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9 CLASIFICACIÓN DE EXCEPCIONES SEGÚN LA DOCTRINA

Many studies have examined the neural structure in ADHD and other externalizing prob-

lems. A common finding in these studies is differences, typically smaller volume or thinner

cortex, in the PFC and ACC (for a review and meta-analysis of studies in adults, see Yang & Raine, 2009), but other regions are involved, as well (e.g., amygdala; Pardini, Erickson,

Loeber, and Raine, 2014; temporal regions; Michalska, Decety, Zeffiro, and Lahey, 2015). Smaller PFC gray matter volume has been associated with antisocial personality disorder

in adults (Raine, Lencz, Bihrle, LaCasse, & Colletti, 2000). A study examining the brain

structure underlying conduct disorder (CD) symptoms in 22, 14–20-year-old adolescent girls using MRI found that aggressive CD symptoms were associated with smaller DLPFC vol-

ume (Fairchild, Hagan, Walsh, Passamonti, Calder, & Goodyer, 2013). A study comparing

23 boys from ages 12 to 17 with CD and 23 typically-developing boys found a smaller OFC in the boys with CD compared to the typically-developing boys (Huebner et al., 2008).

Regarding the brain structure underlying ADHD, a common finding is that children with ADHD have a thinner cortex than do typically-developing children (Narr et al., 2009).

An MRI study found that 32 children with ADHD had a thinner ACC than did 15 typically-

developing children from ages 9–15 (Bledsoe, Semrud-Clikeman, & Pliszka, 2013). More- over, over one-third of the variance in parents’ ratings of ADHD symptoms was explained

by ACC thickness. The authors interpreted the thinner ACC in ADHD compared to that

found in typically-developing children as reflecting a compromised anterior attention net- work involved in error detection, impulsivity, and inhibitory control. A prospective study

found that a shorter corpus callosum in 784, 6-week-old infants was associated with poorer

executive functioning and inhibition at 4 years of age (Ghassabian et al., 2013). The length of the corpus callosum did not predict later ADHD symptoms, however. An MRI study

found that, compared to 22 community-reared children, 58 children reared in institutions

showed less cortical thickness in many brain regions at 8–10 years of age, including the PFC (McLaughlin, Sheridan, Winter, Fox, Zeanah, & Nelson, 2014). The smaller cortical

thickness mediated the effects of institutionalization on teacher-reported ADHD symptoms.

Several longitudinal studies have examined the neurophysiological development of ADHD (Shaw, Eckstrand, et al., 2007; Shaw, Lerch, et al., 2006; Shaw, Malek, Watson, Green-

stein, Rossi, & Sharp, 2013). One study by Shaw and colleagues (Shaw, Lerch, et al., 2006)

compared the cortical thickness of 163 children with ADHD and 166 typically-developing children using MRI. Four MRI assessments were conducted at the following ages: (1) 7–13

years old, (2) 9–16, (3) 11–18, and (4) 13–22. The study found that, at intake, children with ADHD had a thinner cortex than did controls, particularly in the PFC, cingulate cortex,

outcomes during follow-up assessments had thinner cortices in similar prefrontal regions compared to children with ADHD at intake who showed better outcomes in later assess-

ments, as measured by the Children’s Global Assessment Scale. The authors interpreted

the thinner PFC and ACC as possibly reflecting the attention or response inhibition deficits found in ADHD. The authors interpreted the thinner precentral gyrus in ADHD as possibly

reflecting motor hyperactivity or deficient response inhibition. The authors found no dif-

ferences, however, in the growth rate of cortical thickness over time between children with ADHD and controls, with the exception of regions of the parietal cortex (whose thickness

eventually converged with that of controls).

