Catherine L. Sebastian1 1Univ. London, Royal Holloway, Reino Unido
Neuroimaging studies have shown continued structural and functional development in neural circuitryunderlying social and emotional behaviour during adolescence. This article explores adolescent neurocognitivedevelopment in two domains: sensitivity to social rejection and Theory of Mind (ToM).Adolescents often report hypersensitivity to social rejection. The studies presented here suggest thatthis is accompanied by reduced responses in brain regions involved in emotion regulation. Studies onsocial rejection in adolescents with autism spectrum conditions will also be discussed. ToM is anothersocial cognitive domain which undergoes neurocognitive development between adolescence and adulthood.ToM refers to the ability to understand others' thoughts and intentions. Neuroimaging data suggestthat the ability to integrate emotional information into ToM decisions continues to develop betweenadolescence and adulthood. In sum, these studies demonstrate ongoing development of social and emotionalcognition during adolescence at both behavioural and neural levels, providing a neurocognitiveframework for understanding adolescent behaviour.
Los estudios de neuroimagen han conocido un continuo desarrollo estructural y funcional de los circuitosneuronales que subyacen al comportamiento social y emocional en la adolescencia. Este artículo explorael desarrollo neurocognitivo adolescente en dos dominios: la sensibilidad al rechazo social y la teoríade la mente (TM). Los adolescentes refieren a menudo hipersensibilidad al rechazo social. Los estudiosque se presentan sugieren que se acompa˜na de una disminución de las respuestas en regiones cerebralesvinculadas a la regulación emocional. También se comentarán los estudios sobre rechazo social en adolescentescon trastornos del espectro autista. La teoría de la mente es otro campo cognitivo social quesubyace al desarrollo neurocognitivo entre adolescencia y edad adulta. Dicha teoría alude a la capacidadde comprender los pensamientos e intenciones de los demás. Los datos de neuroimagen sugieren que lacapacidad de integrar la información emocional en decisiones de teoría de la mente sigue desarrollándoseentre la adolescencia y la edad adulta. En síntesis, tales estudios demuestran que hay un desarrollocontinuo de la cognición social y emocional durante la adolescencia tanto en el nivel comportamentalcomo neuronal, proporcionando un marco neurocognitivo para explicar el comportamiento adolescente.
Human adolescence is a period of physical, psychological, and social transition between childhood and adulthood ( Spear, 2000 ). While it is difficult to define the precise onset and end point of adolescence, it has been described as ning with the onset of puberty and ending with a stable commitment to an adult role ( Damon, 2004 ). For the purposes of this article, adolescence will be broadly defined as the second decade of life. While there are undoubtedly cultural influences at play, adolescence is often characterised by an increase in emotional lability and risk-taking behaviours. Epidemiological data also suggest that adolescence is a key time for the onset of psychological disorders characterised by emotional dysregulation ( Kessler et al., 2005 ). These internalising disorders such as depression and anxiety, as well as externalising disorders such as conduct disorder.
It has been suggested that this vulnerability results from ongoing brain development occurring during adolescence, particularly in brain regions responsible for high level cognitive abilities such as planning, decision-making, and regulating emotions (e.g., Paus, Keshavan, & Giedd, 2008 ). In the last 15 years, the availability of safe and non-invasive neuroimaging methods such as magnetic resonance imaging (MRI) has revolutionised the study of adolescence. It is now known that significant development occurs in the brain's grey and white matter and that those brain regions which are latest to mature are those responsible for complex human behaviours, notably the prefrontal cortex and temporo-parietal regions ( Giedd et al., 1999; Gogtay et al., 2004; Shaw et al., 2008; Sowell et al., 1999 ). Different brain regions have also been shown to mature at different rates and with differing trajectories; for example, Shaw et al. (2008) found that evolutionarily older parts of the brain, such as the limbic system, mature in a simpler linear trajectory than regions that evolved more recently, such as the neocortex. Neurotransmitter systems also continue to develop; for example the dopaminergic system undergoes substantial remodelling during adolescence ( Steinberg, 2008).
