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Journal of Abnormal ChildPsychologyAn official publication of theInternational Society for Research inChild and Adolescent Psychopathology ISSN 0091-0627Volume 42Number 4 J Abnorm Child Psychol (2014)42:659-668DOI 10.1007/s10802-013-9810-4

Paralimbic Gray Matter Reductions inIncarcerated Adolescent Females withPsychopathic Traits

Lora M. Cope, Elsa Ermer, PrashanthK. Nyalakanti, Vince D. Calhoun & KentA. Kiehl

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Paralimbic Gray Matter Reductions in IncarceratedAdolescent Females with Psychopathic Traits

Lora M. Cope & Elsa Ermer & Prashanth K. Nyalakanti &Vince D. Calhoun & Kent A. Kiehl

Published online: 25 October 2013# Springer Science+Business Media New York 2013

Abstract Psychopathy-related paralimbic and limbic struc-tural brain abnormalities have been implicated in incarceratedadult and adolescent male samples. However, there have beenfew neuroimaging studies of psychopathic traits in females ingeneral and no studies from incarcerated female youth inparticular. Here we present the first study to examine therelationship between brain gray matter volumes and psycho-pathic traits (assessed using the Psychopathy Checklist-YouthVersion [PCL-YV]) in a sample of maximum-security incar-cerated female adolescents (N =39; mean age=17.6 years).Consistent with male samples, regional gray matter volumeswere negatively related to psychopathic traits in female youthoffenders in limbic and paralimbic areas, includingorbitofrontal cortex, parahippocampal cortex, temporal poles,and left hippocampus. These results provide evidence that

psychopathic traits manifest similar neural abnormalitiesacross sex and age.

Keywords Voxel-basedmorphometry (VBM) . Psychopathictraits .Adolescentfemales .Paralimbicstructures .PsychopathyChecklist-YouthVersion (PCL-YV) . Incarcerated offenders

Antisocial behavior in youth is a severe social problem costingU.S. taxpayers roughly $56.7 billion per year1 (Caldwell et al.2006b). Although behavioral problems tend to be more prev-alent in boys (American Psychiatric Association 2000), girlsstill constitute a considerable portion of adolescent antisociality(Silverthorn and Frick 1999). Considerable efforts have beenapplied to examining the psychological and social factors thatcontribute to antisociality in adolescence; however, relativelylittle work has specifically examined these factors in femaleyouth. Indeed, traditional theories of youth antisociality weredeveloped specifically about males (e.g., Moffitt 1993), lead-ing some to question whether these theories can be generalizedto females (Silverthorn and Frick 1999).

For some antisocial adolescent girls, problematic behaviorpersists and becomes more severe, often leading to arrests,mental health problems, and maladaptive drug and alcoholuse in adulthood (Silverthorn and Frick 1999). Adults on thelife-course persistent trajectory often meet diagnostic criteriafor psychopathy, which is an important predictor of persistencein criminal activity and recidivism (Hemphill et al. 1998; Yanget al. 2010).

1 This figure is based on two factors: a) The estimated cost of all crime inthe United States in 1987 was $257 billion (Cohen et al. 1994), and b)Juveniles accounted for 22 % of all arrests in that year (Federal Bureau ofInvestigation 1996). Considering that the annual burden of crime intoday’s dollars has been estimated at $1 trillion (Anderson 1999) andindividuals under 18 accounted for over 14 % of all arrests in 2009(Federal Bureau of Investigation 2010), $56.7 billion per year is undoubt-edly an underestimate.

Electronic supplementary material The online version of this article(doi:10.1007/s10802-013-9810-4) contains supplementary material,which is available to authorized users.

L. M. Cope :K. A. KiehlDepartment of Psychology, University of New Mexico,Albuquerque, NM, USA

L. M. Cope : P. K. Nyalakanti :V. D. Calhoun :K. A. KiehlThe Mind Research Network and Lovelace Biomedical andEnvironmental Research Institute, Albuquerque, NM, USA

E. ErmerDerner Institute Psychology Department,Adelphi University, Garden City, NY, USA

V. D. CalhounDepartment of Electrical and Computer Engineering,University of New Mexico, Albuquerque, NM, USA

L. M. Cope (*)Addiction Research Center and Department of Psychiatry,The University of Michigan, 4250 Plymouth Rd., Ann Arbor,MI 48109, USAe-mail: lcope@med.umich.edu

