PERSPECTIVE

published: 12 May 2022

doi: 10.3389/fnhum.2022.782205

Neuroscience Outside the Box: From

the Laboratory to Discussing Drug
Abuse at Schools
Thereza Cristina Machado do Vale 1,2 , Luana da Silva Chagas 1,2 ,
Helena de Souza Pereira 3 , Elizabeth Giestal-de-Araujo 2 , Analía Arévalo 4† and
Priscilla Oliveira-Silva Bomfim 1,2* †
1
NuPEDEN, Nucleus for Research, Education, Dissemination and Neurosciences Popularization, Department of
Neurobiology and Program of Neurosciences, Institute of Biology, Federal Fluminense University, Niterói, Brazil, 2 Department
of Neurobiology and Program of Neurosciences, Institute of Biology, Federal Fluminense University, Niterói, Brazil,
3
Department of Molecular and Cell Biology, Institute of Biology, Federal Fluminense University, Niterói, Brazil, 4 Department of
Experimental Surgery, University of São Paulo Medical School, São Paulo, Brazil

One of the effects of the current COVID-19 pandemic is that low-income countries were
pushed further into extreme poverty, exacerbating social inequalities and increasing
susceptibility to drug use/abuse in people of all ages. The risks of drug abuse may
Edited by: not be fully understood by all members of society, partly because of the taboo
Madhavi Rangaswamy, nature of the subject, and partly because of the considerable gap between scientific
Christ University, India
production/understanding and communication of such knowledge to the public at large.
Reviewed by:
Susan Janse Van Rensburg,
Drug use is a major challenge to social development and a leading cause of school
Stellenbosch University, South Africa dropout rates worldwide. Some public policies adopted in several countries in recent
Lukasz Konopka, decades failed to prevent drug use, especially because they focused on imposing
Brain to Behavior Neuroscience
IPD-Duly, United States combative or coercive measures, investing little or nothing in education and prevention.
*Correspondence: Here we highlight the role of neuroscience education as a valid approach in drug
Priscilla Oliveira-Silva Bomfim use education and prevention. We propose building a bridge between schools and
[email protected]
scientists by promoting information, student engagement and honest dialogue, and
† These authors share senior
authorship
show evidence that public policy regulators should be persuaded to support such
science-based education programs in their efforts to effect important positive changes
Specialty section: in society.
This article was submitted to
Cognitive Neuroscience, Keywords: neuroscience, education, public policies, science outreach, drug education
a section of the journal
Frontiers in Human Neuroscience
Received: 24 September 2021 INTRODUCTION
Accepted: 25 April 2022
Published: 12 May 2022 The abuse of substances, illicit or not, is a worldwide health problem that deserves immediate
Citation: attention. According to the United Nations Office on Drugs and Crime, millions of drug users
Machado do Vale TC, worldwide also have depression, anxiety or suicidal intentions (UNODC, 2021). Secondary
da Silva Chagas L, consequences of drug abuse include a heightened risk of contracting hepatitis B/C and HIV and
de Souza Pereira H, death or injuries from vehicle accidents (Olfson et al., 2018; Glei and Preston, 2020). The combined
Giestal-de-Araujo E, Arévalo A and costs of these possible consequences most likely surpass the cost of most government prevention
Oliveira-Silva Bomfim P (2022)
programs. In low- and middle-income countries, huge social inequalities worsen the issue and
Neuroscience Outside the Box: From
the Laboratory to Discussing Drug
highlight the inefficiency of public policies that focus more on fighting rather than preventing drug
Abuse at Schools. abuse (UNODC, 2021).
Front. Hum. Neurosci. 16:782205. Here we address neuroscience’s potential to contribute to this discussion (World Health
doi: 10.3389/fnhum.2022.782205 Organization [WHO], 2004), especially in schools, a privileged environment for knowledge

Frontiers in Human Neuroscience | www.frontiersin.org 1 May 2022 | Volume 16 | Article 782205