Research is currently engaged in further linking specific adolescent behaviours with particular patterns of brain development. Several recent models of the link between adolescent brain and behaviour have proposed the idea of a ‚Äėdevelopmental mismatch‚Äô between parts of the brain involved in processing emotional and reward signals (including regions such as the amygdala and ventral striatum) and those responsible for regulating these responses (e.g., parts of the prefrontal cortex) ( Casey, Jones, & Hare, 2008; Nelson, Leibenluft, McClure, & Pine, 2005; Steinberg, 2008 ). During adolescence, it is hypothesised that the development of regulatory regions lags behind that of emotional processing regions, rendering the adolescent brain a ‚Äėfast car with poor brakes‚Äô. Although this formulation is undoubtedly oversimplified, it provides a useful framework and generates predictions that can be tested using methods such as al magnetic resonance imaging (fMRI).
In addition to emotional processing, regulation, and behaviour, it is also important to consider the role of social development in adolescence. Indeed, the social environment is crucial in shaping the adolescent brain ( Blakemore, 2008 ). The role of peers is vital, with evidence suggesting that by mid-adolescence, individuals spend more time with their peers than with their parents ( Steinberg & Silverberg, 1986 ). Also important is the increasing ability of adolescents to think abstractly about themselves and other people. This means they have a more sophisticated understanding of complex social phenomena such as reputation, social hierarchy, personality traits, and how others see them (the ‚Äėlooking glass self‚Äô) than they did at an earlier age ( Harter, 1990; Parker, Rubin, Erath, Wojslawowicz, & Buskirk, 2006; Sebastian, Burnett, & Blakemore, 2008 ).Social Rejection in Adolescence
Given this ongoing development in both affective (emotional) and social domains, several researchers have investigated whether ‚Äėdevelopmental mismatch‚Äô, resulting in poor emotion regulation, could interact with social cognitive development to account for social behaviours commonly seen in adolescence. One phenomenon that captures the overlap between social and emotional processes particularly well is sensitivity to social rejection in adolescence. Social rejection, or ostracism, refers to being deliberately ignored or excluded by an individual or a group ( Williams, 2007 ). In adolescence, social rejection is often used as a form of relational aggression or bullying, with one study ( Wang, Iannotti, & Nansel, 2009 ), reporting that 27.4% adolescent girls had been excluded or ignored by peers at school. Boys may also use relational aggression but girls are more likely to do so, and to be upset when they are the victim ( Crick & Nelson, 2002; Wang et al., 2009 ). Self-report studies have suggested that adolescents might be more sensitive to social rejection than both adults and younger children in everyday life ( Kloep, 1999; O‚ÄôBrien & Bierman, 1988 ). However, the social, cognitive, and neural processes underlying this effect have only recently been investigated experimentally.
As a starting point, it is important to establish whether adolescent sensitivity to social rejection can be replicated in the laboratory. If so, this would suggest that the phenomenon is not just an artefact of the adolescent social environment (e.g., social hierarchies at school). In recent years, the ‚ÄėCyberball‚Äô paradigm ( Williams, Cheung, & Choi, 2000 ) has been used extensively to experimentally investigate responses to social rejection in a wide range of populations. Cyberball is a computer game in which participants are told that they are playing a game of ‚Äėcatch‚Äô over the internet with two other players, and that the researchers are interested in ‚Äėmental visualisation ability‚Äô during the game. In fact, the actions of the other players are pre-programmed by the experimenter to either or exclude the participant in a systematic way. Reactions to this manipulation can then be measured (see Williams, 2007, for a review).