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Psychopathy is a personality disorder characterized byinterpersonal, antisocial, and affective traits such as glibness,impulsivity, and lack of empathy, guilt, and remorse (Cleckley1976; Hare 2003). Psychopathy in adults is commonlyassessed with the Hare Psychopathy Checklist-Revised(PCL-R; Hare 2003), the most widely accepted diagnosticinstrument for psychopathy. The PCL-R can be meaningfullydivided into two factors, with Factor 1 comprising interper-sonal and affective traits (conceptually similar to callous andunemotional traits in youth) and Factor 2 comprising lifestyleand antisocial traits (conceptually similar to conduct disorderin youth). Given the strong evidence that psychopathic symp-toms manifest early in development (Lahey and Kazdin1990), Hare and colleagues constructed a downward exten-sion of the PCL-R, the Psychopathy Checklist-Youth Version(PCL-YV; Forth et al. 2003), for use in adolescent samples. Itis important to note that psychopathy in youth does not implythat adolescents with these traits are on a predetermined and/orunchangeable path of antisociality and/or adult psychopathy.Indeed, recent evidence suggests that early interventions showgreat promise for reducing antisocial outcomes in high riskyouth (Caldwell et al. 2006a).

Evidence from electrophysiology (e.g., Kiehl et al. 1999),functional neuroimaging (e.g., Birbaumer et al. 2005;Harenski et al. 2010; Kiehl et al. 2001; Muller et al. 2003),structural neuroimaging (e.g., De Oliveira-Souza et al. 2008;Ermer et al. 2012; Muller et al. 2008), and brain damage andlesion studies (e.g., Malloy et al. 1993) suggests thatparalimbic cortex and limbic structures are involved in psy-chopathic symptomology (reviewed in Kiehl 2006). Resultsfrom structural MRI studies support the hypothesis that limbicand paralimbic regions (e.g., De Oliveira-Souza et al. 2008;Ermer et al. 2012; Muller et al. 2008; Tiihonen et al. 2008) aswell as prefrontal areas (De Oliveira-Souza et al. 2008; Yanget al. 2005) are impaired in psychopathy, however thesestudies have generally been limited to adult males.

Results from a recent large-scale structural study of incar-cerated male youth (N =191; mean age 17.3) support thenotion that psychopathic traits may manifest with neural dif-ferences in adolescence (Ermer et al. 2013). In Ermer et al.(2013), adolescent males were assessed for psychopathy withthe PCL-YV and regional differences in gray matter volumewere examined using voxel-based morphometry (VBM).Brain volume, age, and substance use were covaried in orderto isolate the effects of psychopathy on gray matter. Decreasesin gray matter volume were found in the posterior cingulatecortex and orbitofrontal cortex, extending into the para-hippocampal cortex and temporal poles. Additionally, therewas an area of positive association between psychopathictraits and gray matter volume in medial prefrontal cortex.These findings are consistent with the hypothesis that psy-chopathy is a neurodevelopmental disorder. Other studieshave shown that boys with conduct disorder (CD) have

reduced volumes in the temporal lobe (M =16 years;Kruesi et al. 2004), insula and amygdala (M =13 years;Sterzer et al. 2007), and temporal lobes, amygdala, hippo-campus, orbitofrontal cortex, and ventromedial prefrontalcortex (M =14 years; Huebner et al. 2008). However, onestudy of boys from the community (M =11 years) with callousand unemotional traits found increased gray matter volume insuperior temporal gyrus, orbitofrontal cortex, anterior cingu-late cortex, left hippocampus, insula, and posterior cingulatecortex (De Brito et al. 2009).

These studies on male adolescents and adults suggest thatpsychopathic traits are associated with altered gray matterdevelopment, but the extent to which these differences arefound in adolescent female offenders is unknown. Though onestudy of adolescent females found gray matter reductions in aconduct disorder group versus healthy controls (Fairchildet al. 2013), to our knowledge no studies have addressed theeffect of psychopathic traits on gray matter volume in incar-cerated adolescent female offenders using the PCL-YV. Herewe begin to address this gap by presenting results from VBManalyses on the relationship between brain structure and psy-chopathic traits (assessed using the PCL-YV) in a sample ofmaximum-security incarcerated female adolescents (N =39;mean age=17.6 years). Here we test the hypothesis that, asin samples of adult and adolescent males, elevated psycho-pathic traits will be associated with reduced gray matter vol-umes in the parahippocampus, amygdala, hippocampus, tem-poral poles, anterior and posterior cingulate, and orbitofrontalcortex in incarcerated female youth.

