Elsevier

Psychoneuroendocrinology

Volume 88, February 2018, Pages 24-37
Psychoneuroendocrinology

Review
The role of trauma in the hormonal interplay of cortisol, testosterone, and oxytocin in adolescent aggression

https://doi.org/10.1016/j.psyneuen.2017.11.005Get rights and content

Highlights

  • Cortisol, testosterone, and oxytocin interact with each other.

  • Timing of trauma leads to distinct hormonal patterns.

  • We propose that timing of trauma affects the hormonal interplay in aggression.

  • The model is influenced by gender and type of aggression.

  • Our model contributes to a more accurate neuroendocrine profile of aggression.

Abstract

Although numerous studies have examined the neuroendocrinology of aggression, the findings are mixed and focused on cortisol and testosterone. We argue that past findings remain inconclusive partly because the key roles of oxytocin and trauma have not been systematically integrated yet. Oxytocin is associated with social behavior and interacts with cortisol and testosterone, whereas trauma is a crucial risk factor of aggression that strongly affects hormonal activity. In this review, we investigate the role of trauma in the hormonal interplay of cortisol, testosterone, and oxytocin in aggression during adolescence. We first discuss how these hormones interact with each other and how trauma influences these interactions and then we propose a model that highlights the role of trauma in the hormonal interplay in aggression. We suggest that the timing of trauma has a distinct effect on hormonal activity and it should be integrated into any comprehensive model. Current trauma is linked to different levels of oxytocin, cortisol, testosterone, and testosterone/cortisol ratio than childhood trauma, but this distinction is also influenced by gender and type of aggression. We conclude that in order to better understand the neuroendocrinology of aggression, it is crucial to incorporate the investigation of oxytocin and trauma in future research.

Introduction

Cumulative scientific evidence has shown that aggressive behavior is linked to abnormal hormonal levels, most notably lower levels of cortisol and higher levels of testosterone (Yildirim and Derksen, 2012a, Yildirim and Derksen, 2012b). However, empirical findings have also shown conflicting relations, depending on additional other factors including type of aggression, age, the presence of callous-unemotional (CU) traits, and methodological variations (Barzman et al., 2010, Cima et al., 2008, Gao et al., 2009, Herpers et al., 2014). This line of research has provided insight into the psychophysiology of aggression, but it suffers from several shortcomings.

The most notable problem is the conceptual complexity of aggression. Aggression is an umbrella term that generally refers to behaviors that aim to cause physical or psychological pain/harm to another individual or destruction/damage of an entity, but the construct of aggression is far more complicated (Tremblay et al., 2005). Aggression comprises a plethora of different types, including overt and covert aggression, reactive and proactive aggression, impulsive aggression, delinquent behavior, pathological forms of aggression, like oppositional-defiant disorder (ODD), conduct disorder (CD), antisocial personality disorder, and psychopathy or CU traits (APA, 2013, Tremblay et al., 2005). These different types play a key role in the inconsistent findings and incomparability among studies. In addition, research has mainly focused on cortisol and testosterone, ignoring the potential role of oxytocin, a neuropeptide that is strongly associated with social-affective behaviors. Moreover, the variables that have been investigated in order to elucidate the conflicting findings were limited and did not systematically include crucial and complex factors that are consistently related to both aggression and hormonal activity, most importantly, history of trauma.

To elaborate on the first issue, oxytocin is a neuropeptide that has been widely investigated for its role in social-affective behaviors, including social affiliation, pair bonding, emotional recognition, trust, empathy, and attachment, all of which are impaired in aggressive individuals (Campbell, 2008, Campbell, 2010, Lee et al., 2009a, Veening and Olivier, 2013). Oxytocin is also related to cortisol and testosterone in several social behaviors. Specifically, even though cortisol is the most commonly examined stress hormone, oxytocin is also altered under physiological and psychological stressors, both in plasma concentrations and several brain regions (animals: Engelmann et al., 2004, Neumann, 2002; humans: Lee et al., 2009a). The release of oxytocin leads to the decrease of cortisol levels in order to reduce stress (Cardoso et al., 2014). Additionally, oxytocin has the opposite effects of testosterone on the same cognitive and behavioral phenotypes, such as threat response, empathy, and trust (Crespi, 2016). For instance, testosterone administration reduces empathy and trust, whereas oxytocin administration reinforces these behaviors (Crespi, 2016). We argue that oxytocin, in interaction with cortisol and testosterone, also plays a pivotal role in regulating aggressive behavior.

