A time of change: Behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues

Adolescence is a developmental period that entails substantial changes in affective and incentive-seeking behavior relative to both childhood and adulthood, including a heightened propensity to engage in risky behaviors and experience persistent negative and labile mood states. This review discusses the emotional and incentive-driven behavioral changes in adolescents and their associated neural mechanisms, focusing on the dynamic interactions between the amygdala, ventral striatum, and prefrontal cortex. Common behavioral changes during adolescence may be associated with a heightened responsiveness to incentives and emotional cues while the capacity to effectively engage in cognitive and emotion regulation is still relatively immature. We highlight empirical work in humans and animals that addresses the interactions between these neural systems in adolescents relative to children and adults, and propose a neurobiological model that may account for the nonlinear changes in adolescent behavior. Finally, we discuss other influences that may contribute to exaggerated reward and emotion processing associated with adolescence, including hormonal fluctuations and the role of the social environment.     

Sex differences in early childhood, adolescence, and adulthood on cognitive tasks that rely on orbital prefrontal cortex

Through the use of several tests of cognition we have documented sex differences in young children, adolescents, and adults on tasks that rely on the integrity of the orbital prefrontal cortex. In children under three years of age, males performed with significantly fewer errors than did females on tests of object reversals. No significant sex differences were found in older children, despite the use of a more challenging object reversal task. Sex differences were also found in adolescents and adults on the Iowa Gambling Task. On this decision-making task, in contrast to males, females appear to be responding to different elements of the task. Discussion of the implications for these findings is presented.     

Neural correlates of autobiographical memory retrieval in children and adults

Autobiographical memory (AM) is a critically important form of memory for life events that undergoes substantial developmental changes from childhood to adulthood. Relatively little is known regarding the functional neural correlates of AM retrieval in children as assessed with fMRI, and how they may differ from adults. We investigated this question with 14 children ages 8–11 years and 14 adults ages 19–30 years, contrasting AM retrieval with semantic memory (SM) retrieval. During scanning, participants were cued by verbal prompts to retrieve previously selected recent AMs or to verify semantic properties of words. As predicted, both groups showed AM retrieval-related increased activation in regions implicated in prior studies, including bilateral hippocampus, and prefrontal, posterior cingulate, and parietal cortices. Adults showed greater activation in the hippocampal/parahippocampal region as well as prefrontal and parietal cortex, relative to children; age-related differences were most prominent in the first 8?sec versus the second 8?sec of AM retrieval and when AM retrieval was contrasted with semantic retrieval. This study is the first to characterise similarities and differences during AM retrieval in children and adults using fMRI.     

Language comprehension vs. language production: age effects on fMRI activation

Normal language acquisition is a process that unfolds with amazing speed primarily in the first years of life. However, the refinement of linguistic proficiency is an ongoing process, extending well into childhood and adolescence. An increase in lateralization and a more focussed productive language network have been suggested to be the neural correlates of this process. However, the processes underlying the refinement of language comprehension are less clear. Using a language comprehension (Beep Stories) and a language production (Vowel Identification) task in fMRI, we studied language representation and lateralization in 36 children, adolescents, and young adults (age 6-24 years). For the language comprehension network, we found a more focal activation with age in the bilateral superior temporal gyri. No significant increase of lateralization with age could be observed, so the neural basis of language comprehension as assessed with the Beep Stories task seems to be established in a bilateral network by late childhood. For the productive network, however, we could confirm an increase with age both in focus and lateralization. Only in the language comprehension task did verbal IQ correlate with lateralization, with higher verbal IQ being associated with more right-hemispheric involvement. In some subjects (24%), language comprehension and language production were lateralized to opposite hemispheres.     