Methods

Participants

These data were drawn from female participants in the Na-tional Institute of Mental Health (NIMH)-funded SouthWestAdvanced Neuroimaging Cohort, Youth sample (SWANC-Y),collected between June, 2007, and March, 2011, at amaximum-security youth detention facility in New Mexico.This research was approved by the University of NewMexicoHealth Sciences Center Human Research Review Committeeand individuals volunteered to participate after providing writ-ten informed consent (if≥18 years or age) or after providingwritten informed assent and parent/guardian written informedconsent (if<18 years of age). Complete data sets were avail-able from 48 female adolescents, ranging from 15 to 19 yearsof age. Average age of participants was 17.6 years (SD =1.10).Participants were predominantly Hispanic/Latino (39.6 %),white/Caucasian (27.1 %), or Native American (22.9 %).From self-report, 97.9 % participants were right-handed and2.1 % left-handed; all females in the analyzed sample (seebelow) were right-handed. Participants were paid a rate yoked

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to the standard institutional hourly pay scale for their partici-pation in the study.

Assessments and Measures

Psychopathy Interpersonal/affective and lifestyle/antisocialpsychopathic traits were assessed using the PsychopathyChecklist-Youth Version (PCL-YV; Forth et al. 2003). Theassessment includes a review of institutional records and asemi-structured interview covering individuals’ school, fami-ly, work, and criminal histories, as well as their interpersonaland emotional skills. Individuals are scored on 20 items thatmeasure personality traits and behaviors characteristic of psy-chopathy. Scores range from 0 to 40. For adults, the accepteddiagnostic cutoff for psychopathy is 30 and above (Hare1991), and incarcerated populations average scores of 22.1(Hare 2003). Interviews were conducted by trained re-searchers and videotaped for reliability assessment (intra-classcorrelation coefficient [ICC]=0.90 for PCL-YV Total scores,12 % of interviews double-rated). For comparison to adultsamples, we examined a two factor model (Hare 2003; Harpuret al. 1989), with Factor 1 composed of interpersonal andaffective traits and Factor 2 composed of lifestyle and antiso-cial traits.

Control Measures Full-scale IQ was estimated from the Vo-cabulary andMatrix Reasoning subtests of theWechsler AdultIntelligence Scale (WAIS-III; Ryan et al. 1999; Wechsler1997) for participants older than 16 years of age and fromthe Wechsler Intelligence Scale for Children-Fourth Edition(WISC-IV; Sattler and Dumont 2004; Wechsler 2003) forparticipants younger than 16 years of age. The mean full-scale IQ estimate in this sample was 97.2 (SD =12.72); IQscores were unavailable for n =4 participants.

A post-head injury symptoms questionnaire (adapted fromKing et al. 1995) was used to assess history, number, andduration of traumatic brain injuries, in addition to relatedsymptoms. Individuals who reported a traumatic brain injurywith loss of consciousness>1 h were excluded (n =1); infor-mation was not available for n =1 participant. Trained re-searchers administered the Kiddie Schedule for Affective Dis-orders and Schizophrenia for School-Age Children-Presentand Lifetime Version (KSADS-PL; Kaufman et al. 1997).Participants with any history of psychotic (n =2) or bipolar(n =1) disorders were excluded from analyses.

Substance Use Psychopathic traits are frequently comorbidwith substance use in adults (Smith and Newman 1990) andadolescents (O’Neill et al. 2003). We assessed substance usein two ways: 1) Using the KSADS, the total number ofsubstances (alcohol and drugs) for which an individual metthe lifetime dependence diagnostic criteria was calculated(substance dependence ; theoretical range: 0–8). 2) Using a

modified version of the Addiction Severity Index (McLellanet al. 1992), years of use were summed for each substance(alcohol and drug) that the participant reported using on aregular basis (i.e., three or more times per week for a mini-mum of 1 month). These summed scores were then divided byage and a square root transformation was applied to correct forskew (years of regular use ).

