Dysregulated responses to emotions among abstinent heroin users: Correlation with childhood neglect and addiction severity

https://doi.org/10.1016/j.pnpbp.2013.10.011Get rights and content

Highlights

  • Addicted subjects react to emotions with higher arousal but week HPA axis response.

  • Addiction severity seems to be related to the childhood adverse experiences.

  • Emotional impairment seems to link childhood neglect and addiction behaviour.

Abstract

The aim of this paper was to investigate the subjective responses of abstinent heroin users to both neutral and negative stimuli and the related hypothalamus-pituitary-adrenal reactions to emotional experience in relationship to their perception of childhood adverse experiences. Thirty male abstinent heroin dependents were included in the study. Emotional responses and childhood neglect perception were measured utilizing the State-Trait Anxiety Inventory Y-1 and the Child Experience of Care and Abuse Questionnaire. Neutral and unpleasant pictures selected from the International Affective Picture System and the Self-Assessment Manikin procedure have been used to determine ratings of pleasure and arousal. These ratings were compared with normative values obtained from healthy volunteers used as control. Blood samples were collected before and after the experimental sessions to determine both adrenocorticotropic hormone and cortisol plasma levels. Basal anxiety scores, cortisol and adrenocorticotropic hormone levels were higher in abstinent heroin users than in controls. Tests showed that anxiety scores did not change in controls after the vision of neutral slides, whilst they did in abstinent heroin addicts, increasing significantly; and increased less significantly after the unpleasant task, in comparison to controls. Abstinent heroin users showed significantly higher levels of parent antipathy and childhood emotional neglect perception than controls for both the father and the mother. Plasma adrenocorticotropic hormone and cortisol levels did not significantly increase after unpleasant slide set viewing among addicted individuals, because of the significantly higher basal levels characterizing the addicted subjects in comparison with controls. Multiple regression correlation showed a significant relationship between childhood neglect perception, arousal reaction, impaired hypothalamus-pituitary-adrenal axis response and addiction severity. Early adverse experiences seem to affect the entire interaction between hyper-arousal, reduced hormonal response to stress and addiction severity. Our findings, although obtained in a small number of subjects, indicate a significant link between the perception of parental style/care/support during childhood and the ability to cope with stressful emotional stimuli in adulthood and addiction severity.

Introduction

Evidence indicates that detoxified abstinent opioid users have shown compromised emotional response to natural reinforcing stimuli and reduced reward perception (Kornreich et al., 2003). Moreover, current opioid users also may have abnormal emotion processing when exposed to competent positive and negative stimuli (de Arcos et al., 2008). Nevertheless, there are few studies on the addicted patients' capacity to cope with emotions in general. With regard to emotional experience, in our previous study (Gerra et al., 2003), abstinent heroin users have been found to present increased arousal and emotional response to neutral images and reduced response to both pleasant and unpleasant images. More recently, current heroin poly-substance users have shown altered emotional pattern, characterized by heightened response to negative stimuli and blunted response to positive stimuli (de Arcos et al., 2008).

Accordingly, brain-imaging studies have also documented the neural responses to drug or drug-related cues in addicts (e.g., Garavan et al., 2000, George et al., 2001). In particular, Wang et al. (2010) utilized functional magnetic resonance imaging to examine brain responses in heroin addicts revealing a complex pattern of altered processing of non-drug related affective stimuli and showing both heightened and blunted neural responses to emotions in several areas of the brain and for different stimulus valence.

Chronic emotional impairment has been linked to adverse childhood experience with consequences related to depression, anxiety and risky behaviours (Klein et al., 2007, Krause et al., 2003). In fact, persistent changes in the limbic circuitry, which is associated with emotional response and arousal, seem to be produced during early neurodevelopment by stressors such as childhood trauma (McCrory et al., 2011).

Findings from a recent study (Grant et al., 2011) provide support for this by showing that potentiated amygdala response to sad stimuli observed among unipolar depressed patients may be driven primarily by sensitization of the amygdala, secondary to persistent exposure to elevated glucocorticoids following early life adversity. In fact, acute stress is associated with subsequent amygdala hypervigilance to emotional stimuli (van Marle et al., 2009). In line with these findings of persistent vigilance, enhanced left amygdala activation during the processing of negative emotional faces was observed in youths who experienced severe emotional and physical neglect in foster care or orphanages (Maheu et al., 2010) and in young adults reporting high childhood family stress (Taylor et al., 2006).