Cyberball was used to test adolescent responses to social rejection (focusing on females only) in a study by Sebastian, Viding, Williams, and Blakemore (2010) . Twenty-six early adolescents (aged 11-13), 25 mid adolescents (aged 14-15), and 26 adult female controls were first d and then rejected in successive rounds of Cyberball. Self-reported mood and anxiety levels were measured at baseline (i.e., before playing Cyberball), after inclusion, and finally after rejection. (Condition order was not randomised in order to avoid possible negative spillover effects from the rejection to the inclusion condition). Relative to adult females, both adolescent groups reported lower overall mood following rejection. The early adolescents also reported greater anxiety. The mid-adolescents did report high anxiety following rejection, but anxiety was also high following inclusion (relative to baseline). One possible conclusion from this finding is that social interaction in general can be anxiety-provoking at this age. Indeed, the mean age of onset for social phobia occurs in mid-adolescence at age 15 ( Mancini, Van Ameringen, Bennett, Patterson, & Watson, 2005 ). In contrast, all groups reported that they had been excluded by the other players to a similar degree and reported the experience as feeling equally real. This suggests that adolescents (at least adolescent girls) respond more strongly and negatively to social rejection than do adults, even when there are no objective differences in the perception of the rejection episode.Social Rejection and the Adolescent Brain
The behavioural study reported above suggests that sensitivity to rejection in adolescence can be elicited under experimental conditions, even when the rejection encounter is very brief and has no long term consequences for social reputation. It is therefore interesting to consider what factors might underlie this effect. One hypothesis is that ongoing brain development in regions responsible for processing and regulating responses to social rejection may contribute. Eisenberger, Lieberman, and Williams (2003) used the Cyberball paradigm together with fMRI in adults and found that activity in right ventrolateral prefrontal cortex (VLPFC) during social rejection (relative to inclusion) was negatively related to self-reported distress, i.e., a greater response in this region was associated with reduced rejection-related distress. One possibility is that this region is involved in regulating negative emotions such as responses to social rejection, and that this region s differently in adolescents compared with adults.
This hypothesis was investigated in an fMRI study comparing neural responses during Cyberball in 19 adolescent females (aged 14-16) and 16 matched adults ( Sebastian et al., 2011 ). Regardless of age, all participants activated a network of regions involved in social evaluation and negative emotion. These d the medial prefrontal cortex, ventral anterior cingulate cortex, and medial orbitofrontal cortex. However, of most interest was a group difference in right ventrolateral prefrontal cortex. The adult group showed a greater response in this region during rejection compared with inclusion, while the adolescent group showed no difference between rejection and inclusion conditions. It may be that this lack of a difference between conditions reflects a reduced ability to flexibly engage right VLPFC in emotion regulation as needed (in this case, during social rejection).
In support of this interpretation, adolescents reported greater rejection-related distress than did adults (as in the behavioural study above), although it is worth noting that no inverse correlation was found between distress and right VLPFC response in either adolescents or adults. Such a result would have provided stronger evidence that right VLPFC response was ally involved in regulating rejection-related distress. However, another study ( Masten et al., 2009 ) used Cyberball and fMRI with 23 adolescents (both males and females) and did find a negative correlation between distress and right VLPFC activation. The replication of this effect across two studies ( Eisenberger et al., 2003; Masten et al., 2009 ) lends weight to the theory that this region is involved in regulating distress and that its lack of engagement in Sebastian et al. (2011) reflects reduced regulation of rejection-related distress in adolescents relative to adults.
Results from the above studies indicate that adolescents respond to explicit social rejection differently from adults at both the behavioural and the neural levels. Although participants are not aware that the experimental aim is to measure responses to social rejection during Cyberball, they are at least explicitly aware that they are engaged in a social interaction, and that at some points they are d and at others excluded. However, an important aspect of emotion regulation relates to how we respond to implicit emotional cues, and in particular how well executive s such as cognitive control, response inhibition, attention, working memory, conflict monitoring and decision-making can be maintained in the presence of implicit emotional information ( Tottenham, Hare, & Casey, 2011 ).
To investigate this in relation to rejection in adolescence, adolescent and adult participants were scanned while completing a rejection-related emotional Stroop task ( Sebastian, Roiser et al., 2010 ). Individual words were displayed on the computer screen and participants indicated the ink colour in which the word was written (red, blue, green, yellow). Word meanings were either rejection-related (e.g., ‚Äėloser‚Äô), acceptance-related (‚Äėfriend‚Äô), or neutral (e.g., ‚Äėtable‚Äô). Participants were instructed to concentrate on the task (indicating the word colour) rather than word meaning; however, an extensive literature on the emotional Stroop task shows that emotional word meanings interfere with participants ability to perform the task, resulting in both increased reaction times to emotional (and particularly negatively-valenced) words ( Williams, Mathews, & MacLeod, 1996 ) and increased neural responses in regions involved in cognitive control ( Bush, Luu, & Posner, 2000 ). Interestingly, a comparison of fMRI responses during the emotional Stroop task between adolescent and adult responses revealed a group difference in the same right VLPFC region identified in the study using Cyberball. The pattern of results was also similar: adults showed an increased response in this region when processing rejection-related words compared with neutral words, but adolescents showed no difference between the two conditions.