A subsequent study by Shaw’s research team compared the growth trajectories of cortical thickness among 223 children with ADHD compared to 223 typically-developing children

(Shaw, Eckstrand, et al., 2007). The authors found that although trajectories of the rates

of cortical thickening were similar between ADHD and typically-developing children, the children with ADHD showed delayed cortical thickening compared to typically-developing

children. Typically-developing children reached peak cortical thickness by 71/2years of age,

on average, whereas children with ADHD reached peak cortical thickness by 101/2years, on average. The greatest delays in cortical thickening were observed in the middle PFC, where

ADHD children showed delays of approximately 5 years relative to typically-developing

children in terms of cortical thickness. The finding of a lag in brain development in ADHD has been replicated using connectomic analyses of brain networks (Sripada, Kessler, &

Angstadt, 2014).

A third study by Shaw’s research group examined the trajectories of cortical thickening from childhood into adulthood among 92 participants diagnosed with ADHD as children in

relation to ADHD symptoms in adulthood (Shaw, Malek, et al., 2013). The study observed that cortical thinning over time in the medial and dorsolateral PFC was associated with

greater inattentive, but not hyperactive/impulsive, ADHD symptoms in adulthood.

In addition to longitudinal studies of the brain structure in ADHD, another longitudinal study examined the brain structure in general externalizing problems (Ameis et al., 2014).

The study followed 297 children at ages 6–18 years using MRI at 2-year intervals for up

to 3 assessments (517 total scans). Despite the study’s longitudinal design and analytical approach that took into account the dependence of repeated measures data (hierarchical

linear modeling), the study only examined whether brain structure was associated with the

level (i.e., intercept) of externalizing problems and not the development of externalizing problems over time. Externalizing problems were associated with a thinner cortex in the

left OFC and right cingulate cortex. In addition, children with fewer externalizing problems

showed a positive association between OFC and amygdala thickness, whereas children with more externalizing problems showed no association between OFC and amygdala thickness.

This finding is consistent with findings of reduced functional coupling of the OFC and

amygdala in children with ODD/CD and psychopathic traits (Marsh et al., 2013; but see Sarkar et al., 2013).

Another longitudinal study examined change in ACC thickness, self-regulation, and

externalizing problems from ages 12–16 years in 92 adolescents who were selected based on their representing a full range of risk on temperamental negative emotionality and

self-regulation (Vijayakumar, Whittle, Dennison, Y¨ucel, Simmons, & Allen, 2014). Self-

regulation was measured by self reports of their temperamental effortful control. External- izing problems—aggression and risk taking—were also measured by self report. Adolescence

is a period of normative pruning of inefficient synaptic connections, and increases in white matter (via myelination) that result in cortical thinning of gray matter. The authors found

that less cortical thinning in the left ACC from age 12 to 16 was associated with the

development of self-regulation deficits and externalizing problems. Moreover, changes in self-regulation mediated the effect of ACC thinning on changes in externalizing problems,

suggesting that self-regulation may be an underlying, intermediate phenotype of external-

izing problems. These findings are consistent with findings from a study of 5–10-year-old children, in which children with thinner cortex in the PFC (right IFG) and ACC had better

inhibitory control performance on a Simon task (Kharitonova, Martin, Gabrieli, & Sheri-

dan, 2013). In addition, the association between age and inhibitory control was mediated by PFC and ACC thickness. Thus, the development of inhibitory control and externaliz-

ing problems may be explained by the extent of synaptic pruning and cortical gray-matter

thinning in the PFC and ACC.

In sum, compared to typically-developing children, children with ADHD and other ex-

ternalizing problems show a smaller or thinner cortex in brain regions such as the PFC

and ACC that are associated with sustained attention, response inhibition, and higher- order cognitive control processes. Interestingly, the thinner cortex in ADHD compared to

typically-developing children appears to result from a delay in cortical development rather

than a qualitatively distinct trajectory of brain development. In other words, children with ADHD and typically-developing children show similar rates of cortical development when

cortical thickening begins, but children with ADHD may have a delayed onset of cortical thickening. Moreover, less cortical gray-matter thinning in the PFC and ACC during ado-

deficits and externalizing problems. These neural differences (delayed onset of cortical thickening and less cortical thinning in the PFC and ACC during synaptic pruning) may

underlie the symptoms present in ADHD and other disorders of disinhibition. The effects

of the neural differences in ADHD and externalizing problems may be explained through their effects on self-regulation.