Psychobiology of persistent antisocial behavior: Stress, early vulnerabilities and the attenuation hypothesis

doi:10.1016/j.neubiorev.2005.08.002

Neuroscience & Biobehavioral Reviews

Volume 30, Issue 3, 2006, Pages 376-389

https://doi.org/10.1016/j.neubiorev.2005.08.002 Get rights and content

Abstract

Stress experienced during the sensitive prenatal, postnatal and early childhood periods of brain development can have damaging consequences for developing biological systems. Stressors imposed by early physical vulnerabilities and an adverse care giving environment is proposed to set in motion early precursors of later persistent antisocial behavior. The purpose of this report is to present an integrated theoretical perspective of potential mechanisms involved in the development of persistent antisocial behavior with an emphasis on early stressors and the neuroendocrinology of stress. The attenuation of endocrine physiology of the stress system is considered a key mechanism involved in persistent antisocial behavior. The amygdala is considered a structure/process linking subjective experiences, emotional learning, brain development and stress physiology. Attenuated cortisol level subsequent to early vulnerabilities is considered a risk marker for persistent antisocial behavior.

Section snippets

Background of the problem

Stressors imposed by early physical vulnerabilities, such as genes, exposure to teratogenic substances, and an adverse care giving environment are proposed to set in motion early biological precursors of later disruptive and aggressive behavior. The problem is that the biological mechanisms involved in antisocial behavior remain unknown as the findings are disconnected and tend to examine one biological system at a time with little integration across systems. Thus, an opportunity to intervene

The stress system and antisocial behavior

Hypoarousal of the sympathetic nervous system (SNS) components of the stress system is related to antisocial behavior in vastly differing populations. In the 1980 s, Raine and Venables (1984) showed that antisocial subjects were characterized by lower tonic heart-rate levels. An interpretation of these findings was that lower heart rate levels in antisocial adolescents may reflect a vagal passive adaptation to mildly aversive events. Raine also showed that underarousal of both the central

Mechanisms of attenuation of the stress system and antisocial behavior

The theoretical perspective put forth is that inherited vulnerabilities and early life adversities predispose some children toward patterns of attenuation of arousal and these patterns are stable aspects of the psychobiology of persistent antisocial behavior. The stress system is proposed to mediate inherited vulnerabilities and nonoptimal conditions of child rearing through early learning and memory via the amydalar system and its extensive network of connections to the hypothalamus,

Amygdala

The amygdala is considered a key mediator of emotions (Davidson and Irwin, 1999, Joseph, 1999) and conditioning and extinction of fear. Therefore, it is proposed that the effects of the early environment are mediated, at least in part, by altering the degree of neural activity within the amygdala. This heterogeneous structure is involved in the modulation of neuroendocrine functions, visceral effector mechanisms, and complex patterns of integrated behavior including defense reactions,

Early learning

Learning theory suggests that fear is learned after a sufficient number of pairings of a neutral and conditioned stimulus (CS). Long-term changes are established in the brain, such that a CS begins to elicit behavioral, autonomic and endocrine responses that are usually associated with danger (LeDoux, 1986, LeDoux, 1996, LeDoux, 1998). Conditioned fear is an amygdala-dependent form of learning (Rogan et al., 1997). Fear extinction is considered to be influenced by similar principles of learning

Dynamic systems and structures

Any model that aims at contributing to understanding and explaining complex aggressive, delinquent and criminal behavior is by definition an integrated perspective that considers emotional, contextual and neurobiological processes (Magnusson and Cairns, 1996, Lerner, 1998, Lerner and Walls, 1999, Magnusson and Stattin, 1998, Magnusson, 1988, Magnusson, 1999, Magnusson et al., 1999, Susman and Rogol, 2004). At a general level, the holistic nature of neurodevelopmental processes implies that they

Conclusions

Integrated theories consider development as successive changes that entail structural biological change as well as dynamic functional changes in psychological capabilities (Hinde, 1987, Lerner, 1986, Lerner, 1998, Magnusson, 1988, Mayr, 1988, Susman, 1998). Absent in previous models, with Moffitt as the exception, were notions about the synchronization of neurophysiological processes with emotional, cognitive, and care giving contextual processes in the establishment and maintenance of

Acknowledgements

Thank you is extended to David Magnusson for his wise input to this manuscript. This report was made possible by a grant from the Swedish Council for Humanities and Social Sciences to David Magnusson for inviting Elizabeth J. Susman as a distinguished guest researcher to the Laboratory for Developmental Science at Stockholm University, Stockholm, Sweden.