Overall, results across two tasks (one explicit, one implicit) suggest that ventrolateral prefrontal cortex may not regulate emotional responses associated with social rejection as effectively in adolescents as in adults. It is possible that reduced response in this region may contribute to adolescent sensitivity to social rejection seen in everyday life. However, the exact mechanism underlying this reduced response is still unclear. For example, does this finding relate to the idea of a developmental mismatch, with an immature ventrolateral prefrontal cortex unable to regulate the activity of the limbic system effectively? We know that a network of brain regions is involved in the generation and regulation of rejection-related distress: how do these regions connect with each other and interact and how does this network develop during adolescence? It is also important to consider the role of experience: perhaps group differences at the neural level reflect adults‚Äô greater experience in dealing with rejection over time. While there are unanswered questions, the data suggests that focusing on emotion regulation skills, particularly those that engage ventrolateral prefrontal cortex, may be particularly beneficial during adolescence.Social Rejection in Adolescents with Autism Spectrum Conditions
Autism spectrum conditions (ASC) refer to conditions characterised by a triad of impairments comprising language difficulties or delay, communication problems, and stereotyped behaviours. While high-ing individuals with ASC have cognitive abilities in the normal range, their difficulties with social interaction may leave them particularly vulnerable to experiencing social rejection, particularly during adolescence when their peers‚Äô social skills may accelerate ahead. There is evidence that adolescents with autism spectrum conditions (ASC) believe they are less popular than their typically developing peers, while recognising the importance of peer approval ( Williamson, Craig, & Slinger, 2008 ). Individuals with ASC also report a desire for friendship ( Frith, 2004 ), while often experiencing loneliness ( Bauminger & Kasari, 2000) and bullying ( Van Roekel, Scholte, & Didden, 2010 ). It is therefore of interest to explore how individuals with ASC experience social rejection.
We conducted a behavioural study, using Cyberball to investigate self-reported responses to rejection in 13 adolescents with ASC (mean age 16.9) and 13 matched controls ( Sebastian, Blakemore, & Charman, 2009 ). Overall, the two groups reported very similar levels of distress. According to Williams‚Äô (1997) Need Threat model, social rejection threatens four fundamental social needs: self-esteem, belonging, control, and a sense of meaningful existence. These needs can be threatened automatically; for example, Zadro, Williams, and Richardson (2004) showed that rejection causes distress even when participants know that the Cyberball game is controlled by a computer. Adolescents with ASC reported similar or greater levels of need threat across all four needs compared with controls. Anxiety levels were also similar between the two groups. The only difference between groups was seen for self-reported mood: after rejection, the control group showed significantly lowered mood compared with baseline and inclusion conditions, while the group with ASC showed no reduction in mood.
This result was followed up by three studies using neuroimaging methods (fMRI or EEG) to better understand the response to rejection in ASC ( Bolling et al., 2011; Masten et al., 2011; McPartland et al., 2011 ). These studies all found that self-reported (questionnaire) responses to rejection were largely preserved in ASC, as discussed above. However, neural responses to rejection were reduced in individuals with ASC compared with controls (see Sebastian et al., 2011 for a detailed discussion of these studies). This is interesting, as it suggests that it is erroneous to think of responses to rejection in ASC as being either fully preserved or deficient. Adolescents with ASC clearly subjectively perceive social rejection as distressing, despite differences in processing at the neural level. Since individuals with ASC are particularly likely to experience bullying and social rejection, it makes sense to focus on bullying prevention in this group as well as on helping these individuals to develop effective coping strategies.The Adolescent Brain and Theory of Mind
The studies discussed so far have used social rejection as a tool for investigating the development of social and emotional processing in adolescence. Another aspect of social cognition that has received considerable attention with regard to adolescence in recent years is Theory of Mind (ToM: understanding others‚Äô thoughts, beliefs, and intentions). Indeed, while until recently ToM was thought to develop around age 4, evidence now suggests that ToM improves into late adolescence. For example, a behavioural study by Dumontheil, Apperly, and Blakemore (2009) found improvements in the ability to take another person's perspective between late adolescence (14-17 years) and adulthood (see Dumontheil, this volume, for further details).