Sex differences in cerebral laterality of language and visuospatial processing

Sex differences on language and visuospatial tasks are of great interest, with differences in hemispheric laterality hypothesized to exist between males and females. Some functional imaging studies examining sex differences have shown that males are more left lateralized on language tasks and females are more right lateralized on visuospatial tasks; however, findings are inconsistent. Here we used functional magnetic resonance imaging to study thirty participants, matched on task performance, during phonological and visuospatial tasks. For each task, region-of-interest analyses were used to test differences in cerebral laterality. Results indicate that lateralization differences exist, with males more left lateralized during the phonological task and showing greater bilateral activity during the visuospatial task, whereas females showed greater bilateral activity during the phonological task and were more right lateralized during the visuospatial task. Our data provide clear evidence for differences in laterality between males and females when processing language versus visuospatial information.     

Probing emotion in the developing brain: functional neuroimaging in the assessment of the neural substrates of emotion in normal and disordered children and adolescents

Virtually all developmental neuropsychiatric disorders involve some dysfunction or dysregulation of emotion. Moreover, many psychiatric disorders with adult onset have early subclinical manifestations in children. This essay selectively reviews the literature on the neuroimaging of affect and disorders of affect in children. Some critical definitional and conceptual issues are first addressed, including the distinctions between the perception and production of emotion and between emotional states and traits. Developmental changes in morphometric measures of brain structure are then discussed and the implications of such findings for studies of functional brain activity are considered. Data on functional neuroimaging and childhood depression are then reviewed. While the extant data in this area are meager, they are consistent with studies in adults that have observed decreased left-sided anterolateral prefrontal cortex activation in depression. Studies in children on the recognition of emotion and affective intent in faces using functional magnetic resonance imaging are then reviewed. These findings indicate that the amygdala plays an important role in such affective face processing in children, similar to the patterns of activation observed in adults. Moreover, one study has reported abnormalities in amygdala activation during a task requiring the judgment of affective intent from the eye region of the face in subjects with autism. Some of the methodological complexities of developmental research in this area are discussed, and directions for future research are suggested.     

Development of neural systems for processing social exclusion from childhood to adolescence

Adolescence is a period of development in which peer relationships become especially important. A computer-based game (Cyberball) has been used to explore the effects of social exclusion in adolescents and adults. The current functional magnetic resonance imaging (fMRI) study used Cyberball to extend prior work to the cross-sectional study of younger children and adolescents (7 to 17 years), identifying age-related changes in the neural correlates of social exclusion across the important transition from middle childhood into adolescence. Additionally, a control task illustrated the specificity of these age-related changes for social exclusion as distinct from expectancy violation more generally. During exclusion, activation in and functional connectivity between ventrolateral prefrontal cortex and ventral anterior cingulate cortex increased with age. These effects were specific to social exclusion and did not exist for expectancy violation. Our results illustrate developmental changes from middle childhood through adolescence in both affective and regulatory brain regions during social exclusion.     

Functional cerebral asymmetries and cognitive abilities in musicians, painters, and controls

The relative participation of left- and right-hemisphere functions in verbal and spatial processing with musical composers, instrumentalists, painters, and non-musicians from student and junior high school populations was investigated. Hemispheric lateralization was related to the outcome of tests measuring spatial orientation, spatial visualization, tactile-visual discrimination, and verbal fluency. The relationship between lateral dominance and cognitive variables was influenced by sex and musical talents and the ability to paint. Males, irrespective of talents, were lateralized stronger than females. These sex differences were due to nonmusicians, only. Male and female composers, instrumentalists, and painters did not differ in language lateralization. Female left-handers showed a marked tendency for reversed language lateralization; left-handed males did not.     

Development of sex differences in spatial memory.

Males typically perform better than females on tests of spatial abilities. However, Silverman and Eals (1992) found that females can surpass males on certain tasks, in particular recall of object location. This study investigated the age at which females begin having greater recall in object location. Recall was tested with object arrays (sets of line drawings of common objects) using samples of 80 adults (M age = 21 yr.) and 139 children at 3 age groups. Adult data replicated earlier findings, indicating significantly greater recall by women. The samples of children at different ages--4 yr. (n = 43), 10-11 yr. (n = 53), and 15-16 yr. (n = 43)--did not show significant sex differences in this type of recall. The findings suggest that females may surpass males in this spatial ability as adults, apparently due to gradual improvements in spatial memory through childhood and adolescence.     

