ARCHIVES OF NEUROSCIENCES
ANNUS v - 2016
THE ADOLESCENT BRAIN
by Antonio Virgili*
Adolescence is a time of considerable development at the level of behaviour, cognition and the brain. At the same time, adolescence is a developmental period often characterized by suboptimal decisions and actions that are associated with an increased incidence of unintentional injuries, violence, substance abuse, unintended pregnancy, and sexually transmitted diseases. Some traditional neurobiological and cognitive explanations for adolescent behaviour have often failed to account for the nonlinear changes in behaviour observed during adolescence, relative to both childhood and adulthood. A plausible model of the neural mechanisms underlying these nonlinear changes in behaviour, such as neurosciences try to realize, is now taking the place of some previous biological and psychological theories and models. There is evidence, from recent human brain imaging and animal studies, that there is a heightened responsiveness to incentives and socioemotional contexts during this time, when impulse control is still relatively immature. These findings suggest differential development of bottom-up limbic systems, implicated in incentive and emotional processing, to top-down control systems during adolescence as compared to childhood and adulthood. This developmental pattern may be exacerbated in those adolescents prone to emotional reactivity, increasing the likelihood of poor outcomes.
Adolescence could also be described as a progressive transition from childhood into adulthood with an indefinable ontogenetic time course yet often co-occurring with puberty, which is defined by specific biological markers. The significant neuroendocrinological changes associated with puberty, such as increases in adrenal and gonadal hormones, are correlated with the development of secondary sexual characteristics and can influence brain function. The onset and hormone fluctuations of puberty may provide an explanation for the observed functional differences in subcortical activity between children and adolescents, versus activity in the prefrontal region, which reflects a more linear change with age. From an evolutionary perspective, adolescence is the period in which independence skills are acquired in order to increase the success of separating from the protective influence of the family. It is also a period when there is an increase in the likelihood of harm such as injury, depression, anxiety, drug use, and addiction. However, the most recent model suggests that risky behaviour and emotional reactivity are the products of a biologically driven imbalance between increased novelty and positive sensation seeking in conjunction with immature “self-regulatory competence”. One needs to engage in high-risk behaviour in order to leave the family and village to find a mate. This risk behaviour occurs simultaneously with an increase in sexual hormones, resulting in adolescents seeking sexual partners and is seen in other species. In conjunction with this novelty-seeking behaviour, there would need to be some mechanism for detecting cues of safety or danger. The increase in emotional reactivity during this period may allow adolescents to be more vigilant and aware of threat, to ensure their survival as they move from a safe environment to a novel one. In today’s society when adolescence may extend indefinitely—with individuals well into their 20s living with their parents, remaining financially dependent, and choosing mates later in life—these behaviours may be deemed inappropriate. When faced with an immediate personal decision, adolescents will rely less on intellectual capabilities and more on feelings, it is said. Nevertheless, when reasoning about a hypothetical, moral dilemma, the adolescent will rely more on logical information. In other words, when a poor decision is made in the heat of the moment, the adolescent may know better, but the salience of the emotional context biases his or her behaviour in opposite direction of the optimal action.
Today there are several reasons why the study on adolescent brain has relevant social effects, among them three are of recurrent actuality, they are: 1. May adolescents, and at what age, be involved in electoral procedures becoming active (and passive) voters? 2. When adolescents become of age for other social and legal questions? 3. What about legal punishment of minors? Other social and cultural questions could also be mentioned but we restrict reflexions to the points above mentioned, even if, in a certain sense, all depends in large part on two more general questions to which we continue to give vague, dissimilar and contradictory answers: when does adolescence end (or what is the age range of adolescence)? What actual social limits does adolescence impose?
