test conditions. A second-level voxel-based ANOVA analysis was then used to correlate the amplitude of each individual's brain activation with measure of parent-reported frustration. Experimental results indicated increased activity in the middle prefrontal cortex during winning of a desired prize, while lateral prefrontal cortex activity increased during frustration. Further, activity increase in lateral prefrontal cortex during frustration correlated positively with parent-reported frustration tolerance. These findings point to the role of the lateral prefrontal cortex as a potential region supporting the regulation of emotion during frustration.

Keywords: Development; Early childhood; Emotion regulation; Frustration; Prefrontal cortex; fNIRS.

Figure 1

A. Image of the portable CW6 fNIRS instrument (TechEn Inc, Milford, MA USA) used in this study. B. Image of a child demonstrating the placement of the fNIRS cap. C. Schematic of the fNIRS cap layout design.

Figure 2

Visual representation of the FETCH task along with the design matrix of the general linear model.

Figure 3

Brain activity contrast for the group-level hemoglobin signals during the Winning blocks minus the Frustration blocks. Each disk indicates the effect size (T-statistic) for the comparison of the two conditions in the general linear model for each fNIRS source-detector pair. Individual optical measurements that met p<0.05 [corrected] significance are outlined with dark lines. Each disk is drawn at the center of the location on the head sampled by that measurement pair. The approximate locations of the closest international 10–20 coordinates to the fNIRS probe are shown. Oxy- and deoxy-hemoglobin signals are shown in panels A and B respectively.

Figure 4

Reconstructed images of brain activity for the contrast of the Winning blocks minus the Frustration blocks. FNIRS data was reconstructed and displayed using an age-matched template of a brain for visualization purposes. Oxy- and deoxy-hemoglobin signals are shown in panels A and B respectively.

Figure 5

A. Map of brain regions correlated (p<0.05) with the frustration score in a group-level ANOVA regression model. B. Scatter plot of the mean oxy- and deoxy-hemoglobin from this region-of-interest and frustration score for each of the 17 subjects. Positive correlation is observed between the frustration score and the oxy- and deoxy-hemoglobin contrast of the Frustration minus Winning blocks in the left DLPFC