Machado do Vale et al. Neuroscience Outside the Box

dissemination (Faggiano et al., 2005). Activities and programs increase the chances of dropping out of school (Henkel, 2011;
that engage scientists, students, families, school teachers/staff, World Health Organization [WHO], 2014; Tice et al., 2017;
physicians and therapists engaged in rehabilitation, and members Valkov, 2018). Moreover, legal and illegal drug consumption
of the community or neighborhood are much more likely to have profoundly impacts young people’s mental health, a focus
positive results than actions that aim to instill fear (i.e., fighting of great concern among health professionals, families, and
rather than preventing). We emphasize the importance of making public institutions (Galvão et al., 2017). These issues have
the information engaging and accessible to the target audience by become particularly important in recent months, since the
considering their prior knowledge and cultural/socioeconomic beginning of the COVID-19 pandemic, which among other social
level, as well as creating public policies that promote and disruptions, led to school closures (Cowie and Myers, 2020;
support such actions. Chaffee et al., 2021).
In many countries around the world, including Brazil,
depression is higher among individuals who abuse alcohol, one of
THE BRAIN UNDER (DRUG) PRESSURE the first drugs that adolescents have contact with. Depression, in
turn, can lead to suicidal ideation (Kim, 2017; Rehan et al., 2017;
The use of substances such as alcohol, marijuana, cocaine McHugh and Weiss, 2019). Data have shown that 5% of Brazilians
and opioids, among others, usually starts during adolescence, have attempted suicide at least once and that 24% of those cases
a period of rapid brain circuit maturation that is highly are associated with alcohol consumption. Importantly, suicide is
influenced by genetic and environmental factors (Fuhrmann the 3rd cause of death globally and Brazil is among the top 10
et al., 2015; LeNoue and Riggs, 2016; UNODC, 2021). countries with the highest suicide rates (Laranjeira et al., 2012;
The need for independence, identity formation and peer Barbosa and Teixeira, 2021).
acceptance (Bauman and Phongsavan, 1999; UNODC, 2021)
make adolescence a critical period of physiological and
social development characterized by an increase in risk-taking THE IMPACT OF DRUG ABUSE ON
behaviors driven by the pursuit of quick rewards (Botvin EDUCATION
and Botvin, 1992; Willoughby et al., 2013; UNODC, 2021).
These behaviors are associated with an immature prefrontal In Brazil, government data suggest that drug use is prevalent
cortex, an area of the brain responsible for evaluation and among both private and public school students, with public
planning, decision making and impulse control. Since this school students usually consuming heavier, lower-cost drugs.
region remains highly sensitive to external influences until Interestingly, students in both groups lack an understanding of
around 20 years of age, drug use during adolescence can lead substance composition, as well as the risks and consequences of
to significant functional and structural brain changes. These drug use (Laranjeira et al., 2012).
changes, in turn, exacerbate the natural “imbalance” among In terms of neurological effects, evidence indicates that
the regulatory frontal circuits (whose maturation is delayed young people who binge drink or consume heavy amounts
relative to the cortico-limbic circuits), potentially leading to long- of alcohol show reduced gray matter in frontolateral and
term problems in the areas of emotional control and reward temporal cortices, as well as reduced white matter development
feedback (Gogtay et al., 2004; Arain et al., 2013; Ernst, 2014), in the corpus callosum and pons, which may increase the risk
as well as an increased risk of developing drug addiction. of developing alcohol-related disorders, as mentioned above
Furthermore, adolescents seem unconcerned with the possible (Squeglia et al., 2015; Cservenka and Brumback, 2017). Drug use
consequences of using psychoactive substances and a tendency during this period of life can also disrupt motivation, memory,
to believe they are in control and could discontinue use and learning (Fowler et al., 2007), all functions essential during
at any point if they wish (Bauman and Phongsavan, 1999). the educational process.
Importantly, child drug use is associated with the later use of Excessive alcohol consumption also affects brain regions
potentially more harmful drugs, such as heroin and cocaine involved in visual working memory, which can have a significant
(Fletcher et al., 2008). negative effect on learning (Squeglia et al., 2012). Interestingly,
Studies show that an individual’s family may be the root of adolescents undergoing rehabilitation for alcohol dependence
substance use/abuse, since children and adolescents often look show worse performance on verbal and non-verbal memory tasks
up to their parents and caregivers (Flay et al., 1994; Biederman relative to controls, as well as reduced hippocampal volume
et al., 2000). Factors that increase children’s risk of becoming (Brown et al., 2000; Tapert and Schweinsburg, 2005). These
smokers include free access to cigarettes (Kim et al., 2009), structural and functional changes are bound to have long-
having parents who ask them to bring them cigarettes (Hill lasting effects.
et al., 2005) or are heavy smokers (Hill et al., 2005), and being Tobacco use has been shown to increase the risk of addiction
exposed to smoking by others over a period of years (Mays et al., to other substances. Human and animal studies of tobacco use
2014). Furthermore, observing relatives’ social behavior may send show impairments in learning capacity, memory, attentional
children the message that enjoyment is directly related to alcohol control, mood, impulse control, and behavioral problems, even
consumption (Ryan et al., 2010; Smit et al., 2018). when consumed in small doses (Abreu-Villaça et al., 2003;
Alcohol abuse in young people is highly influenced by Counotte et al., 2009; Gould and Leach, 2014; US Department of
underlying levels of stress, anxiety, and depression, and can Health and Human Services, 2016; Valentine and Sofuoglu, 2018;

Frontiers in Human Neuroscience | www.frontiersin.org 2 May 2022 | Volume 16 | Article 782205

Machado do Vale et al. Neuroscience Outside the Box

Zarrindast and Khakpai, 2019; Leslie, 2020). While tobacco use Since most research is published in English, an added
among young people has been a concern for several decades, challenge for scientists and other professionals in non-English
the relatively recent “new wave” of flavored e-cigarettes has speaking countries is translating scientific findings (as well as
worsened the problem, as these are particularly popular among adapting them) for a non-English speaking audience (Márquez
teenagers (Brown et al., 2000). While flavored e-cigarettes are and Porras, 2020; Roche et al., 2020). A major aim of scientific
mostly marketed to people wanting to quit, users are often communication is to reach people who do not work in the areas
young people who never smoked before and who mistakenly of science or health and provide them with the opportunity and
believe that e-cigarettes are less harmful than conventional tools to understand and discuss issues that are of interest to
cigarettes (Flay et al., 1994; Biederman et al., 2000; Kim et al., society, such as drug abuse (Fischhoff, 2013). Figure 1 represents
2009). Besides nicotine, e-cigarettes contain substances- some a model of what this process should include, from scientific
with carcinogenic, pro-inflammatory and immunosuppressive information adapted by scientists for proper communication to
potential- whose short and long-term effects are still unknown the elaboration/modification of targeted public policies.
(Hill et al., 2005; Mays et al., 2014). In line with this proposal and following UNESCO’S
Alcohol and nicotine are thought to be the gateway for recommendation for educators to apply interactive teaching
illegal drugs like Cannabis (Secades-Villa et al., 2015), which also methods (UNESCO et al., 2017), our group previously developed
impairs learning, memory and attention. Most of these effects a neuroscience-based board game called “Crash: find the exit”
are dose-dependent, with considerable interindividual variation to promote information, engagement and dialogue at schools
(D’Souza et al., 2008; Ramaekers et al., 2009; Theunissen et al., about substance abuse and its effects on the central nervous
2012; Petker et al., 2019). Chronic marijuana use in adolescents system (Da Silva Chagas et al., 2020). In this collaborative
can lead to irreversible IQ loss, even when use is interrupted game developed for middle and high school students (ages
in adulthood (Meier et al., 2012). Also, Owens et al. (2019) 12 and older), we present information about 22 neuroactive
reported that a positive urine screen for THC was associated with drugs (e.g., depressants, hallucinogens, stimulants, anabolic
lower performance on working memory tasks, as well as reduced steroids, and prescription drugs) as well as brain anatomy,
fMRI activity in the prefrontal cortex, posterior parietal cortex, cell types/structures, neurotransmitter actions, the impact of
supplementary motor area, and insula, even when there was no drug abuse on nervous system physiology, and the mechanisms
previous history of cannabis use. Furthermore, since learning underlying overdose (including effects on other systems, such
consolidation is aided by positive emotions (Tyng et al., 2017) as cardiovascular and renal). We also added discussion points
and marijuana is involved in the processing of negative emotions about depictions of drug use in series or films, making it
(Bossong et al., 2013), its use may play an additional negative a particularly interesting experience for young audiences (Da
role in learning. Silva Chagas et al., 2020). Other initiatives for teaching young
Finally, as mentioned above, one major consequence of people about drug abuse have also employed games and even
substance abuse in school-aged children (besides the cited interactive platforms (Miller et al., 2006; Cheng et al., 2011;
neurophysiological, social and emotional issues) is an increased Klisch et al., 2013; Epstein et al., 2016; Kapitány-Fövény et al.,
school dropout rate (Tice et al., 2017; Valkov, 2018), a critical 2018; Stapinski et al., 2018). Such projects have shown positive
problem in Brazilian education that is also fueled by inefficient results in reducing first use, preventing transition to addiction,
public policies, family disruption, and learning difficulties, and overall prevention (Faggiano et al., 2014).
among other factors (Vasters and Pillon, 2011; Cardoso and Importantly, interventions are most effective if they are
Malbergier, 2014; Bittencourt et al., 2015; de Silva Filho and tailored to the group’s particular age and risk level (Gilligan
Araújo, 2017). et al., 2019). According to MacArthur and colleagues, school
programs target normative beliefs (i.e., beliefs held by peers or
other important people that influence kids’ behaviors), establish
NEUROSCIENCE AS AN ALLY TO a bond with the school, and train risky behavior avoidance.
EDUCATION: A TOOL TO PREVENT However, this approach does not establish a dialogue or promote
USE/ABUSE adolescents’ critical thinking or their ability to make choices.
Instead, it aims to impose socially desirable behaviors while
Neuroscience knowledge can be used to help kids and teens foster avoiding those endorsed by peers (Silva, 2016; MacArthur et al.,
healthy cognitive and emotional skills that will help them make 2018).
choices regarding drug use and other behaviors. However, it is According to Faggiano and colleagues, there are three reasons
often challenging to present this knowledge in a way that is why schools are the right environment to implement drug-
accessible and easy to relate to, and one must always consider prevention programs: (1) four out of five tobacco smokers start
individuals’ prior knowledge and experience (Bruer, 1997; World before adulthood, thus substance use prevention should focus
Health Organization [WHO], 2004; Sigman et al., 2014; Horvath on school-age children and adolescents before their beliefs and
and Donoghue, 2016). The choice of language is critical, as expectations about substance use are established; (2) schools
oversimplifications could generate more neuromyths (Howard- offer the most systematic and efficient way to reach significant
Jones and Fenton, 2012). Furthermore, one must also consider numbers of young people each year, and (3) in most countries,
the audience’s expectations and concerns, their religious and schools can adopt and enforce a wide range of educational
ethical values, and their socio-economic status. policies (Faggiano et al., 2005). While other types of interventions