MRI Acquisition

High-resolution T1-weighted structural MRI scans were ac-quired on the Mind Research Network Siemens 1.5 TAvantomobile scanner, stationed at the maximum-security detentionfacility, using a multi-echo MPRAGE pulse sequence (repeti-tion time=2530 ms, echo times=1.64 ms, 3.50 ms, 5.36 ms,7.22 ms, inversion time=1100 ms, flip angle=7°, slice thick-ness=1.3 mm, matrix size=256×256) yielding 128 sagittalslices with an in-plane resolution of 1.0 mm×1.0 mm. Datawere pre-processed and analyzed using Statistical ParametricMapping software (SPM5; Wellcome Department of Cogni-tive Neurology, London, UK; http://www.fil.ion.ucl.ac.uk/spm). T1 images were manually inspected by an operatorblind to subject identity and realigned to ensure properspatial normalization. Images were spatially normalized tothe SPM5 T1Montreal Neurological Institute (MNI) templateusing non-linear registration, segmented into gray matter,white matter, and cerebrospinal fluid, and modulated withthe Jacobian determinants to preserve total volume(Ashburner and Friston 2000, 2005). The modulated, normal-ized gray matter segments were then averaged to create acustomized, study-specific template. Next, the original graymatter segments were normalized to the customized template.Finally, the images were resampled to 2×2×2 mm andsmoothed with a 10 mm full-width at half-maximum(FWHM) Gaussian kernel. Voxels with a gray matter valueof<0.15 were excluded in order to remove possible edgeeffects between graymatter and whitematter, following Ermerand colleagues (2012).

Analytic Strategy

Our final sample included N =39 individuals, after excludingn =5 for excessive motion or radiological findings (e.g., tu-mors, abnormal ventricles), n =1 who reported a traumaticbrain injury with loss of consciousness>1 h, and n =3 with ahistory of psychotic or bipolar disorders.

Primary Whole Brain Analyses Multiple regression analyseswere performed on a voxel-by-voxel basis over the wholebrain using the general linear model to evaluate the relation-ship between PCL-YV and regional gray matter volumes.Psychopathy scores can be treated continuously or discretized(i.e., low, medium, high), and many researchers agree that

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both analytic approaches are valid (e.g., De Oliveira-Souzaet al. 2008; Muller et al. 2008). Here PCL-YV score wasexamined as a continuous variable.

All analyses included a measure of substance use as acovariate. Substance use can affect gray matter, although thedirection and duration of effects of substance use on graymatter, and the role of related third variables (like psychopathy),is currently unsettled (Tanabe et al. 2009; Yuan et al. 2009).

Adolescence is a period of rapid developmental changes inbrain structure (Giedd 2004) and gray matter volume de-creases with age (Good et al. 2001). Thus, age was includeda covariate in all analyses. Volumetric analyses require acontrol for individual variation in brain size; here we includedbrain volume (white matter + gray matter) as a covariate in allanalyses in order to focus on regionally-specific brain differ-ences (Pell et al. 2008).

In multiple regression analyses evaluating the relationshipbetween the psychopathy factors and regional gray mattervolume, both factors were included in the model simulta-neously, in addition to the substance use, age at time of scan,and brain volume covariates.

Results from an independent incarcerated adult male sam-ple (Ermer et al. 2012) indicate that gray matter volumedifferences are extensively distributed in paralimbic and lim-bic regions, but the effect size at each voxel is small. Wetherefore used a method that tests for potentially small butdistributed effects in whole-brain analyses by estimating thecluster size necessary to correspond to a desired statisticalthreshold.Monte Carlo simulation conducted using AlphaSim(Ward 2000) determined that a 1366 voxel-extent at a heightthreshold of p <0.05 yielded a family-wise error rate (FWE)corrected threshold of p <0.05, accounting for spatial correla-tions between gray matter volumes in neighboring voxels. Alltables and figures are presented in MNI space.

Supplementary Whole Brain Analyses To evaluate the robust-ness of the effects to model variation with regard to themeasure of substance use, an additional analysis with “yearsof regular use” as a covariate instead of “substance depen-dence” was performed (with PCL-YV Total score as thepredictor of interest, controlling for age and brain volume).

Anxiety diagnosis was marginally related to both Factor 1and Total PCL-YV scores; thus anxiety diagnosis was includ-ed in two separate models: one with PCL:YV Total score asthe predictor of interest and one with both factor scores(Table S2; Figures S2 and S3).

