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Social cognitive development during adolescence
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Suparna Choudhury, Sarah-Jayne Blakemore, and Tony Charman
Social relationships are particularly important during adolescence. In recent years, histological and MRI studies have shown that the brain is subject to considerable structural development during adolescence. Brain regions that are implicated in social cognition, including parts of prefrontal, parietal and superior temporal cortex, undergo the most pronounced and prolonged change. However, the development of social cognition during adolescence and its neural underpinnings remains poorly understood. Here, we begin by outlining how the brain changes between childhood and adulthood. We then describe findings that have emerged from behavioural and neuroimaging studies of the recognition of facial expression during adolescence. Finally, we present new data that demonstrate development of emotional perspective taking during adolescence. In this study, 112 participants, aged 8–36 years, performed a computerised task that involved taking an emotional perspective either from the participant's own point of view or from that of another person. The results showed that average difference in reaction time (RT) to answer questions in the first person perspective (1PP) and third person perspective (3PP) significantly decreased with age. The RT difference of adults tended to cluster close to the zero line (3PP = 1PP), while a greater proportion of pre-adolescents had higher difference values in both the positive (3PP > 1PP) and negative direction (1PP > 3PP) of the scale. The data suggest that the efficiency, and possibly strategy, of perspective taking develop in parallel with brain maturation and psychosocial development during adolescence.
Keywords: perspective taking, brain development, adolescence, social cognition, prefrontal cortex, parietal cortex
Adolescence is the transitional period between late childhood and the beginning of adulthood, and marks the beginning of the reproductive lifespan in humans. Adolescence involves sexual maturity in terms of hormones and physical development of the body, and is also characterised by an increase in the complexity of group interactions and thus social behaviour (Lerner and Steinberg, 2004). Adolescence is a period of development and consolidation of the social self, of one's identity and understanding of the self in relation to the social world (Coleman and Hendry, 1990). Anecdotal evidence and self-report data suggest that children seem to become progressively self-conscious and concerned with other people's opinions as they go through puberty and the period of adolescence (Steinberg, 2005). The psychosocial context of adolescents is markedly different to that of children and adults. Relationships with peers, family and society go through distinct changes during this time. Adolescents begin to assert more autonomous control over their decisions, emotions and actions, and start to disengage from parental control. At the same time, the school context involves an intense socialisation process during which adolescents become increasingly aware of the perspectives of classmates, teachers and other societal influences (Berzonsky and Adams, 2003).
Recent evidence has shown that the brain goes through a remodelling process during adolescence. It is possible that neural plasticity facilitates the development of social cognitive skills required during the period of adolescence. In the following section, we describe evidence for neural development during adolescence.
Recent structural MRI studies have demonstrated that the brain undergoes considerable development during adolescence. Both cross-sectional and longitudinal data demonstrate that changes in the frontal and parietal regions are especially pronounced and prolonged (Giedd et al., 1999; Sowell et al., 2003; Gogtay et al., 2004; Toga et al., 2006). Grey matter (GM) development in these areas is non-linear, in contrast to its linear development in the occipital lobes. The volume of GM in the frontal lobes increases during childhood with a peak occurring at around 12 years for males and 11 years for females, roughly coinciding with the age of puberty onset. This is followed by a decline in GM volume during adolescence (Giedd et al., 1999; Sowell et al., 2003; Gogtay et al., 2004; Toga et al., 2006). Similarly, parietal lobe GM volume increases during the pre-adolescent stage to a peak at around 12 years for males and 10 years for females, and is followed by a decline during adolescence (Giedd et al., 1999; Gogtay et al., 2004). While frontal and parietal cortex development is relatively rapid during adolescence, GM in the superior temporal cortex, including superior temporal sulcus (STS), reaches a peak at around 16 years and then follows a steady decline, not reaching maturity until relatively late (Toga et al., 2006). At the same time, there is an increase in prefrontal cortex (PFC) and parietal cortex white matter (WM) density from puberty onset, throughout adolescence and into adulthood (Giedd et al., 1996; 1999; Reiss et al., 1996; Sowell et al., 2001; Barnea-Goraly et al., 2005; for more detailed reviews of structural development in the brain, see Paus, 2005; Blakemore and Choudhury, 2006; Toga et al., 2006).
Earlier post-mortem investigations of human brain development revealed that two main cellular processes occur in the frontal cortex during adolescence: synaptogenesis followed by synaptic pruning (Huttenlocher, 1979; Huttenlocher et al., 1983); and axonal myelination (Yakovlev and Lecours, 1967). Myelinated axons appear white in MR images, whereas non-myelinated matter appears grey. Thus, the increase in WM seen in certain brain areas in MRI images during childhood and adolescence is thought to reflect the increase in myelination in those areas. The decrease in GM during adolescence might simply be a consequence of the increase in WM (since there is no increase in total brain volume). However, the non-linearity of GM development suggests it does not simply reflect the consequences of increased WM. Instead, it has been suggested that the pattern of GM development reflects, at least in part, the synaptic reorganisation that takes place during that period (Paus, 2005). The combined effect of these maturational processes might be to fine-tune neural circuitry in the PFC and other cortical regions, and thus increase efficiency of the cognitive systems they subserve (see Blakemore and Choudhury, 2006 for review).
