A Positive Affective Neuroendocrinology Approach to Reward and Behavioral Dysregulation

Emerging lines of research suggest that both testosterone and maladaptive reward processing can modulate behavioral dysregulation. Yet, to date, no integrative account has been provided that systematically explains neuroendocrine function, dysregulation of reward, and behavioral dysregulation in a unified perspective. This is particularly important given specific neuroendocrine systems are potential mechanisms underlying and giving rise to reward-relevant behaviors. In this review, we propose a forward-thinking approach to study the mechanisms of reward and behavioral dysregulation from a positive affective neuroendocrinology (PANE) perspective. This approach holds that testosterone increases reward processing and motivation, which increase the likelihood of behavioral dysregulation. Additionally, the PANE framework holds that reward processing mediates the effects of testosterone on behavioral dysregulation. We also explore sources of potential sex differences and the roles of age, cortisol, and individual differences within the PANE framework. Finally, we discuss future prospects for research questions and methodology in the emerging field of affective neuroendocrinology.

• Publication year

  2015

• Venue

  Frontiers in Psychiatry

• Publication date

  2015-07-02

• Fields of study

  Medicine, Psychology

• Identifiers
  DOI 10.3389/fpsyt.2015.00093PMID 26191007PMCID 4489099
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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• Pubertal testosterone influences threat-related amygdala-orbitofrontal cortex coupling.

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• Testosterone and Economic Risk Taking: A Review

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• Testosterone and cortisol jointly modulate risk-taking.

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• Close Versus Decisive Victory Moderates the Effect of Testosterone Change on Competitive Decisions and Task Enjoyment

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• Trait Anxiety Moderates the Relationship Between Testosterone Responses to Competition and Aggressive Behavior

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• Risk-taking behavior: dopamine D2/D3 receptors, feedback, and frontolimbic activity.

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• Testosterone, cortisol, and psychopathic traits in men and women.

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• Testosterone rapidly increases neural reactivity to threat in healthy men: a novel two-step pharmacological challenge paradigm.

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• Testosterone is related to deviance in male army veterans, but relationships are not moderated by cortisol.

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• Testosterone and temperament traits in men: Longitudinal analysis.

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• Reward Dysregulation and Mood Symptoms in an Adolescent Outpatient Sample

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• Genetic, Hormonal, and Neural Underpinnings of Human Aggressive Behavior

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• Dopamine Modulates Risk-Taking as a Function of Baseline Sensation-Seeking Trait

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• Mesolimbic dopamine release is linked to symptom severity in pathological gambling

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• Baby cries and nurturance affect testosterone in men.

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• Testosterone Affects Gaze Aversion From Angry Faces Outside of Conscious Awareness

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• Waiting to win: elevated striatal and orbitofrontal cortical activity during reward anticipation in euthymic bipolar disorder adults

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• Fetal Programming Effects of Testosterone on the Reward System and Behavioral Approach Tendencies in Humans

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• Are Women Really More Risk-Averse than Men?

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• Androgen influence on prefrontal dopamine systems in adult male rats: localization of cognate intracellular receptors in medial prefrontal projections to the ventral tegmental area and effects of gonadectomy and hormone replacement on glutamate-stimulated extracellular dopamine level.

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• Testosterone levels in suicide attempters with bipolar disorder.

  2012cited by this paper
• Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: a review of single administration studies.

  2012cited by this paper
• Can Feeling Too Good Be Bad?

  2011influential reference
• State, not trait, neuroendocrine function predicts costly reactive aggression in men after social exclusion and inclusion.

  2011cited by this paper
• What goes up can come down? A preliminary investigation of emotion reactivity and emotion recovery in bipolar disorder.

  2011cited by this paper
• Low- and High-Testosterone Individuals Exhibit Decreased Aversion to Economic Risk

  2011cited by this paper
• The social neuroendocrinology of human aggression.

  2011cited by this paper
• Reward dysfunction in mania: neural correlates of risk and impulsivity in individuals vulnerable to bipolar disorder

  2011cited by this paper
• Cognitive neuroscience of self-regulation failure.

  2011cited by this paper
• Increased testosterone-to-cortisol ratio in psychopathy.

  2011cited by this paper
• Association between impulsivity, reward responsiveness and body mass index in children

  2011cited by this paper
• Hooked on a feeling: rumination about positive and negative emotion in inter-episode bipolar disorder.

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• Importance of considering testosterone-cortisol interactions in predicting human aggression and dominance.

  2011cited by this paper
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• A review and synthesis of positive emotion and reward disturbance in bipolar disorder.

  2011cited by this paper
• X-rated material and perpetration of sexually aggressive behavior among children and adolescents: is there a link?

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• Sex differences in impulsivity: a meta-analysis.

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• The Steroid/Peptide Theory of Social Bonds: integrating testosterone and peptide responses for classifying social behavioral contexts.

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• Testosterone levels correspond with increased ventral striatum activation in response to monetary rewards in adolescents.

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• Who Takes Risks When and Why?

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• Power Posing

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• Neural Mechanisms of the Testosterone–Aggression Relation: The Role of Orbitofrontal Cortex

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• The Role of the Behavioral Approach System (BAS) in Bipolar Spectrum Disorders

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• The role of puberty in the developing adolescent brain

  2010cited by this paper
• Putting pubertal timing in developmental context: implications for prevention.

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• Testosterone decreases trust in socially naïve humans

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• Prosocial motives, emotions, and behavior: The better angels of our nature.

  2010cited by this paper
• Testosterone and cortisol jointly regulate dominance: evidence for a dual-hormone hypothesis.

  2010cited by this paper
• A time of change: behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues.

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• Testosterone reduces amygdala-orbitofrontal cortex coupling.

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• Socially explosive minds: the triple imbalance hypothesis of reactive aggression.

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• Personality and testosterone in men from a high-fertility population

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• Prejudice and truth about the effect of testosterone on human bargaining behaviour

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• Pubertal development and behavior: hormonal activation of social and motivational tendencies.

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• Global burden of substance use disorders in adolescents and young adults aged 10–24 years from 1990 to 2021

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• Adverse events associated with four atypical antipsychotics used as augmentation treatment for major depressive disorder: A pharmacovigilance study based on the FAERS database.

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• Neuroendocrine Mechanisms in the Links Between Early Life Stress, Affect, and Youth Substance Use: A Conceptual Model for the Study of Sex and Gender Differences.

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  2019cites this paper
• Taking risks for personal gain: An investigation of self-construal and testosterone responses to competition

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• Human social neuroendocrinology: Review of the rapid effects of testosterone

  2018cites this paper
• Hormonal underpinnings of status conflict: Testosterone and cortisol are related to decisions and satisfaction in the hawk‐dove game

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• Developmental Differences in Reward Sensitivity and Sensation Seeking in Adolescence: Testing Sex-Specific Associations With Gonadal Hormones and Pubertal Development

  2017cites this paper
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  2017cites this paper
• Dare to approach: Effects of testosterone on avoidance in social anxiety

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  2016cites this paper
• VARIETIES OF GUILT AND THEIR FUNCTIONS

  2016cites this paper
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  2015cites this paper