Neuroimaging evidence is now showing that improvements in social cognition during adolescence are underpinned by ongoing development in relevant brain regions. For example, four recent al magnetic resonance imaging (fMRI) studies using a range of social cognition tasks have shown a reduction in brain activity between adolescence and adulthood in medial prefrontal cortex (see review by Blakemore, 2008 ). This region is activated across a range of social cognition tasks, particularly those requiring ToM. Putative s of this region meta-representation ( Amodio & Frith, 2006; Frith & Frith, 2007 ) or the decoupling of mental states from reality ( Gallagher & Frith, 2003 ), processes that are both necessary for ToM computations such as false belief reasoning, which s understanding that others‚Äô mental states may differ from reality. At present it is unclear what processes underlie the reduction in mPFC response between adolescence and adulthood. It may be that ongoing anatomical development during adolescence contributes to changes in al activation between adolescence and adulthood. Another possibility is that reduced activation relates to increasing efficiency in cognitive strategies used between adolescence and adulthood. These potential explanations are not mutually exclusive, and there may well be a combination of factors contributing to the pattern of results seen. In sum, the findings are suggestive of ongoing development in the neural underpinnings of ToM in adolescence.
While the traditional definition of ToM involves understanding thoughts, beliefs, and intentions, some researchers have suggested that understanding feelings should also be d (e.g., Shamay-Tsoory, Tomer, Berger, Goldsher, & Aharon-Peretz, 2005 ). One recent model ( Shamay-Tsoory, Harari, Aharon-Peretz, & Levkovitz, 2010 ) distinguishes cognitive and affective subprocesses of ToM. Cognitive ToM encompasses ‚Äėclassic‚Äô ToM, defined above, while affective ToM refers to the ability to infer what a person is feeling. According to this model, affective ToM s the integration of cognitive ToM and empathy (i.e., the ability to share and understand the emotional states of others; Singer, Critchley, & Preuschoff, 2009 ). As such, it is a more complex cognitive process than cognitive ToM. There is some evidence for this idea. For example, while children can pass complex cognitive ToM tasks (e.g., understanding what person A understands about what person B thinks) from the age of 6 or 7 years ( Perner & Wimmer, 1985 ), the ability to represent what person A understands about what person B feels (e.g., understanding of social faux pas) develops later, between the ages of 9 and 11 years (Baron-Cohen, O‚ÄôRiordan, Stone, Jones, & Plaisted, 1999).
There is evidence that the ventral portion of medial prefrontal cortex (VMPFC) may be crucial for affective ToM. Lesion studies have shown that VMPFC lesion patients are impaired on tasks of affective ToM (such as understanding the true emotional state behind an ironic remark), but remain unimpaired on cognitive ToM tasks ( Shamay-Tsoory & Aharon-Peretz, 2007; Shamay-Tsoory et al., 2005; Shamay-Tsoory, Tibi-Elhanany, & Aharon-Peretz, 2006 ). The VMPFC is anatomically well-connected for affective ToM processing, since it receives inputs from both medial PFC (involved in cognitive ToM) and regions involved in emotional and empathy processing, including amygdala, temporal pole, and anterior insula ( Shamay-Tsoory et al., 2006 ). Given behavioural evidence of relatively late development of affective ToM and anatomical evidence of the involvement of VMPFC in this process, we investigated whether there might be development between adolescence and adulthood in the involvement of VMPFC in affective ToM ( Sebastian et al., 2012).