Developing connections for affective regulation: age-related changes in emotional brain connectivity

The regulation of affective arousal is a critical aspect of children’s social and cognitive development. However, few studies have examined the brain mechanisms involved in the development of this aspect of “hot” executive functioning. This process has been conceptualized as involving prefrontal control of the amygdala. Here, using functional magnetic resonance imaging (fMRI), we investigated the brain mechanisms involved in the development of affective regulation in typically developing 5- to 11-year-olds and an adult comparison sample. Children and adults displayed differing patterns of increased anterior cingulate cortex and decreased amygdala activation during episodes in which emotion regulation was required. Specifically, amygdala activation increased in adults but decreased in children during recovery from a frustrating episode. In addition, we used effective connectivity analyses to investigate differential correlations between key emotional brain areas in response to the regulatory task demands. We found reliable increases in effective connectivity between the anterior cingulate cortex and the amygdala during periods of increased demand for emotion regulation. This effective connectivity increased with age.     

Co-occurring anxiety influences patterns of brain activity in depression

Brain activation associated with anhedonic depression and co-occurring anxious arousal and anxious apprehension was measured by fMRI during performance of an emotion word Stroop task. Consistent with EEG findings, depression was associated with rightward frontal lateralization in the dorsolateral prefrontal cortex (DLPFC), but only when anxious arousal was elevated and anxious apprehension was low. Activity in the right inferior frontal gyrus (IFG) was also reduced for depression under the same conditions. In contrast, depression was associated with more activity in the anterior cingulate cortex (dorsal ACC and rostral ACC) and the bilateral amygdala. Results imply that depression, particularly when accompanied by anxious arousal, may result in a failure to implement top-down processing by appropriate brain regions (left DLPFC, right IFG) due to increased activation in regions associated with responding to emotionally salient information (right DLPFC, amygdala).     

Analyses of feeding lateralization in the small-eared bushbaby (Otolemur garnettii): a comparison with the ring-tailed lemur (Lemur catta)

Feeding related lateralization was examined in a population of 23 small-eared bushbabies (Otolemur garnettii). The three measures used to determine lateralization were food reaching, holding, and manipulation. Sex and age differences were found, with adult females showing a strong right bias and adult males a left bias. Juvenile males were weakly lateralized and less consistent across measures than adult animals. The use of standard scores to assess lateralization allowed species comparisons to be made. The results of this study were compared with results from a previous study on lateralization in the ring-tailed lemur (Lemur catta). Species comparisons found sex differences to be a stronger factor in lateralization than species differences.     

Action observation network in childhood: a comparative fMRI study with adults

Very little is known about the action observation network and the mirror neuron system (AON/MNS) in children and its age‐related properties compared with those observed in adults. In the present fMRI study we explored the activation of areas belonging to the AON/MNS in children and adults during observation of complex hand‐grasping actions, as compared to observation of simple grasping acts executed with the left and the right hand, seen from a first person perspective. The results indicate that during the action observation tasks in children there was activation of a cortical network similar to that found in adults, including the premotor cortex, the posterior part of the inferior frontal gyrus and the posterior parietal lobe. However, the activation in children was more widespread and showed a higher inter‐subject variability compared with adults. Furthermore, the activated network seems more lateralized to the left hemisphere in adults and more bilateral in children, with a linear growth of lateralization index as a function of age. Finally, in children the activation in the anterior intraparietal cortex (AIP) of each hemisphere was higher during observation of the contralateral hand (hand identity effect) and during the observation of complex actions relative to simple grasping acts, confirming the role of AIP for action‐related hand identity previously described in adults. These results support the assumption that structure and size of action representations are sensitive to mechanisms of development and show physiological plasticity. These properties of the AON/MNS could constitute a powerful tool for spontaneous reorganization and recovery of motor deficits after brain injury in children and in adults, as well as for specific rehabilitation programmes.     