Frontiers in Human Neuroscience | www.frontiersin.org 3 May 2022 | Volume 16 | Article 782205

Machado do Vale et al. Neuroscience Outside the Box

FIGURE 1 | This figure illustrates our view of what a successful educational drug abuse prevention program should include. On the left side, we list the main issues
associated with school-age drug abuse, which include neurophysiological, emotional, and social factors that are known to increase rates of school dropout. On the
right side of the figure are efforts of scientific production, including interactive games and courses, which generate dialogue and critical thinking and, in turn, promote
research incentives, access to neuroscience, inclusion and dialogue, and public policies (middle panel), all of which can help reduce risky behaviors and mental
disorders.

have been proposed, including those targeting individuals and to the drug-abuse conversation started by scientists, family
families (Carney et al., 2016; MacArthur et al., 2018), evidence members, educational staff, and society. In essence, they can add
indicates that school-based interventions are more effective yet another ‘human’ component to complement the statistics
(Faggiano et al., 2005, 2014; Fletcher et al., 2008; Carney et al., (Mills and Wonoprabowo, 2020).
2016; Lichtenberg et al., 2020). Another important strategy is to be welcoming and engaging
As discussed by Sigman et al. (2014), among others, toward families, as several studies have reported an association
social development requires us to build a bridge between between child/adolescent substance use/abuse and their parents’
neuroscientists and school educators. Scientists develop tools, own history of substance and/or psychiatric disorders, two
technologies and educational approaches that engage young variables included in the list of family-based Adverse Childhood
people and promote experiences that consolidate learning. School Experiences (ACEs) (Forster et al., 2018; Shek et al., 2020).
educators, in turn, can use their expertise in dealing with different
age groups to disseminate the information in a palatable and
efficient manner (Howard-Jones and Fenton, 2012). We advocate PUBLIC POLICIES: COMBATIVE vs.
in favor of a two-way partnership between researchers and PREVENTIVE STRATEGIES
teachers or research centers and schools aiming to find creative
alternatives to presenting important information (e.g., about drug In 2018, an estimated 269 million people worldwide had used
abuse1 ). These approaches should be as fun, interactive and drugs at least once (UNODC, 2021). In Brazil, among 50,890
engaging as possible (Da Silva Chagas et al., 2020). interviewed public and private elementary and high school
Importantly, one should always engage the participation of students from all 27 Brazilian capitals, this number was 13,000,
doctors, therapists and other health workers directly involved or 25.5% (see text footnote 1). These high numbers may be
in drug abuse treatment, as these professionals can educate attributed to inefficient policies implemented in Brazil, which, as
the public about the negative impact of drug abuse not only mentioned before, favor a combative and prohibitive approach,
on physical and mental health, but also on individuals’ social rather than one centered on education and prevention (VI
well-being (e.g., work and relationships). Thus, by sharing LENADE, 2010). In 2017, one billion reais (approximately 186
their real-life experiences—which are usually not described in million US dollars as of August 2021) were invested in anti-
scientific articles—health professionals add a fundamental piece drug laws by the state of Rio de Janeiro. This amount would be
enough to fund the education of 252,000 high school students
1
According to data from the sixth national survey on psychotropic drug use among or 32,000 public university students for an entire year or build
public and private elementary and high school students. 121 schools for more than 77 thousand new high school students

Frontiers in Human Neuroscience | www.frontiersin.org 4 May 2022 | Volume 16 | Article 782205