We developed a cartoon vignette task based on a previous similar study in adults ( V√∂llm et al., 2006 ). As a non-verbal task, it had the advantage that results would not be confounded by differing linguistic abilities between adolescent and adult groups. Participants viewed 30 cartoons, with 10 cartoons in each of three conditions (affective ToM, cognitive ToM, physical causality). Each cartoon consisted of three frames which told a story. Stories were matched for social content, with each one portraying two characters. The final frame showed two possible endings, and the participant was asked to the most appropriate ending. In the affective ToM condition, ing the appropriate ending depended on the participant's ability to infer the emotional states of the two characters (e.g., would a mother comfort a child upset by a thunder storm, or laugh at them?). The cognitive ToM condition d inferences based on thoughts and beliefs (e.g., where would the characters place a ladder to reach apples in a tall tree?), while the physical causality condition acted as a control condition requiring basic cause and effect reasoning (e.g., does sunshine melt snow?). Participants were scanned using fMRI while completing the task, and d 15 adolescent males aged 10-16, and 15 IQ-matched male adult controls over the age of 24.
Across all participants, both cognitive ToM and affective ToM conditions (relative to the physical causality control condition) activated a core network of regions known to be involved in ToM processing, including superior temporal sulcus at the temporo-parietal junction (STS/TPJ), temporal pole, and precuneus. However, only affective ToM activated the medial PFC, with activation extending ventrally into VMPFC. Comparing adolescents with adults on the affective ToM>physical causality contrast, a region of VMPFC showed significantly greater activation to affective ToM than physical causality in the adolescent group, but no difference between conditions in the adults.
This finding mirrors evidence of increased activation in mPFC in adolescents compared with adults during cognitive ToM ( Blakemore, 2008 ). The region of VMPFC showing a group difference also overlapped with the region implicated in lesion studies as being crucial for affective ToM ( Shamay-Tsoory & Aharon-Peretz, 2007; Shamay-Tsoory et al., 2005; Shamay-Tsoory et al., 2006 ). Since no group differences were found for the cognitive ToM>physical causality contrast, it may be that development of the neural basis of affective ToM may be particularly protracted even relative to cognitive ToM. This would fit with both behavioural evidence of protracted affective ToM development (e.g., Baron-Cohen, O‚ÄôRiordan, Stone, Jones, & Plaisted, 1999 ), as well as with the model of affective ToM processing by Shamay-Tsoory et al. (2010) which posits that affective ToM is a more complex process than cognitive ToM, requiring integration between cognitive ToM and empathy processing.
Overall, our findings suggest that affective and cognitive ToM are associated with significant areas of overlap in terms of their neural representations, as well as areas of distinct and specialised processing such as VMPFC for affective ToM. The study also provides further evidence of al development within the ‚Äėsocial brain‚Äô between adolescence and adulthood ( Blakemore, 2008 ), with a greater BOLD response in adolescents than adults in a subregion of VMPFC during affective ToM relative to the physical causality control condition. Thus, it appears that the neural basis of the ability to integrate affective information into ToM-based decisions continues to develop between adolescence and adulthood. However, as with previous studies on cognitive ToM, further work is d to determine what this reduction in VMPFC activity with age means in computational terms.Conclusions: Social Rejection and Affective ToM
This review has focused on recent studies of adolescent development of the ‚Äėsocial brain‚Äô, i.e., the neural bases of social cognition. More specifically, however, the research discussed has focused on processes requiring the integration of emotion and social cognition. During social rejection, an emotional response is evoked by a social cause: without an understanding of the social situation, social rejection would not elicit such a strong emotional response. Similarly, during affective ToM, we need to be able to understand the social relationships between individuals to make sense of their emotional state. Adolescence is a time of increasing social sophistication, with adolescents expanding their social sphere into an extended peer group ( Steinberg & Silverberg, 1986 ), and understanding increasingly more about how they fit in and are seen by others ( Harter, 1990; Parker et al., 2006 ). At the same time, adolescents must process and regulate the emotional responses elicited by social situations. The studies presented here suggest that although adolescents are capable of sophisticated social and emotional reasoning, the neural substrates underlying these skills continue to develop between even late adolescence and adulthood. Future research should focus on the precise mechanisms of this development, as well as on how individual differences in the neural processing of social and emotional cues relates to outcomes in terms of adolescent behaviour and wellbeing.Resumen ampliado