Structural development of these cortical regions may influence cognitive functioning during adolescence. A combination of behavioural and fMRI studies have demonstrated development of executive functions, that is, cognitive skills that enable the control and coordination of thoughts and behaviour, which are generally associated with the PFC (Luria, 1966; Shallice, 1982). Behavioural studies of performance on tasks including inhibitory control (Leon-Carrion et al. 2004; Luna et al. 2004a), processing speed (Luna et al. 2004a), prospective memory (MacKinlay et al., 2003), working memory (Anderson et al., 2001), decision-making (McGivern et al., 2002; Hooper et al. 2004; Luciana et al. 2005) and risk-taking (Gardner and Steinberg, 2005) continue to develop during adolescence. fMRI studies have shown that performance changes in executive function tasks are related to PFC development (Casey et al., 1997; Gaillard et al., 2000; Luna et al., 2001; Tamm et al., 2002; Bjork et al., 2004; Brown et al., 2005).
A recent longitudinal MRI study of participants aged between 3 and 29 years revealed that the trajectory of change in cortical thickness is associated with the development of IQ (Shaw et al., 2006). The relationship between cortical thickness and IQ, as indexed by Wechsler intelligence scales, was found to vary with age. Stratification of participants into three IQ bands (average, high and superior IQ) indicated that the maximum trajectory differences between groups were in superior frontal gyrus bilaterally extending into the medial PFC. The developmental shift in trajectory was most pronounced for the most intelligent children and adolescents: the children with the highest IQ had a thinner cortex in early childhood but cortical thickness then increased, peaking at around age 11, and then underwent the most dramatic cortical thinning thereafter. Shaw and colleagues proposed that intelligence levels relate to how the cortex changes during development.
While several studies have investigated the development of executive function in adolescence, as yet, few have looked at the development of social cognition during this period. In the next section, we describe studies that have focussed on the development of socio-emotional processing during adolescence.
The environmental and biological changes at adolescence lead to new social encounters and heightened awareness and interest in other people. The importance of evaluating other people may be associated with increased attention to socially salient stimuli, particularly faces, and the processing of emotional information. Recognition of facial expressions of emotion is one area of social cognition that has been investigated during adolescence (Herba and Phillips, 2004). The amygdala, a brain region associated with emotion processing (Adolphs, 1999; Dolan, 2002; Phillips et al., 2003), was found to be significantly activated in response to the perception of fearful facial expressions in an fMRI study of adolescents aged between 12 and 17 years (Baird et al., 1999). The perception of happy faces compared with neutral was associated with significant bilateral amygdalar activation in a group of 12 adolescents aged 13–17 years (Yang et al., 2003). Sex-differences in amygdala-mediated cognitive development have also been reported to occur during adolescence (Killgore et al., 2001). While the left amygdala responded to fearful facial expressions in all children, left amygdala activity decreased over the adolescent period in females but not in males. Females also demonstrated greater activation of the dorsolateral PFC over this period, whereas males demonstrated less activation in this region with age. These findings were taken as evidence for an association between cerebral maturation and increased regulation of emotional behaviour; the latter mediated by prefrontal systems. A similar result was found in a recent study by Yurgelun-Todd and Killgore (2006) in a study of facial emotion processing in adolescents. In this study, bilateral prefrontal activity increased with age (from 8 to 15 years) for girls, whereas only the activity in right PFC was correlated with age in boys. It is possible that functional maturation associated with face emotion processing may be modulated by gender-specific hormonal profiles.
The effect of age on amygdala response to fearful facial expressions was addressed byThomas and colleagues (2001). Adults (mean age 24 years) relative to children (mean age 11 years) demonstrated greater amygdala activation to fearful facial expressions, whereas children relative to adults showed greater amygdala activation to neutral faces. It was argued that the children perceived the neutral faces as more ambiguous than the fearful facial expressions, with resulting increases in amygdala activation to the neutral faces. Age-related differences in neural strategies for emotion processing have been shown in an fMRI study of a group of adolescents (aged 7–17 years) and a group of adults (aged 25–36 years) who viewed faces showing emotional expressions. While viewing faces with fearful emotional expressions, compared with adults, adolescents exhibited greater activation of the amygdala, orbitofrontal cortex (OFC) and anterior cingulate cortex (ACC) (Monk et al. 2003). When subjects were asked to switch their attention between a salient emotional property of the face, like thinking about how afraid it makes them feel, and a non-emotional property, such as how wide the nose is, adults, but not adolescents, selectively engaged and disengaged OFC. In other words, the adult brain better modulated OFC activity based on attention demands, while the adolescent brain better modulated activity based on the demands of emotion. On the other hand, when there were no attentional demands, emotional content of the stimuli induced higher activity in ACC, OFC and amygdala in the adolescents compared with the adults. These fMRI results suggest that both the brain's emotion processing and cognitive appraisal systems develop during adolescence. This development has previously been interpreted in the context of the Social Information Processing Network (SIPN) model (Nelson et al., 2005).