Machado do Vale et al. Neuroscience Outside the Box

(Lemgruber et al., 2021). These data suggest that money allocated openly with their students to help them make better drug-related
to “fight drugs” (i.e., costs associated with public safety, public choices. In Australia (see text footnote 2) a similar initiative
ministry and defense, the rehabilitation of juvenile offenders, and is implemented from the beginning of the educational process
the prison system) might be better used in preventive programs. as part of the “health and physical education” curriculum. The
Scientists and educators should join forces to develop programs goal is to promote a discussion about drugs and their impact
that follow this line of thinking and that meet the needs of on different levels, including personal, familial and community.
communities from different socioeconomic levels and cultures in This Australian Program revisits the school curriculum early
different parts of the world. on (foundation to year 10), providing young people with
However, not all prevention-based programs are successful. honest and scientifically accurate information that is age-
In the US, two well-known campaigns–“Just Say No” and appropriate and thus enables them to evaluate information
its byproduct DARE (Drug Abuse Resistance Education)–were critically and consciously. Following educational public policies,
developed in the early 80s and were implemented for many successful programs cover topics such as HIV transmissibility
decades. Despite extraordinary government investments and (needle sharing), teenage pregnancy (considering the impact
insistence on these programs, it is generally known that they of drugs in fetal development), chemical dependence, mental
failed at what they proposed to do (Pan and Bai, 2009; Lilienfeld health disorders, and the consequences of car accidents (e.g.,
and Arkowitz, 2014). While the approach was preventive and resulting from drunkenness), all potential consequences of drug
not combative, the “Just Say No” campaign did not provide use/abuse (UNODC, 2021).
any useful information or tools for young people to make the
right decisions autonomously. While the DARE campaign2 , 3
did involve some drug-related education, its approach was CONCLUSION
never inclusive or interactive. The same failure has been
observed with a Brazilian adaptation of these programs, a project While, there is some disagreement on the potential contribution
called PROERD (Educational Program for Drug Resistance of using neuroscience-based knowledge in the classroom (and
and Violence) (Sanchez et al., 2021), which has traditionally how such contributions should be implemented) (Bruer, 1997;
followed a more combative approach. In sum, none of these Sigman et al., 2014; Horvath and Donoghue, 2016), we strongly
programs invite young people to think, judge, evaluate or make believe there is an effective way of using scientific knowledge
their own decisions. in favor of social development, as has been shown with several
On the other hand, positive results have been observed successful projects cited above. However, it is important to
with the application of some non-normative programs emphasize that such efforts should engage teachers, parents and
in Europe. A study conducted simultaneously in Austria, the community at large to (1) create a positive atmosphere that
Belgium, Germany, Greece, Italy, Spain, and Sweden aimed to promotes open discussion; (2) avoid spreading erroneous or
prevent/avoid the use (experimental and regular) of alcohol, misleading information about drug abuse or other neuroscience
tobacco, and illicit drugs among students 12–14. In this 1 h/week concepts; (3) improve and stimulate neuroscience knowledge
in-school intervention over 12 weeks (with an 18-month follow- as a tool to prevent drug use/abuse among the youngest; (4)
up), students learn about different substances and search for guide teachers and students on how to approach this topic
the associated toxic properties and physiological alterations. creatively; (5) legitimize the school’s role in transforming society
This study resulted in a reduction of about 38% for alcohol use while providing knowledge to both children/adolescents and
and 26% for cannabis use (Faggiano et al., 2010). Moreover, their communities; (6) stimulate the study/popularization of
other reviews covering 29 and 51 US-based studies, respectively neuroscience in schools by leading important discussions about
(Faggiano et al., 2005, 2014) indicate that school-based programs social development; (7) promote the dissemination of this
produce a Number Needed to Treat (NNT) ratio of 33 for content beyond the school environment to promote critical
marijuana use (i.e., one out of every 33 students will be reflection in the community at large.
positively influenced by the intervention and will choose not to In this paper, we show how strategies that aim to fight
smoke marijuana), which is considered successful compared to drug use by instilling fear or teaching young people to avoid
similar studies. certain behaviors often meet little or no success, while those
More recently, programs like those cited above have been that foster inclusion and incite dialogue and understanding are
gradually implemented in school curricula in some countries. much more effective. Conducting fun activities while teaching
In the US, the “Safety first Program” includes 15 45–50 min neuroscience in an audience-appropriate language can be an
classes containing teacher-guided interactive activities providing excellent tool in such efforts. In Brazil, efforts to establish a
information regarding substances, their effects and drugs policies. bridge between the (neuroscience) laboratory and schools as well
This program is part of Drug Policy Alliance (see text footnote as the community at large have been increasing in the last few
2), a US-based policy that trains high school teachers to converse years. For such efforts to work, scientists must find a way to
work side by side with people in the schools (teachers, students,
2
families, staff), listening to their needs and finding new ways to
Drug Policy and Alliance (2021). https://drugpolicy.org/resource/safety-first-
real-drug-education-teens provide information through neuroscience-based activities. The
3
Australian curriculum review (2021). https://www.australiancurriculum.edu.au/ development of socially innovative tools such as the board game
f-10-curriculum/health-and-physical-education/structure/ developed by our group pave the way for new similar approaches.

Frontiers in Human Neuroscience | www.frontiersin.org 5 May 2022 | Volume 16 | Article 782205

Machado do Vale et al. Neuroscience Outside the Box

In addition, the discussion about issues like drug abuse needs to AUTHOR CONTRIBUTIONS
be encouraged at home as well. The first critical step is to start
the dialogue by making information accessible and motivating TM, AA, and PO-S designed the study. TM, LS, HS, and
scientists to engage society. These scientists can then join forces to PO-S managed literature searches and wrote the manuscript.
develop new preventive strategies. For now, our aim is to expose EG-d-A, AA, and PO-S critically reviewed the manuscript. LS,
these ideas and encourage scientists, educators and policymakers HS, and PO-S designed the figure. All authors contributed to and
around the world to actively engage in such efforts and thus approved the final manuscript.
contribute to improving society’s knowledge and well-being.

FUNDING
DATA AVAILABILITY STATEMENT
This work was supported by FAPERJ, PROEX/ UFF (Brazil), and
The original contributions presented in the study are included IBRO/ Dana Baw Grant 2022. They had no further role in study
in the article/supplementary material, further inquiries can be design, preparation, writing of the report, or in the decision to
directed to the corresponding author. submit this manuscript for publication.