Numerosos estudios realizados con neuroimagen est√°n demostrando que durante la adolescencia se da un desarrollo estructural y funcional continuado en los circuitos neurales que subyacen al comportamiento emocional y social. En este art√≠culo exploraremos el desarrollo neurocognitivo del adolescente en dos aspectos: la sensibilidad al rechazo social y la teor√≠a de la mente (TM). Los adolescentes se quejan frecuentemente de hipersensibilidad al rechazo social en la vida cotidiana. Los estudios presentados aqu√≠ tienen como objetivo explorar la posibilidad de que este fen√≥meno venga acompa√Īado de un descenso en la activaci√≥n de determinadas regiones del cerebro implicadas en la regulaci√≥n emocional. A este respecto, tambi√©n se discuten algunos estudios que han explorado las respuestas de adolescentes con trastornos del espectro autista. La TM es otro aspecto de la cognici√≥n social que sufre un desarrollo neurocognitivo entre la adolescencia y la adultez. Se refiere a la capacidad de comprender los pensamientos y las intenciones de los otros. En este trabajo mostrar√© datos de neuroimagen que sugieren que la capacidad de integrar la informaci√≥n emocional en las decisiones sobre la TM (afectiva) sigue desarroll√°ndose entre la adolescencia y la adultez.
En este art√≠culo definiremos la adolescencia, de manera general, como el per√≠odo correspondiente a la segunda d√©cada de la vida. Mientras es cierto que existen influencias culturales importantes, el adolescente se caracteriza a menudo por presentar un aumento de la labilidad emocional y de comportamientos de alto riesgo. Los datos epidemiol√≥gicos tambi√©n sugieren que la adolescencia es un per√≠odo clave para el inicio de trastornos caracterizados por una desregulaci√≥n emocional. Se ha sugerido que esta vulnerabilidad es consecuencia de un desarrollo cerebral a√ļn en curso durante la adolescencia, particularmente en regiones cerebrales responsables de habilidades cognitivas superiores tales como la planificaci√≥n, la toma de decisiones y la regulaci√≥n de las emociones. Se supone que durante la adolescencia la maduraci√≥n y desarrollo de las regiones regulatorias va con retraso respecto a las regiones de procesamiento emocional, dando lugar a una situaci√≥n que podr√≠amos definir gr√°ficamente como que el cerebro adolescente es ‚Äėun coche veloz con malos frenos‚Äô. Aunque esta es sin duda una descripci√≥n excesivamente simplista, proporciona no obstante una marco te√≥rico y de trabajo √ļtil, capaz de generar predicciones contras utilizando m√©todos como la resonancia magn√©tica funcional (fMRI).
Un fen√≥meno que es capaz de captar particularmente bien las relaciones e interacciones entre los procesos sociales y los emocionales es la sensibilidad al rechazo social en los adolescentes. Los adolescentes parecen ser m√°s sensibles a este rechazo que las personas de mayor o menor edad. Para explorar este fen√≥meno, se suele emplear el paradigma ‚ÄėCyberball‚Äô, un juego de interacci√≥n virtual con otros dos jugadores en el que las acciones de los otros dos hipot√©ticos jugadores se programan de antemano tanto para incluir como para excluir del juego al sujeto de estudio, de una manera sistem√°tica. Se pueden medir las reacciones a esta manipulaci√≥n.
Cuando el paradigma Cyberball se ha empleado en entornos fMRI en adolescentes y adultos, se comprueba que, independientemente de la edad, todos los participantes activan una red de regiones cerebrales implicada en la evaluaci√≥n social y las emociones negativas. Entre dichas √°reas se encuentra el c√≥rtex medial prefrontal, el c√≥rtex cingulado anterior ventral y la corteza orbitofrontal medial. Sin embargo, el resultado m√°s interesante es la diferente activaci√≥n entre grupos del c√≥rtex ventrolateral prefrontal (VLPFC por sus siglas en ingl√©s). Los adultos muestran una mayor activaci√≥n en el VLPFC derecho durante el rechazo en comparaci√≥n con la inclusi√≥n, mientras los adolescentes no muestran diferencias de activaci√≥n en dicha zona al comparar la situaci√≥n de rechazo con la de inclusi√≥n. Posiblemente, esta falta de diferente activaci√≥n refleja una escasa capacidad por parte de los adolescentes para utilizar flexiblemente el VLPFC derecho en la regulaci√≥n emocional en funci√≥n de las necesidades situacionales. Se sabe que el VLPFC derecho est√° implicado en la regulaci√≥n de los efectos emocionales negativos de una situaci√≥n de rechazo social. Los datos apoyar√≠an por tanto que una estrategia particularmente beneficiosa para los adolescentes ser√≠a centrarse en las habilidades de regulaci√≥n de la emoci√≥n, particularmente aquellas que implican al VLPFC.