The disturbance of emotion-processing among addicted individuals could correspond to a dysregulation of neuro-physiological reactions. For example, the altered emotional response seems to be associated in heroin-abstinent individuals with a dysfunction of the hypothalamus-pituitary-adrenal (HPA axis), characterized by elevated cortisol and adrenocorticotropic hormone (ACTH) basal levels and a consequent lack of response to unpleasant stimuli (Gerra et al., 2003). Also, HPA axis dysregulation has been repeatedly hypothesized to affect the relationship between childhood traumatic experiences, stressful stimuli, emotional changes and substance abuse vulnerability (Gerra et al., 2008, Heim et al., 2002, Schäfer et al., 2010, Shea et al., 2005). Adverse family relationships in childhood, for example, appear associated to significantly reduced salivary cortisol across a behavioural task in adulthood (Luecken et al., 2009). In particular, childhood parental divorce was found associated with attenuated cortisol in young adulthood (Kraft and Luecken, 2009), which may contribute to the inability to cope with emotional stress.

However, little is known about the influence of childhood adverse events reported retrospectively by addicted patients on their emotional response to different stimulus valence. Therefore, in the present study we investigate the responses to neutral and negative stimuli in human laboratory study, and the related HPA reactions to emotional arousal, among abstinent heroin users, in relationship to their perception of childhood neglect experience. Moreover, considering the relevance that has been attributed to childhood trauma for later drug dependence severity, with significant emotional impairment, insecurity in social contacts and phobic fear (Schnieders et al., 2006), we also explored whether or not the severity of addiction was correlated to the emotional responses to neutral and unpleasant stimuli, the history of neglect and the HPA axis hormone reactivity.

We hypothesized that: 1) the greatest HPA and emotional dysregulation to neutral and unpleasant stimuli will be evident in the heroin addicts compared with controls; 2) in abstinent heroin abusers, HPA axis and emotional response to neutral and unpleasant stimuli will be associated with a significant severity of addiction and high levels of childhood neglect perception.

Thirty abstinent heroin addicts, in comparison with 30 control healthy subjects (never exposed to drugs) were investigated and submitted to a test about their retrospective perception of childhood neglect and to both psychosocial scale and hormonal measures in response to neutral and unpleasant stimuli in human lab (Lang slides).

Section snippets

Subjects

Thirty (30) male heroin-dependent subjects, aged 22–35 years (M ± SD = 29 ± 6 years), with a history of heroin dependence of 3–7 years (M ± SD 5 ± 2.2 years), were included in the study, after written informed consent. They were not paid for their participation and accepted to enter the study as volunteers. They had been using heroin two or three times a day (active principle 5%–10%) for at least 3 years without any abstinence periods. Heroin dependence was diagnosed following Diagnostic and Statistical

Psychiatric evaluation

Among addicted patients, who were diagnosed as ‘heroin dependent’ following DSM-IV criteria, 7 (23.3%) were dually diagnosed for major depression; 6 (20.0%) of the subjects were found to be suffering from antisocial personality disorder; 6 (20.0%) presented generalized anxiety symptoms; and 3 (10.0%) presented attention deficit hyperactivity disorder. Among addicted individuals, other subjects showed psychiatric symptoms (i.e. borderline personality disorder traits), but they did not fulfil the

Discussion

In the present study abstinent heroin addicts presented high level of sensitivity to negative emotions, with increased levels of arousal after the dislikeable slides. Accordingly, increased perception of unpleasantness has been reported in our previous study in a smaller sample of addicted subjects (Gerra et al., 2003) and greater sensitivity to the stimuli of neutral or negative nature has been repeatedly evidenced among heroin addicts by other authors (de Arcos et al., 2008).

Overreaction to

Conclusion

In spite of such limitations, the study appears to indicate a significant link between perception of parental style/care/support during childhood and the ability to cope with stressful stimuli in adulthood, the impaired reactivity of HPA axis and addiction severity. Child neglect poses a significant challenge to children's psychobiological development and well-being, with a long lasting vulnerability condition that can predispose to the most severe forms of substance abuse disorders.

The

Acknowledgements

The authors wish to thank Dr. Pompeo Lattanzi for his linguistic assistance in manuscript preparation.

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