References (138)

V. Arango et al.
Genetics of the serotenergic system in suicidal behavior
J. Psychiatr. Res.
(2003)
S. Brody
Age at first intercourse is inversely related to female cortisol stress reactivity
Psychoneuroendocrinology
(2002)
L. Cahill et al.
Mechanisms of emotional arousal and lasting declarative memory
Trends Neurosci.
(1998)
E.F. Coccaro et al.
Impulsive aggression in personality disorder correlates with platelet 5-HT-sub(2A) receptor binding
Neuropsychopharmacology
(1997)
M. Davis
Are different parts of the extended amygdala involved in fear versus anxiety?
Biol. Psychiatry
(1998)
M. Davis et al.
The role of glutamate and gamma-aminobutyric acid in fear extinction: Clinical implications for exposure therapy
Biol. Psychiatry
(2002)
J.S. DeOlmos
Amygdala
G. Gerra et al.
Aggressive responding in abstinent heroin addicts: Neuroendocrine and personality correlates
Prog. Neuropsychopahrmacol. Biol. Psychiatry
(2004)
M.R. Gunnar
Quality of early care and buffering of neuroendocrine stress reactions: Potential effects on the developing human brain
Prev. Med.: An Int. J.
(1998)
M.R. Gunnar et al.
Social regulation of the cortisol levels in early human development
Psychoneuroendocrinology
(2002)

P.C. Holland et al.

Amygdala circuitry in attentional and representational processes

Trends Cogn. Neurosci.

(1999)

E. Johnson et al.

Mechanisms of stress: A dynamic overview of hormonal and behavioral homeostasis

Neurosci. Biobehav.l Rev.

(1992)

J.P. Kemph et al.

Treatment of aggressive children with clonidine: Results of an open pilot study

J. Am. Acad. Child Adolesc. Psychiatry

(1993)

J.J. Lambert et al.

Neurosteroid modulation of GABAA receptors

Prog. Neurobiol.

(2003)

J.E. LeDoux

Fear and the brain: Where have we been, and where are we going?

Biol. Psychiatry

(1998)

R.M. Lerner

Theories of human development: Contemporary perspectives

S. Manuck et al.

Central nervous system serotonergic responsivity and aggressive disposition in men

Physiol. Beh.

(2002)

L. Matykiewicz et al.

Adjudicated adolescent males: Measures of urinary 5-hydroxyindoleacetic acid and reactive hypoglycemia

Personality and Individual Differences

(1997)

K. McBurnett et al.

Anxiety, inhibition, and conduct disorder in children: II. Relation to salivary cortisol

J. Am. Acad. Child Adol. Psychiatry

(1991)

J.L. McGaugh et al.

Neuromodulatory systems and memory storage: Role of the amygdala

Behav. Brain Res.

(1993)

K.A. Miczek et al.

Neurosteroids, GABAA receptors, and escalated aggressive behavior

Horm. Behav.

(2003)

T. Moffitt et al.

Whole blood serotonin relates to violence in an epidemiological sample

Biol. Psychiatry

(1998)

H.B. Moss et al.

Salivary cortisol responses and the risk for substance abuse in prepubertal boys

Biol. Psychiatry

(1995)

A.S. New et al.

Serotonergic function and self-injurious behavior in personality disorder patients

Psychiatry Res.

(1997)

D. Oyserman et al.

Influences of maternal mental illness on psychological outcomes for adolescent children.