Additionally, given differences in antisocial behavior andbrain structure between males and females, the moderatingeffect of participant sex was addressed using a previously-published sample of incarcerated male adolescents (Ermeret al. 2013). Here males and females were combined intoone sample (N =230; 1334 voxel-extent) and the interactionbetween psychopathy (Total scores) and participant sex was

evaluated. In this model, substance dependence, brain vol-ume, age, participant sex, PCL-YV Total scores, and a partic-ipant sex by PCL-YV Total score interaction term were in-cluded as predictors. Differences between males and females,controlling for age and brain volume were also examineddirectly (Figure S5).

Regions of Interest Analysis In addition to the whole-brainanalyses, we also tested our hypotheses in a priori regionsof interest (ROI) based on anatomical ROI peak coordinatesidentified in an independent adult sample (Ermer et al.2012; N =254). Because the peaks associated with theamygdala, hippocampus, and parahippocampal regions werevery close spatially, we averaged these peak coordinates toproduce one set of coordinates for the right and for the left,denoted “parahippocampal” in Table 2. We then used thesecoordinates to conduct small volume correction (SVC),using 10 mm diameter spheres, in our adolescent femalesample.

Comparison with Previous Samples

These female adolescents were demographically similar tomale adolescents scanned at the same facility in terms ofage, IQ, substance dependence, psychopathic traits, diagno-ses of oppositional defiant disorder and conduct disorder,and criminal convictions (Ermer et al. 2013; Table 1). Theproportion of female youth with anxiety, depressive, andattention deficit-hyperactivity disorder (ADHD) diagnoseswas significantly greater than that for males (Table 1). Con-sistent with prior literature (Puzzanchera et al. 2011), thetotal number of criminal convictions was similar for malesand females, although female adolescents tended to havefewer convictions for violent crimes than did male adoles-cents (Table 1).

The female youth sample covered a wide range of PCL-YVscores (9.4-36), with a mean score (M =22.4, SD =6.43) com-parable to those observed in adult incarcerated populations(Hare 2003) and in incarcerated male adolescents from thesame facility (M =23.6, SD =6.19; Ermer et al. 2013). As istypical, Factor 1 and Factor 2 were significantly positivelycorrelated at r (39)=0.60, p <0.001.

Consistent with findings in adult men (Ermer et al.2012) and male adolescents (Ermer et al. 2013), PCL-YVTotal scores were not significantly correlated with IQ,r (35)=−0.23, p =0.18, or traumatic brain injury history:r (38)=0.04, p =0.81; number: r (38)=0.08, p =0.64; or du-ration: r (37)=−0.03, p =0.85. Adult men and male adoles-cents showed moderate positive correlations (r ~= 0.2) withsubstance use measures; here PCL-YV Total scores in thefemale adolescent sample were significantly positively cor-related with years of regular use, r (38)=0.57, p <0.001, butnot substance dependence, r (39)=−0.26, p =0.10. Total

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PCL-YV scores were significantly correlated with age,r (39)=−0.36, p =0.02. Like adult and adolescent males,there were no significant correlations between brain volumeand PCL scores: Total, r (39)=0.00, p =0.99; Factor 1,r (39)=0.10, p =0.53; Factor 2, r (39)=−0.07, p =0.69.

Regarding other mental illness diagnoses and differenceson PCL-YV scores, there were no significant differencesbetween those with a past or present anxiety diagnosis andthose without: Total, t (36)=−1.81, p =0.08; Factor 1,t (36)=−1.92, p =0.06; Factor 2, t (36)=−1.31, p =0.20;those with a past or present depression diagnosis and thosewithout: Total, t(36)=0.13, p =0.90; Factor 1, t (36)=−0.03,p =0.98; Factor 2, t(36)=−0.29, p =0.77; and those withADHD and those without: Total, t (36)=1.25, p =0.22; Fac-tor 1, t (36)=1.23, p =0.23; Factor 2, t (36)=1.35, p =0.18.

Results

Were Psychopathic Traits (PCL-YV Total scores) Associatedwith Brain Structure in Incarcerated Adolescent Females?

Consistent with hypotheses, cluster threshold (1366 voxels)analyses across the whole brain showed that gray matter

volumes in paralimbic regions were negatively associatedwith PCL-YV Total scores, controlling for brain volume,substance dependence, and age. Two clusters in the (1)orbitofrontal cortex, extending into right parahippocampalcortex and temporal pole, and in the (2) left temporal pole,extending to left parahippocampal cortex at a trend level, werefound (Fig. 1). There were no clusters that were positivelyassociated with PCL-YV Total scores. The widespread natureof these results is consistent with the large extent of structuraldifferences in psychopathy evidenced in adult men and maleadolescents (Ermer et al. 2012, 2013).