A Brain-Based Account of the Development of Rule Use in Childhood

ABSTRACT— The ability to follow explicit rules improves dramatically during the course of childhood, but relatively little is known about the changes in brain structure and function that underlie this behavioral improvement. Drawing from neuroscientific studies in human adults and other animals, as well as from an emerging literature in developmental cognitive neuroscience, we propose a brain-based account of the development of rule use in childhood. This account focuses on four types of rules represented in different parts of the prefrontal cortex: simple rules for reversing stimulus–reward associations, pairs of conditional stimulus–response rules (both univalent and bivalent), and higher-order stimulus–response rules for selecting among task sets. It is hypothesized that the pattern of developmental changes in rule use reflects the different rates of development of specific regions within the prefrontal cortex.     

Cognitive control moderates early childhood temperament in predicting social behavior in 7‐year‐old children: an ERP study

Behavioral inhibition (BI) is a temperament associated with heightened vigilance and fear of novelty in early childhood, and social reticence and increased risk for anxiety problems later in development. However, not all behaviorally inhibited children develop signs of anxiety. One mechanism that might contribute to the variability in developmental trajectories is the recruitment of cognitive‐control resources. The current study measured N2 activation, an ERP (event‐related potential) associated with cognitive control, and modeled source‐space activation (LORETA; Low Resolution Brain Electromagnetic Tomography) at 7 years of age while children performed a go/no‐go task. Activation was estimated for the entire cortex and then exported for four regions of interest: ventromedial prefrontal cortex (VMPFC), ventrolateral prefrontal cortex (VLPFC), dorsal anterior cingulate cortex (dorsal ACC), and dorsal lateral prefrontal cortex (DLPFC). BI was measured in early childhood (ages 2 and 3 years). Anxiety problems and social reticence were measured at 7 years of age to ascertain stability of temperamental style. Results revealed that BI was associated with increased performance accuracy, longer reaction times, greater (more negative) N2 activation, and higher estimated dorsal ACC and DLPFC activation. Furthermore, early BI was only associated with social reticence at age 7 at higher (more negative) levels of N2 activation or higher estimated dorsal ACC or DLPFC activation. Results are discussed in the context of overcontrolled behavior contributing to social reticence and signs of anxiety in middle childhood.     

Mapping numerical processing, reading, and executive functions in the developing brain: an fMRI meta-analysis of 52 studies including 842 children

Tracing the connections from brain functions to children's cognitive development and education is a major goal of modern neuroscience. We performed the first meta-analysis of functional magnetic resonance imaging (fMRI) data obtained over the past decade (1999-2008) on more than 800 children and adolescents in three core systems of cognitive development and school learning: numerical abilities, reading, and executive functions (i.e. cognitive control). We ran Activation Likelihood Estimation (ALE) meta-analyses to obtain regions of reliable activity across all the studies. The results indicate that, unlike results usually reported for adults, children primarily engage the frontal cortex when solving numerical tasks. With age, there may be a shift from reliance on the frontal cortex to reliance on the parietal cortex. In contrast, the frontal, temporo-parietal and occipito-temporal regions at work during reading in children are very similar to those reported in adults. The executive frontal regions are also consistent with the imaging literature on cognitive control in adults, but the developmental comparison between children and adolescents demonstrates a key role of the anterior insular cortex (AIC) with an additional right AIC involvement in adolescents.     

Developmental outcomes after early prefrontal cortex damage

The neuropsychological bases of cognitive, social, and moral development are minimally understood, with a seemingly wide chasm between developmental theories and brain maturation models. As one approach to bridging ideas in these areas, we review 10 cases of early prefrontal cortex damage from the clinical literature, highlighting overall clinical profiles and real life developmental outcomes. Based on these cases, there is preliminary evidence to support distinctive developmental differences after: (1) dorsolateral, (2) mesial, and (3) orbital-polar prefrontal lesions, for more profound impairments after bilateral damage, and possibly for recovery differences after very early vs. later childhood lesion onset. Further case and group studies are needed to confirm reliable effects of specific lesion locations, the influence of age of lesion onset, and related experiential and treatment variables in determining adult outcomes. Rather than a single underlying deficit associated with early prefrontal cortex damage, we interpret the findings to suggest that it is the altered integration and interplay of cognitive, emotional, self-regulatory, and executive/metacognitive deficits that contribute to diverse developmental frontal lobe syndromes. The findings support the fundamental importance of prefrontal cortex maturation in protracted cognitive, social-emotional, and moral development.     