J. Adolesc.

(2002)

A. Addell et al.

Comparitative study in the rat of the actions of different types of stress on the release of 5-HT in raphe nuclei and forebrain areas

Neuropharmacology

(1997)

B. Aguilar et al.

Distinguishing the early-onset/persistent and adolescence-onset antisocial behavior types: From birth to 16 years

Dev. Psychopathol.

(2000)

H. Als et al.

Early experience alters brain function and structure

Pediatrics

(2004)

B. Bergman et al.

Hormone levels and personality traits in abusive and suicidal male alcoholics

Alcohol. Clin. Exp. Res.

(1994)

A.J. Bond et al.

Tryptophan depletion increases aggression in women during the premenstrual phase

Psychopharmacology

(2001)

P.A. Brennan et al.

Psychophysiological protective factors for male subjects at high risk for criminal behavior

Am. J. Psychiatry

(1997)

P.A. Brennan et al.

Relationship of maternal smoking during pregnancy with criminal arrest and hospitalization for substance abuse in male and female adult offspring

Am. J. Psychiatry

(2002)

C. Buechel et al.

The functional anatomy of attention to visual motion: A functional MRI study

Brain

(1998)

R.B. Cairns et al.

Developmental behavior genetics: Fusion, correlated constraints, and timing

C. Caldji et al.

Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat

Proc. Natl. Acad. Sci.

(1998)

S.D. Calkins et al.

Physiological and behavioral regulation in two-year-old children with aggressive/destructive behavior problems.

J. Abnorm. Child Psychol.

(2000)

W.B. Cannon

The wisdom of the body

(1932)

A. Caspi et al.

Role of genotype in the cycle of violence in maltreated children

Science

(2002)

A. Caspi et al.

Influence of life stress on depression: Moderation by a polymorphism in the 5-HTT gene

Science

(2003)

D.R. Cherek et al.

Prolactin response to buspirone was reduced in violent compared to nonviolent parolees

Psychopharmacology

(1999)

G.P. Chrousos et al.

The concepts of stress and stress system disorders

J. Am. Med. Assoc.

(1992)

D. Cicchetti

Development and self-regulatory structures of the mind

Dev. Psychopathol.

(1994)

D. Cicchetti et al.

Failures in the expectable environment and their impact on individual development: The case of child maltreatment

H.M. Cleckley

The Mask of Sanity: An Attempt to Clarify Some Issues about the So-called Psychopathic Personality, Mosby

St Louis

(1976)

E.F. Coccaro et al.

Physiological responses to d-fenfluramine and ipsapirone challenge correlate with indices of aggression in males with personality disorder

Int. Clin. Psychopharmacol.

(1995)

J.N. Constantino et al.

CSF 5-HIAA and family history of antisocial personality disorder in newborns

Am. J. Psychiatry

(1997)

Crittenden, P.M., Danger and development: The organization of self-protective strategies, in: Vondra, J.I., Barnett, D....

K.M. Davidge et al.

Association of the serotonin transporter and 5HT1Dbeta receptor genes with extreme, persistent and pervasive aggressive behavior in children,

Psychiatr. Genet.

(2004)

J.M. Davidson et al.

The functional neuroanatomy of emotion and affective style

Trends Cognitive Neurosci.

(1999)

M. Davis

Pharmacological and anatomical analysis of fear conditioning using the fear-potentiated startle paradigm

Behav. Neurosci.

(1986)

Cited by (270)