Social and cultural roots
In societies without passage rites, it is difficult to say when and how an adolescent become, or has to be considered, an adult. In tribal societies it is easy, maybe something wrong but clear. The adolescence “phase” is essentially a construction typical of modern societies and of psychological studies (and the related trend of psychologization of culture). The first psychologist to propose a theory on adolescence was Stanley Hall (1844-1924), who based his studies on a scientifically based method, innovative with respect to the analyzes of other contemporary scholars who had anticipated the topic. Hall's theory was influenced by the scientific discoveries of the time, especially the theory of biological evolution by Charles Darwin. With the publication, "The origins of the species", Darwin stated that the evolution of all living beings had been caused by a slow but gradual biological change. On the earth there are unicellular organisms that have developed up to now, reaching ever more complex forms. Margaret Mead strongly questioned Hall and Freud's conception of the universality of their theories, based on the observations of an exclusively Western-type adolescent sample. Mead did not come to a theoretical elaboration, but identified "cultural relativism" as a basic element for understanding human development; germ cells do not transmit culture, social orders and cultural agents are the reference for understanding human development. Mead directly observed the youth of the Samoa islands and found that children participated in all the sexual or social processes of the community without prejudice or imposed respectability. Sex, death, the origin of life were presented to the child as natural events, society did not inhibit social learning. If we consider the didactic suggestions of our days we highlight the foolishness of the contemporary mass school that speaks of "skills" to be acquired in crowded parking areas for young people.
Lewin arrived in 1939 to consider the non-relevance of these factors on the influence of human development. He found it interesting to identify how the biological, psychological and social components interacted with each other to determine the growth of the individual. The interest in these dynamics led Lewin to a remarkable discovery with "Field Theory"; unfortunately his suggestions to a wider integration of social components did not obtain much attention among psychologists. Jean Piaget contributed much to the understanding of cognitive development. He focused his research initially on childhood and childhood; only later did he become interested in adolescence. Piaget's theory was based on the development of the individual through stages or phases. Each stage represents a totality of inter-connected and non-casual behaviors, composed of a set of thoughts and behaviors. The transition from one stage to another is hierarchically oriented. The adolescent acquires the ability of abstract reasoning, moving away from the real world and accessing the world of the possible. Traces the various problems using abstract intelligence. This allows him to discover an infinite world of solutions, to travel in space, to travel through time, to create solutions, to destroy something by foreseeing the consequences. All with the sole power of thought. The development of thought is facilitated by the maturation of the nervous system, as well as by experiences with physical reality and the social environment.
Recognizing that the adolescent phenomenon is strongly correlated with social and cultural dynamics does not allow us to argue that adolescence does not exist. It is a social phenomenon, not natural, and it is certainly related, for its duration, to the social need to prepare the individual for his own place in the differentiated universe of work. Psychologists, sociologists and cultural anthropologists have studied adolescence for a long time, even though they have not yet developed a clear and linear discourse capable of expressing the integrated point of view of the various disciplines. The impression one gets in approaching the broad specialist literature is indeed that each discipline has developed its own particular perspective on the subject and, while modifying details or adding updated information, continues to reiterate it, neglecting the suggestions that could come from the other disciplines. More recently, neuroscience has oriented part of the studies on adolescence, but always giving greater weight to the individual and psycho-physiological components.
As every persons or scholar that habitually attends adolescents knows well, there are wide individual differences among them at the same age. For example, at the age of 12 or 13, some of them are both physically and for their behaviour still childish, some others are much more mature and looks like being one or two years older. It is also known that between male and female adolescent growth rate are staggered, so as is puberty (earlier for girls, later for boys). These are rather known differences, instead those connected to brain development, behavioural experiences and patterns, and the modelling role of families and of peer groups are less well known, so they are problematic to define limits and characteristics that should have to be certain and are still today vague. They should have been certain because in the most of societies these limits mean very different social and legal possibilities about marriage, criminal responsibility, work activities, family norms, appointments, etc.