With respect to the role of trauma, previous studies have not systematically taken into account the potential role of trauma in relation to abnormal hormonal activity in aggressive individuals. Childhood trauma is predictive of persistent aggression and offending and antisocial adolescents have usually experienced multiple traumas, such as loss and bereavement, domestic violence, physical and emotional maltreatment, abuse, and neglect (Dierkhising et al., 2013, Fox et al., 2015, Foy et al., 2012, Jonson-Reid et al., 2010, Kotch et al., 2008, Steiner et al., 2011, Wilson et al., 2009). Additionally, hormone production and secretion are substantially influenced by early social experiences long before the manifestation of aggressive behavior. It has been proposed that early negative social experiences change sensitivity to neuropeptides and steroids by reorganization of receptors or alterations in hormone production and secretion that in turn influence social behaviors (Cushing and Kramer, 2005). In humans, trauma is a multifaceted construct with acute and chronic effects that lead to distinct alterations in the brain and the neuroendocrine systems (Cushing and Kramer, 2005, Teicher et al., 2003). Therefore, the hormonal alterations caused by trauma might interfere with the unique neuroendocrine profile of aggression leading to the observed conflicting findings. In sum, traumatic experiences are of paramount importance in our effort to disentangle the psychophysiology of aggression not only due to their high prevalence rates in antisocial and delinquent individuals but also due to their effect on hormonal activity.

The aim of this review is to address these issues and present a model based on the neuroendocrine findings of the hormonal interplay between cortisol, testosterone, and oxytocin as well as their relation to trauma. First, a brief description of the endocrinological changes in adolescence and the relation of cortisol and testosterone with aggression are presented. Since previous reviews and meta-analyses have already thoroughly discussed this topic and the aim of the current review is to focus on the interplay among these hormones and the role of trauma, it is outside the scope of this review to repeat the findings of the separate effects of these hormones in detail (e.g., Hawes et al., 2009, Yildirim and Derksen, 2012a, Yildirim and Derksen, 2012b). Second, we review in more detail the evidence on the association between oxytocin and aggression. Third, we discuss in detail the interactions among these hormones followed by their association with trauma. Due to the limited number of studies examining the interaction among all three hormones, we also include studies that focused on the interaction between two of the three hormones. We finally integrate previous findings in a model presenting how the presence and timing of trauma influences the hormonal interplay of these hormones in aggression. The model is followed by a critical discussion of its strengths, limitations, and clinical relevance. We focus on findings in adolescence, because it is a unique developmental period with significant hormonal and maturational changes as well as high prevalent rates of aggression (Bramen et al., 2011, Merikangas et al., 2010, Shirtcliff et al., 2012, Shirtcliff et al., 2009a).

Given the scarce evidence on the relation between oxytocin and aggression or trauma in adolescence, we also discuss adult and children studies for oxytocin in an effort to shed light on its hormonal activity and interplay. Finally, several types of aggression have been examined in relation to hormonal secretion but due to the limited research on the specific hormonal interactions under investigation, we included studies that examined various types of aggression and we did not focus on one explicit type of aggression. Specifically, we included conduct disorder, antisocial personality disorder, offending, psychopathy, and aggression provocation in healthy samples. We also included Attention-Deficit Hyperactivity Disorder (ADHD) due to the impulsive aggressive outbursts often observed in youth with ADHD as well as the high comorbidity with conduct disorder (APA, 2013). As described above, these types have conceptual and behavioural differences and distinct characteristics, which might lead to distinct neuroendocrine profiles that will be taken into account in the model.

Although the aim of this review is to focus on the hormonal interplay in relation to trauma, there are several other factors that are associated with aggression and might influence its neuroendocrine profile that need to be acknowledged. For instance, alcohol and drug use is a well-known risk factor of aggression and delinquency (Assink et al., 2015, Hoaken and Stewart, 2003, Lundholm et al., 2013) and substance use disorders are often comorbid with antisocial personality disorder (Hasin and Kilcoyne, 2012). Relatedly, externalizing problems in adolescence are usually accompanied with symptoms of anxiety and depression (Hill, 2002). Despite its indisputable importance, the role of comorbidity in the neuroendocrine profile of aggression in relation to trauma is outside of the scope of this review as previous research examining all the aforementioned factors is considerably scarce.