Con respecto a la teor√≠a de la mente (TM), mientras hasta hace poco se pensaba que se desarrollaba en torno a los 4 a√Īos de edad, las evidencias m√°s recientes demuestran por el contrario que la TM contin√ļa desarroll√°ndose y mejorando hasta las √ļltimas etapas de la adolescencia. Estas mejoras en la TM durante la adolescencia tendr√≠an su fundamento en el desarrollo continuado de √°reas relevantes del cerebro. Normalmente se distingue entre subprocesos cognitivos y afectivos en la TM. La TM cognitiva incluye la ‚Äėcl√°sica‚Äô TM, es decir, la comprensi√≥n de los pensamientos, creencias e intenciones de los otros. Por su parte, la TM afectiva se refiere a la habilidad para inferir lo que siente una persona. Mientras los ni√Īos de 6 o 7 a√Īos ya son capaces de superar pruebas complejas de TM cognitiva (p. ej., comprender lo que la persona A entiende acerca de lo que piensa la persona B), la capacidad para representarse lo que la persona A entiende acerca de lo que la persona B siente (p. ej., comprender las consecuencias de violar las normas sociales) se desarrolla m√°s tarde, entre los 9 y los 11 a√Īos de edad. Hay evidencia de que la porci√≥n ventral del c√≥rtex prefrontal medial (VMPFC por sus siglas en ingl√©s) puede ser crucial para la TM afectiva. As√≠, en experimentos con fMRI se puede apreciar c√≥mo tanto la TM cognitiva como la afectiva activan una serie de regiones cerebrales implicadas en la TM, incluyendo el surco temporal superior en la uni√≥n temporo-parietal, el polo temporal y el prec√ļneo, solo la TM afectiva implica al VMPFC. De los diferentes estudios realizados se deduce la posibilidad de que la maduraci√≥n de estas regiones del VMPFC est√© particularmente retrasada, especialmente en relaci√≥n al resto de regiones implicadas en la TM (especialmente en la TM cognitiva), no habi√©ndose producido su maduraci√≥n a√ļn durante la adolescencia. En l√≠nea con estos hallazgos, parece que la TM afectiva es en s√≠ un proceso mucho m√°s complejo que la TM cognitiva, pues requiere de la integraci√≥n entre la TM cognitiva y los procesos de empat√≠a. Curiosamente, esta regi√≥n VMPFC se muestra mucho m√°s activa en adolescentes que en adultos en tareas de TM afectiva, lo que sugiere que su menor activaci√≥n con la edad se relaciona con una mayor eficacia en su funci√≥n.
En definitiva, la adolescencia es un periodo en el que el cerebro social contin√ļa madurando, aumentando y mejorando su sofisticaci√≥n y eficacia. La adolescencia es un per√≠odo en el cual la esfera social se hace m√°s compleja, a la par que aumenta el tama√Īo del grupo social de referencia cercana (de miembros de la misma edad) y cada vez se comprende mejor c√≥mo encaja uno en un grupo y c√≥mo es visto por los otros. Los adolescentes deben aprender a ser capaces de procesar y regular las respuestas emocionales provocadas por las distintas situaciones sociales. Comprender el cerebro adolescente nos permite entender mejor su mente y su comportamiento y, por lo tanto, adaptar los programas educativos a las peculiaridades de esta etapa vital.Conflict of Interest
The author of this article declares no conflict of interest.
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