In several Countries the decision to impose criminal responsibility rests on an assumption about the defendant's decision to engage in proscribed conduct. We punish only those who we believe had the capacity to make a choice. In an increasingly violent society, the criminal law and the assumptions upon which it rests are relentlessly tested. A new generation of neuro‐imaging technologies and neuroscience researches seems to offer to provide insights into structural and functional abnormalities in the brain that may limit the autonomy of many dangerous offenders and unravel the fabric of the criminal justice system. How will the results of these technologies be received by the courts—are they relevant to existing formulations of the prima facie case, the insanity defence, or mitigation of sentence; will changes in the science or the law be required to accommodate this knowledge? The new generation of studies may appropriately play a role in assessing culpable mental states or other social norms. But, are they also reliable? May we consider adult with mental problems more, or less, responsible than adolescents? Is it socially acceptable that an adolescent killer is not responsible? What about persons having different mental problems? And, what to do if some societies make mental problems more diffused?
On a cognitive or behavioural level, the immature cognition of adolescence is characterized as impulsive (i.e., lacking cognitive control) and risk taking, with these constructs used synonymously and without appreciation for distinct developmental trajectories for each. Human imaging and animal studies suggest distinct neurobiological and developmental trajectories for the neural systems that underlie these separate constructs of impulse control and risky decisions. In a rather short period of time – about twenty years - the neuroscience of adolescence has matured from a general exploratory point to one that is now approaching a consolidated knowledge and the prevalent model. Even if, as in any field that is barely young, there remain many contradictions and unknowns. Thank the many researches and studies it is demonstrated that the adolescent's brain is different from both the child's brain and the adult's brain. It is different with respect to both morphology and function, and at the levels of brain structures, regions, circuits, and systems. It is different with respect to grey matter, white matter, structural connectivity and neurotransmission. It is different in ways that are revealed in studies of sleep, electrophysiology, functional imaging, pharmacological challenge and stress reactivity, so as by observations of behavioural scientists who study both normative development and developmental psychopathology. On the other side it could appear that the notion of “the adolescent brain” is some sort of myth, because still there is not a definite separation among childhood, adolescence phases, and early adulthood. But probably there could not be so definite separation because the changes are along a continuum from the age of 11 till the age of 20.
It is important to note that: A) “different” brain does not necessarily mean “deficient”; B) while there are some universals in adolescent brain development, there are also very important individual differences; C) the process of brain maturation in adolescence (or during any period, for that matter) unfolds within an environmental context that influences the course of neural development and moderates its expression in emotion, behaviour, and cognition. It is also important to acknowledge that currently there is a better understanding of the ways in which adolescent brain development may contribute to psychopathology and problem behaviour than of the ways in which it may contribute to normative development and positive functioning, and that researchers have paid more attention to the study of universals and processes of biological maturation than to individual differences and environmental influences. As collaborations between neuroscientists and other social scientists, mainly sociologists (neuro-sociologists) and anthropologists become more common, attention to these issues will most likely increase. As said before, till now the psychological approach is widely prevailing.
The evidence also points to early adolescence as a time of considerable brain plasticity, which has several important implications. To the extent that patterns of synaptic proliferation and elimination are contextually-dependent (something that is not yet known), we should expect to see considerable individual differences in brain structure and function that can be linked to differences in experience. In this sense, brain plasticity in adolescence makes this period a time of considerable opportunity for intervention. At the same time, however, heightened brain plasticity in adolescence may contribute to increased vulnerability to certain forms of psychopathology, many of which begin or intensify during adolescence. Whereas synaptic pruning in the frontal lobe was the main focus of attention in previous research on structural aspects of brain development in adolescence, white matter development has clearly stolen some of the scientific limelight. It is now clear that adolescence is a time of dramatic changes in fiber tracts that link different brain regions and structures. This increase in structural connectivity is, not surprisingly, paralleled by increases in functional connectivity, which has significant implications for our understanding of changes in adolescent behaviour, especially with regard to cognitive control.