Section snippets

Endocrine changes in adolescence

Adolescence is a unique developmental period characterized by substantial neurobiological, physiological, and psychological changes. In relation to the endocrine system, hormonal changes in the Hypothalamic-Pituitary-Adrenal (HPA) axis and the Hypothalamic-Pituitary-Gonadal (HPG) occur during puberty in adolescence (Gunnar and Vazquez, 2015, Shirtcliff et al., 2012, Shirtcliff et al., 2009a, Shirtcliff et al., 2009b). Previous research has shown that HPA activity increases in adolescence with

Cortisol and aggression

Cortisol is a glucocorticoid hormone and the end product of the Hypothalamus-Pituitary-Adrenal (HPA) axis. The HPA axis is the hormonal response system activated in the presence of mental and physical stressors (Johnson et al., 1992). The stress response consists of three steps: neurons in the paraventricular nucleus of hypothalamus secrete corticotrophin-releasing hormone (CRH), CRH goes to the anterior pituitary gland which produces adrenocortocotropin hormone (ACTH), and ACTH signal travels

Testosterone/Cortisol ratio

An area of study that has received increased attention is the association between testosterone and cortisol in aggression. It has been proposed that high testosterone levels in combination with low cortisol levels might be predictive of aggressive behavior (Terburg et al., 2009). This model suggests that a high testosterone to cortisol (T/C) ratio leads to increased attention to threatening cues, low sensitivity to stress, decreased emotional recognition, and a salience of dominance and

The effect of trauma

Although the aforementioned findings have contributed to our understanding of the neuroendocrinology of aggression, the findings of cortisol, oxytocin, and the testosterone/cortisol ratio in relation to aggression are still mixed. We argue that the observed inconsistencies might derive from the presence of trauma, which is highly prevalent in aggressive individuals and it affects the hormonal activity (Cushing and Kramer, 2005, De Bellis and Zisk, 2014, Fox et al., 2015). The psychological

The model

The evidence reviewed so far presents a rather complicated picture that makes it imperative to integrate all the information into a meaningful and comprehensive model in order to piece together all the findings. We suggest that a comprehensive model can help us not only better understand the different and seemingly contradictory findings but also guide future research in a theoretically meaningful direction. We thus propose a model that specifies how the hormonal interplay in aggression might

Strengths and limitations

In this review, we presented the existing evidence on the associations between oxytocin, cortisol, testosterone, aggression, and trauma and introduced a model that describes the role of current or childhood trauma in the hormonal interplay underlying aggression. First, we added the potential role of oxytocin in aggression, extending existing models that specify high testosterone/cortisol ratio in aggression. Second, we reviewed the interplay between these three hormones, focusing on aggression

Future directions and clinical relevance

Our proposed model is built upon existing empirical evidence but it also highlights the gaps in research. Part of our goal in pulling together this body of data and proposing a concrete, testable model, is to urge future research forward; specifically research that investigates our hypotheses about the role of oxytocin in the development of aggression and explores its association with cortisol and testosterone. We argue that these hormones are highly interconnected and investigating them in

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Acknowledgment

No acknowledgment.

References (201)

  • L.L. Carpenter et al.

    Decreased adrenocorticotropic hormone and cortisol responses to stress in healthy adults reporting significant childhood maltreatment

    Biol. Psychiatry

    (2007)
  • L.L. Carpenter et al.

    Effect of childhood emotional abuse and age on cortisol responsivity in adulthood

    Biol. Psychiatry

    (2009)
  • J.M. Carre et al.

    Social neuroendocrinology of human aggression: examining the role of competition-induced testosterone dynamics

    Neuroscience

    (2015)
  • J.M. Carre et al.

    The social neuroendocrinology of human aggression

    Psychoneuroendocrinology

    (2011)
  • M. Cima et al.

    Distinct characteristics of psychopathy relate to different subtypes of aggression

    Personal. Ind. Diff.

    (2009)
  • M. Cima et al.

    Self-reported trauma, cortisol levels, and aggression in psychopathic and non-psychopathic prison inmates

    Biol. Psychol.

    (2008)
  • B.S. Cushing et al.

    Mechanisms underlying epigenetic effects of early social experience: the role of neuropeptides and steroids

    Neurosci. Biobehav. Rev.

    (2005)
  • J. Deardorff et al.

    Father absence, body mass index, and pubertal timing in girls: differential effects by family income and ethnicity

    J. Adolesc. Health

    (2011)
  • M.D. De Bellis et al.

    Developmental traumatology part I: biological stress systems

    Biol. Psychiatry

    (1999)
  • M.D. De Bellis et al.

    The biological effects of childhood trauma

    Child Adolesc Psychiatr Clin N Am

    (2014)
  • T.F. Denson et al.

    Endogenous testosterone and cortisol jointly influence reactive aggression in women

    Psychoneuroendocrinology

    (2013)
  • J.R. Doom et al.

    Child maltreatment and gender interactions as predictors of differential neuroendocrine profiles

    Psychoneuroendocrinology

    (2013)
  • C. Eisenegger et al.

    The role of testosterone in social interaction

    Trends Cogn. Sci.

    (2011)
  • B.M. Elzinga et al.

    Diminished cortisol responses to psychosocial stress associated with lifetime adverse events A study among healthy young subjects

    Psychoneuroendocrinology

    (2008)
  • M. Engelmann et al.