REFERENCES Cheng, M. T., Annetta, L., Folta, F., and Holmes, S. Y. (2011). Drugs and the
Brain: Learning the Impact of Methamphetamine Abuse on the Brain through
Abreu-Villaça, Y., Seidler, F. J., Qiao, D., Tate, C. A., Cousins, M. M., Thillai, a Virtual Brain Exhibit in the Museum. Int. J. Sci. Educat. 33, 299–319. doi:
I., et al. (2003). Short-term adolescent nicotine exposure has immediate and 10.1080/09500693.2010.482571
persistent effects on cholinergic systems: critical periods, patterns of exposure, Counotte, D. S., Spijker, S., Van de Burgwal, L. H., Hogenboom, F., Schoffelmeer,
dose thresholds. Neuropsychopharmacology 28, 1935–1949. doi: 10.1038/sj.npp. A. N., De Vries, T. J., et al. (2009). Long-lasting cognitive deficits resulting from
1300221 adolescent nicotine exposure in rats. Neuropsychopharmacology 34, 299–306.
Arain, M., Haque, M., Johal, L., Mathur, P., Nel, W., Rais, A., et al. (2013). doi: 10.1038/npp.2008.96
Maturation of the adolescent brain. Neuropsychiatr. Dis. Treat. 9, 449–461. Cowie, H., and Myers, C. A. (2020). The impact of the COVID-19 pandemic
doi: 10.2147/NDT.S39776 on the mental health and well-being of children and young people.
Australian curriculum review (2021). Health and Physical Education (Version 8.4). Child. Soc. 10.1111/chso.12430. [Ebup ahead of print]. doi: 10.1111/chso.
Available online at https://www.australiancurriculum.edu.au/f-10-curriculum/ 12430
health-and-physical-education/ [accessed on Sep 9, 2021]. Cservenka, A., and Brumback, T. (2017). The Burden of Binge and Heavy Drinking
Barbosa, A., and Teixeira, A. F. C. T. (2021). Epidemiological and psychosocial on the Brain: Effects on Adolescent and Young Adult Neural Structure and
profile of suicide in Brazil. Res. Soc. Devel. 10:e32410515097. doi: 10.33448/rsd- Function. Front. Psychol. 8:1111. doi: 10.3389/fpsyg.2017.01111
v10i5.15097 Da Silva Chagas, L., Chagas De Almeida Silva, S., Matos Coelho De Oliveira, R.,
Bauman, A., and Phongsavan, P. (1999). Epidemiology of substance use in Magalhães Manhães, T., Vicenta De Oliveira Braga, G., Sarmiero Rodolpho, B.,
adolescence: prevalence, trends and policy implications. Drug Alcohol Depend. et al. (2020). Crash: find the exit- a neuroscience board game as a tool to discuss
55, 187–207. doi: 10.1016/s0376-8716(99)00016-2 mechanisms of drug abuse and addiction issues in the classroom. J. Biol. Educ.
Biederman, J., Faraone, S. V., Monuteaux, M. C., and Feighner, J. A. (2000). 1–9. doi: 10.1080/00219266.2020.1757489 [Epub ahead of print].
Patterns of alcohol and drug use in adolescents can be predicted by parental de Silva Filho, R. B., and Araújo, R. M. (2017). Evasão e abandono escolar na
substance use disorders. Pediatrics 106, 792–797. doi: 10.1542/peds.106.4.792 educação básica no Brasil: fatores, causas e possíveis consequências. Educação
Bittencourt, A. L. P., França, L. G., and Goldim, J. R. (2015). Adolescência Por Escrito 8, 35–48. doi: 10.15448/2179-8435.2017.1.24527
vulnerável: fatores biopsicossociais relacionados ao uso de drogas. Rev. Bioética Drug Policy and Alliance (2021). Safety First: Real Drug Education for
23, 311–319. doi: 10.1590/1983-80422015232070 Teens. Available online at: https://drugpolicy.org/resource/safety-first-real-
Bossong, M. G., van Hell, H. H., Jager, G., Kahn, R. S., Ramsey, N. F., drug-education-teens [accessed on Sep. 8, 2021].
and Jansma, J. M. (2013). The endocannabinoid system and emotional D’Souza, D. C., Ranganathan, M., Braley, G., Gueorguieva, R., Zimolo, Z., Cooper,
processing: a pharmacological fMRI study with 19-tetrahydrocannabinol. Eur. T., et al. (2008). Blunted psychotomimetic and amnestic effects of delta-9-
Neuropsychopharmacol. 23, 1687–1697. doi: 10.1016/j.euroneuro.2013.06.00 tetrahydrocannabinol in frequent users of cannabis. Neuropsychopharmacology
Botvin, G. J., and Botvin, E. M. (1992). Adolescent tobacco, alcohol, and drug 33, 2505–2516. doi: 10.1038/sj.npp.1301643
abuse: prevention strategies, empirical findings, and assessment issues. JDBP Epstein, J., Noel, J., Finnegan, M., and Watkins, K. (2016). Bacon Brains: Video
13, 290–301. Games for Teaching the Science of Addiction. J. Child Adolesc. Subst. Abuse 25,
Brown, S. A., Tapert, S. F., Granholm, E., and Delis, D. C. (2000). Neurocognitive 504–515. doi: 10.1080/1067828X.2015.1103348
functioning of adolescents: effects of protracted alcohol use. Alcoholism Clin. Ernst, M. (2014). The triadic model perspective for the study of adolescent
Exp. Res. 24, 164–171. doi: 10.1111/j.1530-0277.2000.tb04586.x motivated behavior. Brain Cogn. 89, 104–111. doi: 10.1016/j.bandc.2014.01.006
Bruer, J. T. (1997). Education and the brain: a bridge too far. Educat. Res. 26, 4–16. Faggiano, F., Minozzi, S., Versino, E., and Buscemi, D. (2014). Universal
doi: 10.3389/fpsyg.2016.00377 school-based prevention for illicit drug use. Cochrane Datab. System. Rev.
Cardoso, L. R. D., and Malbergier, A. (2014). Problemas escolares e o consumo de 2014:CD003020. doi: 10.1002/14651858.CD003020.pub3
álcool e outras drogas entre adolescentes. Psicol. Escolar Educacional 18, 27–34. Faggiano, F., Vigna-Taglianti, F. D., Versino, E., Zambon, A., Borraccino, A., and
doi: 10.1590/S1413-85572014000100003 Lemma, P. (2005). School-based prevention for illicit drugs’. Cochrane Datab.
Carney, T., Myers, B. J., Louw, J., and Okwundu, C. I. (2016). Brief System. Rev. 18:CD003020. doi: 10.1002/14651858.CD003020.pub2
school-based interventions and behavioural outcomes for substance-using Faggiano, F., Vigna-Taglianti, F., Burkhart, G., Bohrn, K., Cuomo, L., Gregori, D.,
adolescents. Cochrane Datab. System. Rev. 2016:CD008969. doi: 10.1002/ et al. (2010). The effectiveness of a school-based substance abuse prevention
14651858.CD008969.pub3 program: 18-month follow-up of the EU-Dap cluster randomized controlled
Chaffee, B. W., Cheng, J., Couch, E. T., Hoeft, K. S., and Halpern-Felsher, trial. Drug Alcohol Depend. 108, 56–64. doi: 10.1016/j.drugalcdep.2009.
B. (2021). Adolescents’ Substance Use and Physical Activity Before and 11.018
During the COVID-19 Pandemic. JAMA Pediatr. 175, 715–722. doi: 10.1001/ Fischhoff, B. (2013). The sciences of science communication. Proc. Natl. Acad. Sci.
jamapediatrics.2021.0541 U S A. 110, 14033–14039. doi: 10.1073/pnas.1213273110