Some works have described that individual differences in individuals' vulnerability to peer pressure are correlated with differences in structural and functional connectivity in ways that link the development of resistance to peer influence to improvements in the coordination of emotion and cognition. This finding is also consistent with research showing that individual differences in structural connectivity during early adolescence are correlated with delay discounting performance, such that individuals with more highly organized white matter are less likely to be drawn to immediate rewards. It is worth nothing, however, that these findings are hard to reconcile with some reports indicating that structural maturity of white matter is correlated with more, not less, risk-taking. It is too early in the development of this area of work to render an explanation for this apparent inconsistency, but my guess is that research on the behavioural correlates of inter-regional connectivity ultimately may prove more informative than that on the correlates of grey or white matter density, especially in the study of self-regulation. Evidence also grows concerning important changes in subcortical processes during adolescence. Especially important are increases in dopaminergic activity during early adolescence in pathways linking limbic, striatal, and prefrontal areas. These changes, documented in both human and animal studies, have been linked to changes in reward-directed activity, but also that the pubertal period is a time of changes in appetitive behaviour more generally, and not simply in reward-driven behaviour. Dopamine, of course, plays a role in reward anticipation and reward-seeking, but it also has been implicated in motivated action more broadly. So, these three changes – the change in the ratio of grey to white matter in prefrontal areas, the increase in connectivity between prefrontal and other regions, and the increase in dopaminergic activity in prefrontal-striatal-limbic pathways – provide the basis for a theory that links brain maturation in adolescence to increased vulnerability to risky behaviour.
Probably, middle adolescence is a time of heightened vulnerability to risky and reckless behaviour because of the temporal disjunction between the rapid rise in dopaminergic activity around the time of puberty, which leads to an increase in reward-seeking, and the slower and more gradual maturation of the prefrontal cortex and its connections to other brain regions, which leads to improvements in cognitive control and in the coordination of affect and cognition. As dopaminergic activity declines from its early adolescent peak, and as self-regulatory systems become increasingly mature, risk-taking begins to decline. As a consequence, middle adolescence (roughly 14 to 17) should be a period of especially heightened vulnerability to risky behaviour, because sensation-seeking is high and self-regulation is still immature. And in fact, many risk behaviours follow this pattern, including unprotected sex, criminal behaviour, attempted suicide, and reckless driving. But, how do we explain risky behaviour that follows a different developmental trajectory? It may be argued that the reason that certain other risky behaviours, such as binge drinking, peak a little later in development is because there are more constraints on opportunities to engage on them during middle adolescence as there are several prohibitions operating in this age time.
This prevalent general model of adolescent brain development has been extended beyond the study of risk-taking in several perspectives. In fact adolescence is also a time of important changes in the processing of social and emotional information, much of which is subserved by the same regions and systems that undergird the motivational and self-regulatory changes described by scholars who have focused on risk taking. Whether and how these various sets of changes may be linked is an important social question. For instance, there is evidence that adolescents are highly responsive to the social rewards afforded by positive peer evaluation and that such rewards activate the same brain regions as non-social rewards. Many forms of psychopathology onset or intensify during adolescence. Some, but not all, of these forms of psychopathology in one way or another involve appetitive or affective dysregulation (e.g., depression, substance abuse, eating disorders). This leads to the very reasonable hypothesis that at least some forms of adolescent psychopathology are related to abnormalities in the remodelling of the dopaminergic system at puberty (which would affect appetitive and affective functioning) or in the morphological changes of the prefrontal cortex or its connections to other brain regions over the course of adolescence (which would affect self-regulation).
The emergent neuroscientific perspective, saying “emergent” because the framework is still developing, has the potential to structure a new, overarching model of normative and atypical adolescent development. Notably, the basic notion that early adolescence is characterized by a dramatic increase in appetitive drive that remains relatively unchecked until self-regulatory systems mature is eerily similar to the basic Freudian model of adolescence (change “appetitive drive” to “libido” and “self-regulatory systems” to “ego development” and see for yourself) that modern-day empiricists have derided. According to this model, in emotionally salient situations, the more mature limbic system will win over the prefrontal control system. In other words, when a poor decision is made in an emotional context, the adolescent may know better, but the salience of the emotional context biases his or her behaviour in opposite direction of the optimal action.