    The hypothalamic–neurohypophysial system regulates the hypothalamic–pituitary–adrenal axis under stress: an old concept revisited

    Front. Neuroendocrinol.

    (2004)
  • J. Feilhauer et al.

    Salivary cortisol and psychopathy dimensions in detained antisocial adolescents

    Psychoneuroendocrinology

    (2013)
  • S.O. Fetissov et al.

    Aggressive behavior linked to corticotropin-reactive autoantibodies

    Biol. Psychiatry

    (2006)
  • J.C. Flanagan et al.

    Effects of adverse childhood experiences on the association between intranasal oxytocin and social stress reactivity among individuals with cocaine dependence

    Psychiatry Res.

    (2015)
  • B.H. Fox et al.

    Trauma changes everything: examining the relationship between adverse childhood experiences and serious, violent and chronic juvenile offenders

    Child Abuse Negl.

    (2015)
  • S.N. Geniole et al.

    Effects of competition outcome on testosterone concentrations in humans: an updated meta-analysis

    Hormones Behav.

    (2017)
  • S.N. Geniole et al.

    Testosterone dynamics and psychopathic personality traits independently predict antagonistic behavior towards the perceived loser of a competitive interaction

    Horm. Behav.

    (2013)
  • S.N. Geniole et al.

    State, not trait, neuroendocrine function predicts costly reactive aggression in men after social exclusion and inclusion

    Biol. Psychol.

    (2011)
  • G. Gerra et al.

    Neurotransmitter-neuroendocrine responses to experimentally induced aggression in humans: influence of personality variable

    Psychiatry Res.

    (1997)
  • G. Gerra et al.

    Neurotransmitter-hormonal responses to psychological stress in peripubertal subjects: relationship to aggressive behavior

    Life Sci.

    (1998)
  • E.B. Gordis et al.

    Asymmetry between salivary cortisol and α-amylase reactivity to stress: relation to aggressive behavior in adolescents

    Psychoneuroendocrinology

    (2006)
  • A. Gossen et al.

    Oxytocin plasma concentrations after single intranasal oxytocin administration − a study in healthy men

    Neuropeptides

    (2012)
  • A.J. Gostisha et al.

    Beyond physiological hypoarousal: the role of life stress and callous-unemotional traits in incarcerated adolescent males

    Horm. Behav.

    (2014)
  • A.J. Guastella et al.

    Recommendations for the standardisation of oxytocin nasal administration and guidelines for its reporting in human research

    Psychoneuroendocrinology

    (2013)
  • P.E. Gustafsson et al.

    Does quantity have a quality all its own? Cumulative adversity and up-and down-regulation of circadian salivary cortisol levels in healthy children

    Psychoneuroendocrinology

    (2010)
  • P.N.S. Hoaken et al.

    Drugs of abuse and the elicitation of human aggressive behavior

    Addict. Behav.

    (2003)
  • S.G. Hofmann et al.

    Effect of intranasal oxytocin administration on psychiatric symptoms: a meta-analysis of placebo-controlled studies

    Psychiatry Res.

    (2015)
  • J.L. Alcorn et al.

    Effects of oxytocin on aggressive responding in healthy adult men

    Behav. Pharmacol.

    (2015)
  • J.L. Alcorn et al.

    Effects of intranasal oxytocin on aggressive responding in antisocial personality disorder

    Psychol. Rec.

    (2015)
  • L.R. Alink et al.

    Cortisol and externalizing behavior in children and adolescents: mixed meta-analytic evidence for the inverse relation of basal cortisol and cortisol reactivity with externalizing behavior

    Dev. Psychobiol.

    (2008)
  • American Psychiatric Association

    Diagnostic and Statistical Manual of Mental Disorders

    (2013)
  • B.Å Armelius et al.

    Cognitive-behavioral treatment for antisocial behavior in youth in residential treatment

    Cochrane Database Syst. Rev.

    (2007)
  • B. Auyeung et al.

    Prenatal and postnatal hormone effects on the human brain and cognition

    Pflugers Arch.

    (2013)
  • M.J. Bakermans-Kranenburg et al.

    Oxytocin decreases handgrip force in reaction to infant crying in females without harsh parenting experiences

    Soc. Cogn. Affect. Neurosci.

    (2011)
  • D.H. Barzman et al.

    Neuroendocrine aspects of pediatric aggression: can hormone measures be clinically useful?

    Neuropsych. Dis. Treatment

    (2010)
  • J. Belsky et al.

    Childhood experience, interpersonal development, and reproductive strategy: an evolutionary theory of socialization

    Child Dev.

    (1991)
  • Cited by (0)

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