Frontiers in Human Neuroscience | www.frontiersin.org 6 May 2022 | Volume 16 | Article 782205

Machado do Vale et al. Neuroscience Outside the Box

Flay, B. R., Hu, F. B., Siddiqui, O., Day, L. E., and Sussman, S. (1994). Differential LeNoue, S. R., and Riggs, P. D. (2016). Substance Abuse Prevention. Child Adolesc.
influence of parental smoking and friends’ smoking on adolescent initiation Psychiatr. Clin. North Am. 25, 297–305. doi: 10.1016/j.chc.2015.11.007
and escalation of smoking. J. Health Soc. Behav. 35, 248–265. doi: 10.2307/213 Leslie, F. M. (2020). Unique, long-term effects of nicotine on adolescent brain.
7279 Pharmacol. Biochem. Behav. 197:173010. doi: 10.1016/j.pbb.2020.173010
Fletcher, A., Bonell, C., and Hargreaves, J. (2008). School effects on young Lichtenberg, N. T., Thompson, A. B., Iguchi, M. Y., Evans, C. J., and Romero-
people’s drug use: a systematic review of intervention and observational studies. Calderón, R. (2020). An Undergraduate Student-Led Neuroscience Outreach
J. Adolesc. Health 42, 209–220. doi: 10.1016/j.jadohealth.2007.09.020 Program Shows Promise in Shifting Teen Attitudes About Drugs. J. Int. Mind
Forster, M., Grigsby, T. J., Rogers, C. J., and Benjamin, S. M. (2018). Brain Educat. Soc. 14, 387–399. doi: 10.1111/mbe.12261
The relationship between family-based adverse childhood experiences and Lilienfeld, S. O., and Arkowitz, A. (2014). Just Say No? Scientif. Am. Mind 25,
substance use behaviors among a diverse sample of college students. Addict. 70–71. doi: 10.1038/scientificamericanmind0114-70
Behav. 76, 298–304. doi: 10.1016/j.addbeh.2017.08.037 MacArthur, G., Caldwell, D. M., Redmore, J., Watkins, S. H., Kipping, R., White,
Fowler, J. S., Volkow, N. D., Kassed, C. A., and Chang, L. (2007). Imaging the J., et al. (2018). Individual-, family-, and school-level interventions targeting
addicted human brain. Sci. Pract. Perspect. 3, 4–16. doi: 10.1151/spp07324 multiple risk behaviours in young people. Cochrane Datab. System. Rev.
Fuhrmann, D., Knoll, L. J., and Blakemore, S. J. (2015). Adolescence as a Sensitive 10:CD009927. doi: 10.1002/14651858.CD009927.pub2
Period of Brain Development. Trends Cogn. Sci. 19, 558–566. doi: 10.1016/j.tics. Márquez, M. C., and Porras, A. M. (2020). Science Communication in Multiple
2015.07.008 Languages Is Critical to Its Effectiveness. Front. Commun. 5:31. doi: 10.3389/
Galvão, A., Pinheiro, M., Gomes, M. J., and Ala, S. (2017). Ansiedade, stress e fcomm.2020.00031
depressão relacionados com perturbações do sono-vigília e consumo de álcool. Mays, D., Gilman, S. E., Rende, R., Luta, G., Tercyak, K. P., and Niaura, R. S. (2014).
Rev. Portug. Enferm. Saúde Mental 5, 8–12. doi: 10.19131/rpesm.0160 Parental Smoking Exposure and Adolescent Smoking Trajectories. Pediatrics
Gilligan, C., Wolfenden, L., Foxcroft, D. R., Williams, A. J., Kingsland, M., Hodder, 133, 983–991. doi: 10.1542/peds.2013-3003
R. K., et al. (2019). Family-based prevention programmes for alcohol use McHugh, R. K., and Weiss, R. D. (2019). Alcohol Use Disorder and Depressive
in young people. Cochrane Datab. System. Rev. 3:CD012287. doi: 10.1002/ Disorders. Alcohol Res. 40:arcr.v40.1.01. doi: 10.35946/arcr.v40.1.01
14651858.CD012287.pub2 Meier, M. H., Caspi, A., Ambler, A., Harrington, H., Houts, R., Keefe, R. S.,
Glei, D. A., and Preston, S. H. (2020). Estimating the impact of drug use on et al. (2012). Persistent cannabis users show neuropsychological decline from
US mortality, 1999-2016. PLoS One 15:e0226732. doi: 10.1371/journal.pone. childhood to midlife. Proc. Natl. Acad. Sci. U S A. 109, E2657–E2664. doi:
0226732 10.1073/pnas.1206820109
Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, Miller, L., Moreno, J., Willcockson, I., Smith, D., and Mayes, J. (2006). An online,
A. C., et al. (2004). Dynamic mapping of human cortical development during interactive approach to teaching neuroscience to adolescents. CBE Life Sci.
childhood through early adulthood. Proc. Natl. Acad. Sci. U S A. 101, 8174– Educat. 5, 137–143. doi: 10.1187/cbe.05-08-0115
8179. doi: 10.1073/pnas.0402680101 Mills, J., and Wonoprabowo, L. (2020). Primary Care-Based Interventions to
Gould, T. J., and Leach, P. T. (2014). Cellular, molecular, and genetic substrates Prevent Illicit Drug Use in Children. Am. Fam. Phys. 102, 493–494.
underlying the impact of nicotine on learning. Neurobiol. Learn. Mem. 107, Olfson, M., Crystal, S., Wall, M., Wang, S., Liu, S. M., and Blanco, C. (2018).
108–132. doi: 10.1016/j.nlm.2013.08.004 Causes of death after nonfatal opioid overdose [published correction appears