Were Results Robust to Alternative Models?

In the analysiswith years of regular drug use as the substance usecovariate instead of substance dependence (Figure S1), negativecorrelations between gray matter volumes and PCL-YV Totalscores were still found in the lateral orbitofrontal cortex, tempo-ral poles, and insula. The relationship between PCL-YV scoresand medial orbitofrontal cortex gray matter volume did notsurvive correction for multiple comparisons in this analysis.Similarly, there were fewer significant psychopathy-related ef-fects in the parahippocampal gyri when years of regular drug usewas the covariate.

Table 1 Comparison of means (and standard deviations) or counts (and percent) for descriptive variables for female (N=39; present study) and male(N =191; Ermer et al. 2013) adolescent samples

Variable Females Males t or Χ2 p r or phi

Age at Scan 17.6 (1.10) 17.6 (1.12) t(228)=0.16 0.87 0.01

IQ 97.2 (12.72) 92.8 (12.06) t(211)=1.85 0.07 0.13

Substance Dependence 2.5 (1.62) 2.2 (1.63) t(228)=0.88 0.38 0.06

Years of Regular Use 0.60 (0.29) 0.55 (0.27) t(220)=0.90 0.37 0.06

Psychopathic Traits

Total Scores 22.4 (6.43) 23.6 (6.19) t(228)=1.04 0.30 0.07

Factor 1 (interpersonal/affective) 6.6 (3.37) 6.6 (3.14) t(228)=0.16 0.88 0.01

Factor 2 (lifestyle/antisocial) 14.4 (3.28) 14.7 (3.28) t(228)=0.48 0.63 0.03

KSADS Diagnosesa (n /percent)

Anxiety Disorders 14 (36.8 %) 16 (8.4 %) Χ2(1)=22.56 < 0.001* 0.31

Depressive Disorders 15 (39.5 %) 31 (16.2 %) Χ2(1)=10.67 < 0.01* 0.22

Attention Deficit-Hyperactivity Disorder 11 (28.9 %) 22 (11.5 %) Χ2(1)=7.81 < 0.01* 0.19

Oppositional Defiant Disorder 9 (23.7 %) 57 (29.8 %) Χ2(1)=0.59 0.44 0.05

Conduct Disorder 35 (92.1 %) 180 (94.3 %) Χ2(1)=0.41 0.52 0.04

Childhood Onset 15 (39.5 %) 96 (50.3 %) Χ2(1)=1.55 0.21 0.08

Adolescent Onset 20 (52.6 %) 84 (44.0 %) Χ2(1)=0.91 0.34 0.06

Criminal Convictionsb

Total 8.3 (7.80) 7.7 (7.84) t(100)=0.38 0.70 0.04

Violent 0.8 (1.01) 1.6 (1.96) t(100)=1.82 0.07 0.18

Non-violent 7.4 (7.69) 6.6 (7.54) t(100)=0.58 0.56 0.06

Point-biserial r is listed as a measure of effect size. a Includes both current and past diagnoses. b Criminal conviction data available for n =24 females andn =78 males. *Significant at the p <0.05 level (two-tailed). Trend-level p-values are in italics

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In the analyses that included anxiety diagnosis, there wereseveral frontal, temporal, and parietal areas negatively associ-ated with psychopathy scores (Table S2; Figures S2 and S3).There were no areas positively associated with psychopathyscores.

Were Psychopathic Traits Associated with Brain Structurein Regions of Interest?

Region of interest analyses on 10 mm diameter spheresaround peak coordinates from an independent adult sample(Ermer et al. 2012) showed that PCL-YV scores were signif-icantly (FWE p <0.05) negatively associated with gray mattervolumes (Table 2) in the left and right lateral orbitofrontalcortex, and that a statistical trend (in the negative direction)was found for the medial orbitofrontal cortex.

Were PCL-YV Factors Associated with Brain Structure?