Several unresolved issues
The WHO considers adolescents those aged 10-19 years old, and it seems a reasonable point of view because includes individual neuro-anatomical variabilities, social and cultural differences, and put at 20 the age to be “surely” an adult. On the opposite side, under 10 years old it is childhood. The problem is that the “legal” age is (and has to be) a standard value, so it neglects or ignores the individual and social differences.
It has to be said that there are many behavioural and self-report studies that compare children and adolescents, fewer that compare adolescents and adults, and almost none that compare children, adolescent, and adults all at once and allow for the detection of trends that may not be linear. This is especially problematic where reward-seeking and risk-taking are concerned, because, in light of research indicating the curvilinear nature of the developmental trajectory of dopaminergic receptor remodelling, there is reason to think that these behaviours increase until middle adolescence and then decline. In contrast, given what we know about maturation of the prefrontal cortex and its connections with other brain regions, the developmental course of cognitive control would be expected to increase linearly and into the decade of the 20s. To the extent that a goal of research on brain development is to better understand adolescent behaviour, it is important to complement the neurobiological studies with both experimental and field research designed to examine whether the basic principles of development identified in the lab have parallels in the real world.
Despite the basic heuristic utility of this emergent model, one element that has been missing from most discussions linking adolescent brain development and behaviour is the context in which adolescents live. Here I am not referring so much to the impact of context on brain development (although the likely plasticity of the adolescent brain makes this a crucial issue for future study), but the role of context in moderating the way that neural influences are expressed. The heightened vulnerability of middle adolescence will have different consequences in different settings, both as a function of available opportunities to engage in reward-seeking, and as a function of the degree to which external agents regulate adolescents whose self-regulation is still maturing. With respect to reward-seeking, there are many ways for adolescents to satisfy their inclinations toward sensation-seeking that are not harmful or antisocial. And with respect to self-regulation, the degree to which adolescents engage in risky behaviour is in part a function of opportunities to access substances and circumstances that place them at risk. The reason that the incidence of alcohol-related driving fatalities declined when the legal drinking age was raised from 18 to 21 in the US has nothing to do with changes in the brain development of young people that somehow magically transformed high school students into mature decision-makers. By the same token, increasing parental monitoring, placing restrictions on teen driving, or providing adult supervision during after-school hours would likely reduce teen pregnancies, car crashes, and juvenile crime, but for reasons that have nothing to do with neurobiological development. Brain development undoubtedly influences adolescents' behaviour, but it does so within a context.
There are some ethical questions too. Have we to consider neurobiological trajectories as the right way to classify persons and the individual behaviour? Are we not moving toward a kind of biological or genetic reason of violence, social problems, etc. as in past time someone did about less developed areas, criminal people and other racial discriminations? Will we build a kind of “criminal brain”? The findings and model have significant implications for heated debates on public policy and the treatment of minors in the judicial system. Adolescents show adult levels of intellectual capability earlier than they show evidence of adult levels of impulse control. As such, adolescents may be capable of making informed choices about their future (e.g., terminating a pregnancy) but often do not yet have full capacity to override impulses in emotionally charged situations that require decisions in the heat of the moment. Unfortunately, judges, politicians, advocates, and journalists are biased toward drawing a single line between adolescence and adulthood, adolescence and childhood, for different purposes under the law that is at odds with developmental cognitive neuroscience and sometimes also against ethical and moral common sense.
*Antonio Virgili, is a scholar of Sociology, Psychology and Neurosciences, Specialised in Neuro-sociology and Sexology; former lecturer of Social Psychology at Istituto Superiore di Sociologia, is the Scientific Director of Istituto Italiano di Scienze Sociali and professor of Social Sexology at the UNISED.
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