Physiological response to pain in female adolescents with nonsuicidal self-injury as a function of severity
2023, Journal of Affective Disorders
Preliminary evidence indicates altered hypothalamic-pituitary-adrenal (HPA) axis and autonomic nervous system (ANS) response to experimental pain in individuals with nonsuicidal self-injury (NSSI). This study investigated effects of NSSI severity and severity of psychopathology on the HPA axis and ANS response to pain.
N = 164 adolescents with NSSI and n = 45 healthy controls received heat pain stimulation. Salivary cortisol, α-amylase and blood pressure were repeatedly assessed before and after painful stimulation. Heart rate (HR) and heart rate variability (HRV) were assessed continuously. NSSI severity and comorbid psychopathology were derived from diagnostic assessments. Main and interaction effects of time of measurement and NSSI severity, adjusted for severity of adverse childhood experiences, borderline personality disorder and depression, on HPA axis and ANS response to pain were examined using regression analyses.
Increasing NSSI severity predicted an increasing cortisol response (χ²(3) = 12.09, p = .007) to pain. After adjusting for comorbid psychopathology, greater NSSI severity predicted decreased α-amylase levels following pain (χ²(3) = 10.47, p = .015), and decreased HR (χ²(2) = 8.53, p = .014) and increased HRV(χ²(2) = 13.43, p = .001) response to pain.
Future research should implement several NSSI severity indicators, potentially revealing complex associations with the physiological response to pain. Assessing physiological responses to pain in NSSI in a naturalistic setting presents a promising avenue for future research in NSI.
Findings indicate an increased pain-related HPA axis response and an ANS response characterized by reduced sympathetic and increased parasympathetic activity associated with NSSI severity. Results support claims for dimensional approaches to NSSI and its related psychopathology alongside shared, underlying neurobiological correlates.
Cortisol across preschool day relates to teacher ratings of executive functioning for children facing economic hardship
2023, Early Childhood Research Quarterly
Experiences of poverty and racism in early childhood can overburden physiological systems that respond to stress with implications for the development of the prefrontal cortex and related executive functioning. The present study is unique in its examination of basal cortisol output across the preschool day in relation to teacher ratings of executive functioning. Participants were 310 children attending Head Start preschool in the United States, a majority of whom were Black, Hispanic, or Asian Heritage. Salivary cortisol was sampled in duplicate at 4 times across 2 days near the beginning of the school year, resulting in a total of 16 samples per child. Several weeks later, the BRIEF-P teacher rating scale assessed various components of executive functioning. Zero-order correlations suggested that basal cortisol output across the preschool day related to each assessed component of executive functioning, as well as to composite scores. Results of hierarchical linear modeling indicated that higher cortisol across the preschool day related to greater difficulties in overall teacher-reported executive functioning, controlling for child age, birth-assigned sex, race/ethnicity, and family income. Implications concern understanding the impact of stress on executive functioning in the preschool classroom and promoting positive outcomes for children facing adversity.
The role of inflammatory markers and cortisol in the association between early social cognition abilities and later internalising or externalising problems: Evidence from a UK birth cohort
2022, Brain, Behavior, and Immunity
Deficits in social cognition are associated with internalising (emotional and peer problems) and externalising (conduct problems and hyperactivity/inattention) symptoms in youth. It has been suggested that stress may be one of the mechanisms underlying these associations. However, no empirical studies have investigated if physiological stress can explain the prospective associations between social cognition deficits and internalising and externalising symptoms in the general youth population. This study addressed this question and focused on two indicators of physiological stress, dysregulated diurnal cortisol patterns and systemic inflammation.
Participants were 714 individuals from the Avon Longitudinal Study of Parents and Children (ALSPAC), a UK population-based birth cohort. Bayesian structural equation modelling was used to investigate a) the associations of social cognition abilities at ages 8, 11, and 14 years with internalising and externalising problems at age 17 years and b) the potential mediating effects of cortisol parameters at age 15 years and inflammatory markers [interleukin 6 (IL-6) and C-reactive protein (CRP)] at ages 9 and 16 years.
We found that social cognition difficulties were associated with later internalising and externalising problems. Flattened diurnal cortisol slope was associated with hyperactivity/inattention problems two years later. Lower morning cortisol partially mediated the direct association between social communication deficits at 8 years and hyperactivity/inattention and conduct problems at 17 years, even after adjustments for inflammation and confounders (for hyperactivity/inattention: indirect effect = 0.07, 95% CI [0.00, 0.18], p = .042; for conduct problems: indirect effect = 0.04, 95% CI [0.00, 0.11], p = .040). We did not find a significant association between systemic inflammation and social cognition difficulties, internalising problems, or externalising problems.