The SIPN model posits that social information processing occurs by way of three interacting neural ‘nodes’, which afford the detection of social stimuli that are then integrated to a larger emotional and cognitive framework (Nelson et al., 2005). Nelson and colleagues propose that the ‘detection node’, comprising the intraparietal sulcus, STS, fusiform face area as well as temporal and occipital regions, deciphers social properties of the stimulus such as biological motion. The ‘affective node,’ including limbic areas of the brain including the amygdala, ventral striatum, hypothalamus and OFC, processes the emotional significance of the social stimulus. Finally, the ‘cognitive-regulatory node’, consisting of much of the PFC, is responsible for theory of mind, impulse inhibition and goal-directed behaviour. Development during adolescence of the nodes, the connections between them, the innervation by gonadal steroid receptors and the maturation of the neural substrates themselves, are proposed to explain development of social cognitive behaviours.
The emergence of the social self seems to be marked by a period of heightened self-consciousness, during which adolescents are thought to become increasingly preoccupied with other people's concerns about their actions, thoughts and appearance. This development has been described in terms of phases of egocentrism during childhood and adolescence (Elkind, 1967) and is based on Piaget's stages of cognitive growth (Inhelder and Piaget, 1958). It is proposed that after children develop internal representations of objects and referential thinking during early childhood, they reach the stage of the ‘emergence of concrete operations’. Between the ages of 7 and 11 years, children's abilities to deal with classes and hierarchies are proposed to be restricted to concrete, physical entities and do not extend to abstract thought. Children of this age group therefore manifest an inability to distinguish between a mental construction and perceptual phenomena. By age 11, the emergence of ‘formal operational thought’ enables children to differentiate between the perception of an object and their own mental construction of it, allowing them to objectify their own thoughts and reason about them. Piaget proposed that this new form of thinking allows children at early adolescence to conceptualise other people's thoughts and take their perspectives (Inhelder and Piaget, 1958).
The development of adolescent egocentrism is therefore thought to be a dialectic process: it is the ability to represent other people's thoughts as distinct from their own and therefore decentre themselves that also drives the new form of egocentrism. In other words, as soon as they are able to understand that other people have distinct thoughts and perspectives, they become preoccupied with the notion that other people's thoughts are focused on their own behaviour or appearance (Elkind, 1967). Elkind's original theoretical model of adolescent egocentrism delineates two ideation patterns thought to arise as a consequence, and to characterise common adolescent social behaviours: the ‘imaginary audience’ and the ‘personal fable’. The notion of the imaginary audience refers to adolescents’ beliefs that they are the object of other people's scrutiny. According to Elkind's theory, this belief results in increased self-consciousness, a tendency to anticipate the reactions of other people in relation to the self, and a feeling of being the focus of attention, regardless of whether a real audience exists or not in the situation. The personal fable, a related construct, denotes adolescents’ convictions of their own personal uniqueness, giving rise to the sense of being ‘special’ (Elkind, 1967).
Since this original account of adolescent egocentrism, social psychological studies have investigated the imaginary audience with questionnaires and qualitative approaches. The exact age, validity and explanation (e.g. Lapsely and Murphey, 1985; Frankenberger, 2000; Vartinian and Powlishta, 2001; Bell and Bromnick, 2003) of Elkind's account of adolescent egocentrism have been challenged, and the theory has since evolved.
The ability to take another's perspective is crucial for successful social communication. Reasoning about others, and understanding what they think, feel or believe, involves stepping into their ‘mental shoes’ and taking their perspective (Gallese and Goldman, 1998). The distinction between the phenomenal and representational levels of self-other relationships is worth noting. As detailed by Frith and de Vignemont (2005) and Vogeley and colleagues (2004), one can take different perspectives in terms of spatial representations, such that the locations of other entities in space are represented by the beholder in different reference frames. In an egocentric frame of reference, the location of an object is represented in relation to the subject, i.e. in relation to the personal agent (e.g. is the line on your right or left?), whereas in the allocentric frame of reference, the location of one object in relation to another object is represented by the agent (e.g. is the line on the right or left of the square?). Thus, while the egocentric perspective relates that which is seen to the agent who sees it, the allocentric perspective is independent of the agent's position. At the phenomenal level, however, the first-person perspective (1PP) (e.g. is the line on your right or left?) and the third-person perspective (3PP) (e.g. is the line on his right or left?) are both centred on an agent. Perspective taking at this phenomenal level requires ‘the translocation of the egocentric viewpoint’ from the 1PP t
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