In multiple regression analyses evaluating the relationshipbetween the PCL-YV factors and regional graymatter volumesin the female youth sample, both factors were included in themodel simultaneously, in addition to brain volume, substancedependence, and age covariates (Table S1). Cluster extentthreshold whole brain analysis (1366 voxels) showed thatFactor 1 scores were negatively associated with gray mattervolumes in clusters in left and right parahippocampal regions(Fig. 2, Panel a). Factor 2 scores were negatively associatedwith gray matter volumes in clusters in the orbitofrontal cortexand cuneus/lingual gyrus (Fig. 2, Panel b). There were noregions with gray matter volumes positively associated withFactor 1 or Factor 2 scores.

Did Participant Sex Moderate the Effects of PsychopathicTraits?

We performed a multiple regression analysis that included apreviously-published sample of incarcerated adolescent malesfrom the same facility (N =191; Ermer et al. 2013) and theincarcerated adolescent females, with substance dependence,brain volume, age, participant sex, PCL-YV Total scores, anda participant sex by PCL-YV Total score interaction termincluded as predictors. There were no regions significantlyassociated with the interaction term using the cluster-correctedthreshold analyses described above (1334 voxel-extent), sug-gesting no moderating effect of participant sex on the rela-tionship between PCL-YV scores and regional gray mattervolume. A scatterplot illustration of these effects for the lefttemporal pole (x =−42 y =0 z =−44) can be found in Supple-mental Material (Figure S4). Depicted in this figure are maineffects for both participant sex and PCL-YV scores, but nointeraction. In the direct comparison between males and fe-males (Figure S5), we found greater volumes in females inbilateral caudate, parts of orbitofrontal cortex, and cingulatecortex. Males had greater gray matter volumes in anteriortemporal cortex, left insula, and medial temporal structuresincluding the amygdala and hippocampus.

Discussion

Consistent with hypotheses, regional gray matter volumes werenegatively related to psychopathic traits in limbic and paralimbicareas, including orbitofrontal cortex, parahippocampal cortex,temporal poles, and left hippocampus in a maximum-securityfemale adolescent sample. These results are consistent withprevious structural MRI findings in adult and adolescent malesassessed for psychopathy (Ermer et al. 2012, 2013). Similar tothe present findings in incarcerated female youth, adolescent(Ermer et al. 2013) and adult (Ermer et al. 2012) incarcerated

Fig. 1 Regional gray matter volumes negatively associated with Psy-chopathy Checklist-Youth Version (PCL-YV) Total scores in females,controlling for brain volume, age at scan, and substance dependence. Allvoxels indicated in blue color map represent regions that are significant inthe whole brain at p<0.05 and 1366-voxel extent. Coordinates are inMontreal Neurological Institute (MNI) space. The color bar represents t-values. Significantly associated clusters can be found in the orbitofrontalcortex, extending into right parahippocampal cortex and temporal pole,and in the left parahippocampal cortex, extending into the temporal pole

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males also showed reduced gray matter associated with psy-chopathy scores in a large cluster in the orbitofrontal cortex,extending into the parahippocampal cortex and temporal poles.The consistency in the brain effects across sex and age lendsignificant support for the hypotheses that these regions areimplicated in psychopathy.

The gray matter regions found in the present study havealso been consistently identified as impaired in functional brainimaging studies of psychopathy. For example, orbitofrontalcortex dysfunction has been found in psychopathy studies ofemotional processing and aversive conditioning in males

(Muller et al. 2003; Veit et al. 2002). Similarly, parahippo-campal cortex is associated with reduced activation in malepsychopaths compared to controls while viewing negativepictures (Muller et al. 2003) and during the processing ofaffective stimuli (Kiehl et al. 2001). The temporal poles werealso found to be under-reactive for emotional stimuli during amemory task (Kiehl et al. 2001). Furthermore, engagement ofthe hippocampus, a region important for aversive conditioning(Buchel et al. 1999), was negatively related to psychopathyscores in violent male offenders (Laakso et al. 2001). Here wefound reduced gray matter in these regions to be associated

Table 2 Small volume correction tests (SVC; 10 mm diameter spheres) in nine regions of interest (ROI) in adolescent females

Peak for Search (from adults) Peak within Volume (from adolescent females)