Brain activity underlying negative self- and other-perception in adolescents: The role of attachment-derived self-representations

One of teenagers’ key developmental tasks is to engage in new and meaningful relationships with peers and adults outside the family context. Attachment-derived expectations about the self and others in terms of internal attachment working models have the potential to shape such social reorientation processes critically and thereby influence adolescents’ social-emotional development and social integration. Because the neural underpinnings of this developmental task remain largely unknown, we sought to investigate them by functional magnetic resonance imaging. We asked n = 44 adolescents (ages 12.01–18.84 years) to evaluate positive and negative adjectives regarding either themselves or a close other during an adapted version of the well-established self-other trait-evaluation task. As measures of attachment, we obtained scores reflecting participants’ positive versus negative attachment-derived self- and other-models by means of the Relationship Questionnaire. We controlled for possible confounding factors by also obtaining scores reflecting internalizing/externalizing problems, schizotypy, and borderline symptomatology. Our results revealed that participants with a more negative attachment-derived self-model showed increased brain activity during positive and negative adjective evaluation regarding the self, but decreased brain activity during negative adjective evaluation regarding a close other, in bilateral amygdala/parahippocampus, bilateral anterior temporal pole/anterior superior temporal gyrus, and left dorsolateral prefrontal cortex. These findings suggest that a low positivity of the self-concept characteristic for the attachment anxiety dimension may influence neural information processing, but in opposite directions when it comes to self- versus (close) other-representations. We discuss our results in the framework of attachment theory and regarding their implications especially for adolescent social-emotional development and social integration.     

Development of emotional facial recognition in late childhood and adolescence

The ability to interpret emotions in facial expressions is crucial for social functioning across the lifespan. Facial expression recognition develops rapidly during infancy and improves with age during the preschool years. However, the developmental trajectory from late childhood to adulthood is less clear. We tested older children, adolescents and adults on a two-alternative forced-choice discrimination task using morphed faces that varied in emotional content. Actors appeared to pose expressions that changed incrementally along three progressions: neutral-to-fear, neutral-to-anger, and fear-to-anger. Across all three morph types, adults displayed more sensitivity to subtle changes in emotional expression than children and adolescents. Fear morphs and fear-to-anger blends showed a linear developmental trajectory, whereas anger morphs showed a quadratic trend, increasing sharply from adolescents to adults. The results provide evidence for late developmental changes in emotional expression recognition with some specificity in the time course for distinct emotions.     

The right hemispheric dominance for face perception in preschool children depends on the visual discrimination level

The developmental origin of human adults’ right hemispheric dominance in response to face stimuli remains unclear, in particular because young infants’ right hemispheric advantage in face‐selective response is no longer present in preschool children, before written language acquisition. Here we used fast periodic visual stimulation (FPVS) with scalp electroencephalography (EEG) to test 52 preschool children (5.5 years old) at two different levels of face discrimination: discrimination of faces against objects, measuring face‐selectivity, or discrimination between individual faces. While the contrast between faces and nonface objects elicits strictly bilateral occipital responses in children, strengthening previous observations, discrimination of individual faces in the same children reveals a strong right hemispheric lateralization over the occipitotemporal cortex. Picture‐plane inversion of the face stimuli significantly decreases the individual discrimination response, although to a much smaller extent than in older children and adults tested with the same paradigm. However, there is only a nonsignificant trend for a decrease in right hemispheric lateralization with inversion. There is no relationship between the right hemispheric lateralization in individual face discrimination and preschool levels of readings abilities. The observed difference in the right hemispheric lateralization obtained in the same population of children with two different paradigms measuring neural responses to faces indicates that the level of visual discrimination is a key factor to consider when making inferences about the development of hemispheric lateralization of face perception in the human brain.