Henkel, D. (2011). Unemployment and substance use: a review of the in JAMA Psychiatry. 2018;75:867]. JAMA Psychiatry 75, 820–827. doi: 10.1001/
literature (1990-2010). Curr. Drug Abuse Rev. 4, 4–27. doi: 10.2174/ jamapsychiatry.2018.1471
1874473711104010004 Owens, M. M., McNally, S., Petker, T., Amlung, M. T., Balodis, I. M., Sweet,
Hill, K. G., Hawkins, J. D., Catalano, R. F., Abbott, R. D., and Guo, J. (2005). Family L. H., et al. (2019). Urinary tetrahydrocannabinol is associated with poorer
influences on the risk of daily smoking initiation. J. Adolesc. Health 37, 202–210. working memory performance and alterations in associated brain activity.
doi: 10.1016/j.jadohealth.2004.08.014 Neuropsychopharmacology 44, 613–619. doi: 10.1038/s41386-018-0240-4
Horvath, J. C., and Donoghue, G. M. (2016). A Bridge Too Far - Revisited: Pan, W., and Bai, H. (2009). A multivariate approach to a meta-analytic review of
Reframing Bruer’s Neuroeducation Argument for Modern Science of Learning the effectiveness of the D.A.R.E. program. Int. J. Environ. Res. Publ. Health 6,
Practitioners. Front. Psychol. 7:377. 267–277. doi: 10.3390/ijerph6010267
Howard-Jones, P. A., and Fenton, K. (2012). The Need for Interdisciplinary Petker, T., Owens, M. M., Amlung, M. T., Oshri, A., Sweet, L. H., and MacKillop, J.
Dialogue in Developing Ethical Approaches to Neuroeducational Research. (2019). Cannabis involvement and neuropsychological performance: findings
Neuroethics 5, 119–134. doi: 10.1080/00219266.2020.1757489 from the Human Connectome Project. JPN 44, 414–422. doi: 10.1503/jpn.
Kapitány-Fövény, M., Vagdalt, E., Ruttkay, Z., Urbán, R., Richman, M. J., and 180115
Demetrovics, Z. (2018). Potential of an Interactive Drug Prevention Mobile Ramaekers, J. G., Kauert, G., Theunissen, E. L., Toennes, S. W., and Moeller,
Phone App (Once Upon a High): Questionnaire Study Among Students. JMIR M. R. (2009). Neurocognitive performance during acute THC intoxication in
Ser. Games 6:e19. doi: 10.2196/games.9944 heavy and occasional cannabis users. J. Psychopharmacol. 23, 266–277. doi:
Kim, M. J., Fleming, C. B., and Catalano, R. F. (2009). Individual and social 10.1177/0269881108092393
influences on progression to daily smoking during adolescence. Pediatrics 124, Rehan, W., Antfolk, J., Johansson, A., Jern, P., and Santtila, P. (2017). Experiences
895–902. doi: 10.1542/peds.2008-2015 of severe childhood maltreatment, depression, anxiety and alcohol abuse among
Kim, Y. H. (2017). Associations of adverse childhood experiences with depression adults in Finland. PLoS One 12:e0177252. doi: 10.1371/journal.pone.0177252
and alcohol abuse among Korean college students. Child Abuse Negl. 67, Roche, J., Bell, L., Galvão, C., Golumbic, Y. N., Kloetzer, L., Knoben, N.,
338–348. doi: 10.1016/j.chiabu.2017.03.009 et al. (2020). Citizen Science, Education, and Learning: Challenges and
Klisch, Y., Bowling, K. G., Miller, L. M., and Ramos, M. A. (2013). The impact of Opportunities. Front. Sociol. 5:613814. doi: 10.3389/fsoc.2020.613814
science education games on prescription drug abuse attitudes among teens: a Ryan, S. M., Jorm, A. F., and Lubman, D. I. (2010). Parenting factors associated
case study. J. Drug Educat. 43, 255–275. doi: 10.2190/DE.43.3.d with reduced adolescent alcohol use: a systematic review of longitudinal studies.
Laranjeira, R., Madruga, C. S., Pinsky, I., Caetano, R., Ribeiro, M., Mitsuhiro, S. Austral. N. Zeal. J. Psych. 44, 774–783. doi: 10.1080/00048674.2010.501759
II, et al. (2012). Ronaldo Laranjeira (Supervisão) [et al.]. São Paulo: Instituto Sanchez, Z. M., Valente, J. Y., Gusmões, J., Ferreira-Junior, V., Caetano, S. C.,
Nacional de Ciência e Tecnologia para Políticas Públicas de Álcool e Outras Cogo-Moreira, H., et al. (2021). Effectiveness of a school-based substance use
Drogas (INPAD). prevention program taught by police officers in Brazil: Two cluster randomized
Lemgruber, J., Telles, A. C., Neder, R., Borges, D., Vargas, K., Siracusa, M. et al. controlled trials of the PROERD. Int. J. Drug Policy 98:103413. doi: 10.1016/j.
(2021). Um tiro no pé: Impactos da proibição das drogas no orçamento do drugpo.2021.103413
sistema de justiça criminal do Rio de Janeiro e São Paulo. Relatório da primeira Secades-Villa, R., Garcia-Rodríguez, O., Jin, C. J., Wang, S., and Blanco, C. (2015).
etapa do projeto “Drogas: Quanto custa proibir, et al Edn. Rio de Janeiro: Probability and predictors of the cannabis gateway effect: a national study. Int.
CESeC, março de. J. Drug Policy 26, 135–142. doi: 10.1016/j.drugpo.2014.07.011

Frontiers in Human Neuroscience | www.frontiersin.org 7 May 2022 | Volume 16 | Article 782205