Our findings suggest that part of the effect of social communication difficulties in childhood on externalising problems in adolescence was mediated by lower morning cortisol. Hence, our study indicates that the hypoactivity of the hypothalamic–pituitary-adrenal (HPA) axis may be one of the physiological mechanisms linking some social cognition deficits to externalising problems.
Neighborhood Disadvantage Associated With Blunted Amygdala Reactivity to Predictable and Unpredictable Threat in a Community Sample of Youth
2022, Biological Psychiatry Global Open Science
Childhood socioeconomic disadvantage is a form of adversity associated with alterations in critical frontolimbic circuits involved in the pathophysiology of psychiatric disorders. Most work has focused on individual-level socioeconomic position, yet individuals living in deprived communities typically encounter additional environmental stressors that have unique effects on the brain and health outcomes. Notably, chronic and unpredictable stressors experienced in the everyday lives of youth living in disadvantaged neighborhoods may impact neural responsivity to uncertain threat.
A community sample of children (N = 254) ages 8 to 15 years (mean = 12.15) completed a picture anticipation task during a functional magnetic resonance imaging scan, during which neutral and negatively valenced photos were presented in a temporally predictable or unpredictable manner. Area Deprivation Index (ADI) scores were derived from participants’ home addresses as an index of relative neighborhood disadvantage. Voxelwise analyses examined interactions of ADI, valence, and predictability on neural response to picture presentation.
There was a significant ADI × valence interaction in the middle temporal gyrus, anterior cingulate cortex, hippocampus, and amygdala. Higher ADI was associated with less amygdala activation to negatively valenced images. ADI also interacted with predictability. Higher ADI was associated with greater activation of lingual and calcarine gyri for unpredictably presented stimuli. There was no three-way interaction of ADI, valence, and predictability.
Neighborhood disadvantage may impact how the brain perceives and responds to potential threats. Future longitudinal work is critical for delineating how such effects may persist across the life span and how health outcomes may be modifiable with community-based interventions and policies.
Hormonal response to perceived emotional distress in incarcerated men with sexual sadism
2022, Personality and Individual Differences
Sexual sadists derive pleasure from humiliation, domination and infliction of pain on victims. They display increased penile arousal and activation of brain regions involved in sexual arousal and emotional states when viewing stimuli depicting individuals in physical distress. Neuroactive hormones modulate these regions, but it is unknown if sexual sadists also have endocrine responses to depictions of individuals in distress. The present study examined endocrine responses, elicited by viewing a video depicting an individual in extreme emotional distress, in incarcerated adult male sexual offenders (n = 23) with varying levels of sadistic traits. Sadism, was measured by the Severe Sexual Sadism Scale (SeSaS). Testosterone (T), adrenocorticotropic hormone (ACTH), and oxytocin (OT) were assayed before and after participants watched a video depicting an individual in emotional distress. T responses to the video were significantly and positively associated with SeSaS scores. There were no significant associations between sexual sadism and OT or ACTH. Our findings provide physiological evidence of atypical processing of distress cues in sadism consistent with the role of testosterone in sexual arousal and aggressive behaviors. These findings have implications for the evaluation and treatment of sexual sadists.
Callous unemotional trait-like mice and their stressed dams
2021, Psychoneuroendocrinology
The co-occurrence of excess rates of aggression, general violation of societal norms and callous-unemotional trait confers specific risk for adult psychopathy. With the aim to address experimentally a model of conduct disorder, we investigated the male offspring of individual mouse dams characterized by high basal plasma corticosterone concentration (HC trait). Notably, classification indices correlated selectively in these females with quite poor maternal care devoted to their offspring. Contrary to their HC mothers, adult male offspring exhibited an integrated profile of dampened physiological reactivity to external stressors co-occurring poor sociability/emotional contagion, impaired punishment-induced memory, and exacerbated aggression. A significant reduction of glucocorticoid and opioid mu receptors’ expression in frontal cortex of model HC offspring was also evidenced. Moreover, in the absence of changes in oxytocin receptor in behaviorally-relevant neural areas, we showed that intranasal oxytocin administration (0 or 20.0 µg/kg) selectively modulated specific components of the behavioral phenotype. Ultimately, current data support the notion that maternally-inoculated environmental stress early in development may represent a critical risk factor in disturbances characterised by abnormal aggression and excess callousness.

