Elsevier

Psychiatry Research: Neuroimaging

Volume 203, Issues 2–3, August–September 2012, Pages 146-152
Psychiatry Research: Neuroimaging

Prone to excitement: Adolescent females with non-suicidal self-injury (NSSI) show altered cortical pattern to emotional and NSS-related material

https://doi.org/10.1016/j.pscychresns.2011.12.012Get rights and content

Abstract

Emotion-regulation difficulties have been identified as one of the core components in Non-suicidal self-injury (NSSI), a behaviour often beginning in adolescence. This pilot study evaluated differences in emotion processing between 18 female adolescents with and without NSSI by using verbal responses and functional magnetic resonance imaging (fMRI). Responses to pictures taken from the International Affective Picture System and slides with reference to NSSI were recorded both by verbal rating of valence and arousal and by fMRI. The NSSI group rated pictures with self-injurious reference as significantly more arousing than controls. For emotional pictures, the NSSI group showed a significantly stronger brain response in the amygdala, hippocampus and anterior cingulate cortex bilaterally. Depression explained differences between groups in the limbic area. Furthermore, the NSSI group also showed increased activity in the middle orbitofrontal cortex, and inferior and middle frontal cortex when viewing NSSI picture material. Participants with NSSI showed decreased activity in correlation to arousal in the occipital cortex and to valence in inferior frontal cortex when watching emotional pictures. The fMRI data support the notion that individuals with NSSI show an altered neural pattern for emotional and NSSI pictures. Behavioural data highlight proneness to excitement regarding NSSI topics. This fMRI study provides evidence for emotion-regulation deficits in the developing brain of adolescents with NSSI.

Introduction

Non-suicidal self-injury (NSSI) is defined as repetitive, deliberate destruction of one's own body tissue, without suicidal intent, that is not socially accepted (Lloyd-Richardson et al., 2007). Among adolescents, lifetime prevalence rates between 15 and 30% are reported in community samples from many nations (for review on prevalence rates, see Plener et al., 2010). Among psychiatric patients, NSSI is the most frequent reason for visits to medical emergency departments (Ballard et al., 2010). NSSI is not defined as a mental health disorder in the classification systems of the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV) and the International Classification of Diseases (ICD-10), but is mentioned as a symptom of borderline personality disorder (BPD). Thus, research about NSSI has often involved individuals with this personality disorder. However, NSSI – especially in adolescence – is not restricted to individuals with BPD but can be detected, for example, in depression, substance use disorders, eating disorders and also in teenagers without any further psychopathology (Jacobson and Gould, 2007, Stanford and Jones, 2009). Nock et al. (2006) showed in a sample of 89 adolescent inpatients with NSSI that only about half of the patients (51.7%) met criteria for BPD, while 59.6% met criteria for substance use disorder, 62.8% for externalizing and 51.7% for internalizing disorders. Thus, NSSI in adolescence does not seem to be specifically related to BPD. Recently, attempts have been made to propose the addition of a NSSI syndrome to the DSM-V (Shaffer and Jacobson, 2009).

Neuroimaging studies involving individuals with NSSI have so far been confined to studies in adults and older adolescents with BPD (and NSSI). One of the first functional magnetic resonance imaging (fMRI) studies compared 12 adult females with BPD and NSSI to 12 healthy controls when administering pain using heat stimuli (Schmahl et al., 2006). Patients with BPD showed an increased activity in the dorsolateral prefrontal cortex and a decrease in the posterior parietal cortex; individually adjusted pain stimuli led to a decreased activity in the perigenual anterior cingulate gyrus and the amygdala. Another study in 11 adult BPD patients and 10 healthy controls using an audioscript design (reporting a situation leading to NSSI) showed a decrease of activation in the right mid-cingulate and the left fusiform gyrus in the BPD group while imaging an act of NSSI (Kraus et al., 2010). Furthermore, studies on emotion processing in adult BPD patients often employed pictures from the International Affective Picture System (IAPS) (Lang et al., 2008). Herpertz et al. (2001) reported an elevated blood oxygenation level dependent (BOLD) fMRI signal in the amygdala bilaterally when comparing six female adult BPD patients with six healthy controls who viewed 12 emotionally aversive IAPS pictures. In another recent study, 20 BPD patients with a history of NSSI were compared to 23 healthy controls when IAPS pictures were presented in combination with warm or painful stimuli; it has been repeatedly shown that pain perception is altered in individuals with BPD (e.g. Cárdenas-Morales et al., 2011). The adult BPD patients with a history of NSSI demonstrated increased activity in the amygdala, insula and anterior cingulate cortex (ACC) when watching both neutral and negative IAPS pictures. Enhanced amygdala activity was positively correlated with self-perceived deficits in emotion regulation (Niedtfeld et al., 2010).