Machado do Vale et al. Neuroscience Outside the Box

Shek, D., Zhu, X., Dou, D., and Chai, W. (2020). Influence of Family Factors US Department of Health and Human Services (2016). E-cigarette Use Among
on Substance Use in Early Adolescents: A Longitudinal Study in Hong Kong. Youth and Young Adults: A Report of the Surgeon General pdf icon
J. Psychoact. Drugs 52, 66–76. doi: 10.1080/02791072.2019.1707333 [PDF – 8.47MB]. Atlanta, GA: US Department of Health and Human
Sigman, M., Peña, M., Goldin, A. P., and Ribeiro, S. (2014). Neuroscience and Services.
education: prime time to build the bridge. Nat. Neurosci. 17, 497–502. doi: Valentine, G., and Sofuoglu, M. (2018). Cognitive Effects of Nicotine:
10.1038/nn.3672 Recent Progress. Curr. Neuropharmacol. 16, 403–414. doi: 10.2174/
Silva, M. C. A. (2016). O papel da escola nas ações preventivas relacionadas ao 1570159X15666171103152136
uso de álcool e outras drogas por alunos do Ensino Fundamental I. Revista Valkov, P. (2018). School Dropout and Substance Use: Consequence
Eletrônica de Sauìde Mental Aìlcool e Drogas. 12, 30–39. doi: 10.11606/issn. or Predictor? Trakia J. Sci. 16, 95–101. doi: 10.15547/tjs.2018.02.
1806-6976.v12i1p30-39 004
Smit, K., Voogt, C., Hiemstra, M., Kleinjan, M., Otten, R., and Kuntsche, E. (2018). Vasters, G. P., and Pillon, S. C. (2011). Drugs use by adolescents and their
Development of alcohol expectancies and early alcohol use in children and perceptions about specialized treatment adherence and dropout. Rev. Latino
adolescents: A systematic review. Clin. Psychol. Rev. 60, 136–146. doi: 10.1016/ Am. Enfermagem 19, 317–324. doi: 10.1590/s0104-11692011000200013
j.cpr.2018.02.002 Willoughby, T., Good, M., Adachi, P. J., Hamza, C., and Tavernier, R. (2013).
Squeglia, L. M., Pulido, C., Wetherill, R. R., Jacobus, J., Brown, G. G., and Tapert, Examining the link between adolescent brain development and risk-taking from
S. F. (2012). Brain response to working memory over three years of adolescence: a social-developmental perspective. Brain Cogn. 83, 315–323. doi: 10.1016/j.
influence of initiating heavy drinking. J. Stud. Alcohol Drugs 73, 749–760. doi: bandc.2013.09.008
10.15288/jsad.2012.73.749 World Health Organization [WHO] (2004). Neuroscience of Psychoactive Substance
Squeglia, L. M., Tapert, S. F., Sullivan, E. V., Jacobus, J., Meloy, M. J., Rohlfing, T., Use and Dependence. Geneva: World Health Organization.
et al. (2015). Brain development in heavy-drinking adolescents. Am. J. Psych. World Health Organization [WHO] (2014). Health for the World’s Adolescents: A
172, 531–542. doi: 10.1176/appi.ajp.2015.14101249 Second Chance in the Second Decade. Available online at: http://apps.who.int/
Stapinski, L. A., Reda, B., Newton, N. C., Lawler, S., Rodriguez, D., Chapman, C., adolescent/second-decade/. [accessed on Aug 24, 2021]
et al. (2018). Development and evaluation of ’Pure Rush’: An online serious Zarrindast, M. R., and Khakpai, F. (2019). The modulatory role of nicotine on
game for drug education. Drug Alcohol Rev. 37, S420–S428. doi: 10.1111/dar. cognitive and non-cognitive functions. Brain Res. 1710, 92–101. doi: 10.1016/
12611 j.brainres.2018.12.002
Tapert, S. F., and Schweinsburg, A. D. (2005). The human adolescent brain and
alcohol use disorders. Recent Dev. Alcohol 17, 177–197. doi: 10.1007/0-306- Conflict of Interest: The authors declare that the research was conducted in the
48626-1_9 absence of any commercial or financial relationships that could be construed as a
Theunissen, E. L., Kauert, G. F., Toennes, S. W., Moeller, M. R., Sambeth, A., potential conflict of interest.
Blanchard, M. M., et al. (2012). Neurophysiological functioning of occasional
and heavy cannabis users during THC intoxication. Psychopharmacology 220, Publisher’s Note: All claims expressed in this article are solely those of the authors
341–350. doi: 10.1007/s00213-011-2479-x and do not necessarily represent those of their affiliated organizations, or those of
Tice, P., Lipari, R. N., and Van Horn, S. L. (2017). “Substance use among 12th grade the publisher, the editors and the reviewers. Any product that may be evaluated in
aged youths, by dropout status,” in The CBHSQ Report, ed. SAMHSA (Rockville, this article, or claim that may be made by its manufacturer, is not guaranteed or
MD: Center for Behavioral Health Statistics and Quality). endorsed by the publisher.
Tyng, C. M., Amin, H. U., Saad, M., and Malik, A. S. (2017). The Influences of
Emotion on Learning and Memory. Front. Psychol. 8:1454. doi: 10.3389/fpsyg. Copyright © 2022 Machado do Vale, da Silva Chagas, de Souza Pereira, Giestal-
2017.01454 de-Araujo, Arévalo and Oliveira-Silva Bomfim. This is an open-access article
UNESCO, UNODC and WHO (2017). Good Policy and Practice in Health distributed under the terms of the Creative Commons Attribution License (CC BY).
Education: Education sector responses to the use of alcohol, tobacco and drugs. The use, distribution or reproduction in other forums is permitted, provided the
Geneva: World Health Organization. original author(s) and the copyright owner(s) are credited and that the original
UNODC (2021). World Drug and Report 2021. United Nations Publication, publication in this journal is cited, in accordance with accepted academic practice.
Sales No.E.21.XI.8). Available online at: https://www.unodc.org/unodc/en/data- No use, distribution or reproduction is permitted which does not comply with
andanalysis/wdr2021.html (accessed August 20, 2021). these terms.

Frontiers in Human Neuroscience | www.frontiersin.org 8 May 2022 | Volume 16 | Article 782205