View all citing articles on Scopus

View full text

ReviewPsychobiology of persistent antisocial behavior: Stress, early vulnerabilities and the attenuation hypothesis

Abstract

Section snippets

Background of the problem

The stress system and antisocial behavior

Mechanisms of attenuation of the stress system and antisocial behavior

Amygdala

Early learning

Dynamic systems and structures

Conclusions

Acknowledgements

J. Psychiatr. Res.

Psychoneuroendocrinology

Trends Neurosci.

Neuropsychopharmacology

Biol. Psychiatry

Biol. Psychiatry

Prog. Neuropsychopahrmacol. Biol. Psychiatry

Prev. Med.: An Int. J.

Psychoneuroendocrinology

Trends Cogn. Neurosci.

Neurosci. Biobehav.l Rev.

J. Am. Acad. Child Adolesc. Psychiatry

Prog. Neurobiol.

Biol. Psychiatry

Physiol. Beh.

Personality and Individual Differences

J. Am. Acad. Child Adol. Psychiatry

Behav. Brain Res.

Horm. Behav.

Biol. Psychiatry

Biol. Psychiatry

Psychiatry Res.

J. Adolesc.

Comparitative study in the rat of the actions of different types of stress on the release of 5-HT in raphe nuclei and forebrain areas

Neuropharmacology

Distinguishing the early-onset/persistent and adolescence-onset antisocial behavior types: From birth to 16 years

Dev. Psychopathol.

Early experience alters brain function and structure

Pediatrics

Hormone levels and personality traits in abusive and suicidal male alcoholics

Alcohol. Clin. Exp. Res.

Tryptophan depletion increases aggression in women during the premenstrual phase

Psychopharmacology

Psychophysiological protective factors for male subjects at high risk for criminal behavior

Am. J. Psychiatry

Relationship of maternal smoking during pregnancy with criminal arrest and hospitalization for substance abuse in male and female adult offspring

Am. J. Psychiatry

The functional anatomy of attention to visual motion: A functional MRI study

Brain

Developmental behavior genetics: Fusion, correlated constraints, and timing

Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat

Proc. Natl. Acad. Sci.

Physiological and behavioral regulation in two-year-old children with aggressive/destructive behavior problems.

J. Abnorm. Child Psychol.

The wisdom of the body

Role of genotype in the cycle of violence in maltreated children

Science

Influence of life stress on depression: Moderation by a polymorphism in the 5-HTT gene

Science

Prolactin response to buspirone was reduced in violent compared to nonviolent parolees

Psychopharmacology

The concepts of stress and stress system disorders

J. Am. Med. Assoc.

Development and self-regulatory structures of the mind

Dev. Psychopathol.

Failures in the expectable environment and their impact on individual development: The case of child maltreatment

The Mask of Sanity: An Attempt to Clarify Some Issues about the So-called Psychopathic Personality, Mosby

St Louis

Physiological responses to d-fenfluramine and ipsapirone challenge correlate with indices of aggression in males with personality disorder

Int. Clin. Psychopharmacol.

CSF 5-HIAA and family history of antisocial personality disorder in newborns

Am. J. Psychiatry

Association of the serotonin transporter and 5HT1Dbeta receptor genes with extreme, persistent and pervasive aggressive behavior in children,

Psychiatr. Genet.

The functional neuroanatomy of emotion and affective style

Trends Cognitive Neurosci.

Pharmacological and anatomical analysis of fear conditioning using the fear-potentiated startle paradigm

Behav. Neurosci.

Review
Psychobiology of persistent antisocial behavior: Stress, early vulnerabilities and the attenuation hypothesis