However, given that NSSI often starts around the age of 13 (Lloyd-Richardson et al., 2007), it seems necessary to assess younger adolescents given the differences in neurobiological alterations. Only a few studies involved adolescents with NSSI. In a study comparing 15 adolescent female BPD patients (mean age: 17.4, S.D.: 1.2) with “parasuicide episodes” to 15 adolescent and young adult females (mean age: 19.7, S.D.: 2.2), decreased volume of the ACC was found in BPD patients, which was correlated with the number of “parasuicide episodes” (Whittle et al., 2009). As parasuicide episodes were defined as “suicide attempts and non-suicidal self-injury”, findings about NSSI alone cannot be extracted from this study. In addition the age difference between patients and healthy controls must be considered as a possible limitation because brain maturation is not completed at this age. In another study of 20 adolescent BPD patients (mean age: 17.3, S.D.: 1.1 years), it was shown that greater numbers of “parasuicidal behaviours” were associated with an increased pituitary gland volume (PGV). Again, the authors did not differ between behaviours with and without suicidal intent (with 16 out of 20 who cut themselves), which – according to them – limited their findings (Jovev et al., 2008). To the best of our knowledge, no neuroimaging study has so far specifically investigated NSSI in adolescents by using an fMRI paradigm.

The regulation of both social situations and affective states has been suggested to be implicated in NSSI (Nock and Prinstein, 2004, Nock and Prinstein, 2005, Klonsky, 2007, Nock, 2010). In one of the few studies specifically addressing adolescents with NSSI, higher physiological reactivity (as measured by skin conductance) was observed in a distress task in subjects with NSSI (Nock and Mendes, 2008), a finding that is in line with poor distress tolerance, which is assumed to be an important factor in NSSI (Chapman et al., 2006). Another recent study showed an attenuated cortisol response to a social stress task in adolescent females with NSSI (Kaess et al., 2012). Based on the assumption that NSSI in adolescence is often used to regulate emotions, we hypothesized that alterations in emotion processing could be detected using fMRI in female adolescents with NSSI compared with healthy controls. As studies on adult BPD patients with NSSI showed a limbic hyperarousal when watching IAPS pictures (Niedtfeld et al., 2010) and pain can lead to decreased functional activity in the ACC and the amygdala (Schmahl et al., 2006), we hypothesized, that adolescents with NSSI would show limbic hyperarousal when watching IAPS pictures in comparison to findings in healthy controls. Furthermore, as NSSI often serves as an emotion-regulation strategy (Nock, 2010) and BPD can be seen as a “prototype of emotion dysregulation” (New et al., 2007), we hypothesized a dysfunctional prefrontal regulation mechanism in adolescents with NSSI, based on findings in BPD patients (New et al., 2007, Silbersweig et al., 2007). We further hypothesized, that adolescents with NSSI would find NSSI-related picture material more arousing than would healthy controls.

Section snippets

Participants

Nine adolescent females with NSSI (mean age 15.2 ± 1.5 years, range 14–18) were included in the study. Affected females had self-injured at least once within the past 6 months according to self-reports (see Table 1). Diagnoses of the NSSI group were defined according to clinical criteria and NSSI was assessed by using standardized instruments such as the Ottawa Self-injury Inventory (OSI; Nixon et al., 2002), the Self-Harm Behaviour Questionnaire (SHBQ; Gutierrez et al., 2001) and the Functional

Psychological tests and rating of pictures

Mean level of intelligence did not differ significantly between participants with NSSI (IQ of 105.2 ± 11.9) and healthy controls (IQ of 104.9 ± 8.5; F = 1.421, d.f. = 1/17, p = 0.22). Patients with NSSI had a significantly increased mean depression score (BDI II 31.2 ± 16.5) compared to controls (BDI II 6.6 ± 7.1; F = 17.0, d.f. = 1/17, p = 0.001). Seven patients and none of the controls presented with clinically relevant depressive symptoms.

Patients with NSSI presented significantly higher arousal ratings for

Discussion

This study is the first to report data on emotion processing in adolescents with NSSI using fMRI. Pictures from the IAPS, as well as visual stimuli depicting NSSI or related content, were used to assess neural correlates of emotion processing and subjective rating of emotional content. Participants with NSSI reported a higher arousal (but no differences in valence) for pictures with NSSI reference compared to age-matched controls. No difference between NSSI patients and controls was found for

References (61)

  • E.D. Klonsky

    The functions of deliberate self-injury: a review of the evidence

    Clinical Psychology Review

    (2007)
  • H.W. Koenigsberg et al.

    Neural corelates of emotion processing in borderline personality disorder

    Psychiatry Research: Neuroimaging

    (2009)
  • M.J. Minzenberg et al.

    Fronto-limbic dysfunction in response to facial emotion in borderline personality disorder: an event-related fMRI study

    Psychiatry Research: Neuroimaging

    (2007)
  • I. Niedtfeld et al.

    Affect regulation and pain in borderline personality disorder: a possible link to the understanding of self-injury

    Biological Psychiatry

    (2010)
  • M.K. Nixon et al.

    Affect regulation and addictive aspects of repetitive self-injury in hospitalized adolescents

    Journal of the American Academy of Child and Adolescent Psychiatry

    (2002)
  • M.K. Nock et al.

    Non-suicidal self-injury among adolescents: diagnostic correlates and relation to suicide attempts

    Psychiatry Research

    (2006)
  • T. Reisch et al.

    An fMRI study on mental pain and suicidal behavior

    Journal of Affective Disorders

    (2010)
  • P.A. Robinson et al.

    Bold responses to stimuli: dependence on frequency, stimulus form, amplitude, and repetition rate

    NeuroImage

    (2006)
  • S. Whittle et al.

    Anterior cingulate volume in adolescents with first-presentation borderline personality disorder

    Psychiatry Research: Neuroimaging

    (2009)
  • T.T. Yang et al.

    Adolescents with major depression demonstrate increased amygdala activation

    Journal of the American Academy of Child and Adolescent Psychiatry

    (2010)
  • E. Ballard et al.

    Understanding brain mechanisms of pain processing in adolescents' non-suicidal self-injury

    Journal of Youth and Adolescence

    (2010)
  • M.A. Brotman et al.

    Amygdala activation during emotion processing of neutral faces in children with severe mood dysregulation versus ADHD or bipolar disorder

    The American Journal of Psychiatry

    (2010)
  • A.B. Brühl et al.

    Differential modulation of emotion processing brain regions by noradrenergic and serotonergic antidepressants

    Psychopharmacology

    (2011)
  • A.M. Dale

    Optimal experimental design for event-related fMRI

    Human Brain Mapping

    (1999)
  • C. Delmo et al.

    Kiddie-Sads-Present and Lifetime Version (K-SADS-PL), 5

    Auflage der deutschen Forschungsversion

    (2000)
  • M. Ernst et al.

    Triadic model of the neurobiology of motivated behavior in adolescence

    Psychological Medicine

    (2006)
  • M. First et al.

    Users' Guide for the Structured Clinical Interview for DSM-IV Axis II Personality Disorders

    (1997)
  • K.J. Friston et al.

    Spatial registration and normalization of images

    Human Brain Mapping

    (1995)
  • T. Frodl et al.

    Neuronal correlates of emotional processing in patients with major depression

    The World Journal of Biological Psychiatry

    (2009)
  • T. Fydrich et al.

    SKID-II. Strukturiertes Klinisches Interview für DSM-IV

  • Cited by (0)

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