Region H x y z x y z t-value p (unc.) FWE

Lateral OFC L −26 32 −20 −30 34 −22 4.51 <0.001 0.001

R 28 48 −18 26 52 −18 2.83 0.004 0.036

Medial OFC – 4 52 −20 2 48 −22 2.40 0.011 0.080

ACC – −2 48 2 0 46 −2 1.04 0.141 0.395

Temporal Pole L −38 12 −40 −40 16 −38 2.28 0.014 0.097

R 34 20 −38 32 22 −34 2.24 0.016 0.104

Parahippocampal L −32 −2 −28 −36 0 −30 1.61 0.056 0.240

R 34 −8 −24 34 −10 −28 1.75 0.044 0.205

PCC – −6 −54 32 −4 −52 28 0.32 0.312 0.548

Brain volume, age at scan, and substance dependence were included in the model as covariates, in addition to the predictor of interest (PsychopathyChecklist-Youth Version [PCL-YV] Total scores). All associations reflect a negative relation between PCL-YV scores and regional gray matter volumesin adolescent females.OFC orbitofrontal cortex; ACC anterior cingulate cortex; PCC posterior cingulate cortex;H Hemisphere; L Left; R Right; FWEfamily wise error rate. Search coordinates based on an independent adult sample (N =254; Ermer et al. 2012). Montreal Neurological Institute (MNI) x, y,and z coordinates, t-values, and p-values (uncorrected) are for the peak voxel in each region

Fig. 2 Panel a : Regional graymatter volumes negativelyassociated with PsychopathyChecklist-Youth Version(PCL-YV) Factor 1 scores infemales, controlling for brainvolume, age at scan, substancedependence, and Factor 2 scores.Panel b : Regional gray mattervolumes negatively associatedwith PCL-YV Factor 2 scores infemales, controlling for brainvolume, age at scan, substancedependence, and Factor 1 scores.These regions are significant inthe whole brain at p <0.05 and1366-voxel extent. Coordinatesare in Montreal NeurologicalInstitute (MNI) space, and thecolor bar represents t-values

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with higher PCL-YV scores in adolescent females. Though itis not yet known whether fMRI results can be directly attrib-utable to structural differences measured by VBM studies, thefindings presented here are consistent with the functionalliterature on psychopathy. Future work should attempt to ad-dress this structure-function relationship more fully.

The present results are relevant for the issue of whetherpsychopathy in females is a valid and useful construct.Though studies of psychopathy in females are relativelysparse, a few previous studies have indicated psychopathy-related similarities with males. Kennealy et al. (2007) foundsimilar correlations in male and female samples betweenpsychopathy scores and a variety of behavioral correlatesincluding age of onset of criminal activity, number of nonvi-olent and violent crimes, nonviolent and violent institutionalmisconduct, and interpersonal violence and aggression. As inmen, psychopathy scores in women are associated with defi-cient emotional responding (Sutton et al. 2002) and dysfunc-tional selective attention (Vitale et al. 2007). It is also relevantto note that male and female patients with orbitofrontal brainlesions display similar psychopathic-like behaviors (Andersonet al. 1999; Bechara et al. 1994). These latter effects suggestbrain damage to the same regions implicated in the presentstudy lead to similar sex-related impairments and sym-ptomology. Thus, the present psychopathy-related neuroana-tomical findings may be related to these behavioral and affec-tive symptoms, and lend further support to the validity of theconstruct of psychopathy to women. Despite these similari-ties, it should be noted that not all studies have found consis-tency of effects in psychopathy across male and female sam-ples. For example, one study (Vitale and Newman 2001)found that response perseveration may not be as prominent afeature of female psychopathy as it is in male psychopathy(Newman et al. 1987).

Our results need to be considered with respect to thebroader literature. In contrast with recent studies of males(Ermer et al. 2012, 2013), adolescent females in the presentstudy did not show any significant differences in the posteriorcingulate. Additionally, a cluster of positive association inmedial prefrontal cortex between psychopathic traits and graymatter volume in adolescent males (Ermer et al. 2013) was notfound here in the adolescent females. One potential reason forthese findings is the difference in sample sizes among theadolescent male (N =191), adult male (N =254) and adoles-cent female (N =39) studies. It should be noted that a test ofthe interaction between psychopathic traits and participant sexrevealed no significant regions.

Whereas we found reduced gray matter volumes in femaleadolescences with elevated psychopathic traits, one study hasreported increased gray matter in medial orbitofrontal cortex,anterior cingulate, and bilateral temporal regions in boys withcallous and unemotional traits (De Brito et al. 2009). Theseinconsistencies raise the possibility that the differences

between these studies may be due to methodological issues.The two studies differed in a number of important ways, includ-ing the samples (incarcerated female youth versus male youth inthe community), assessment of traits (expert-rated PCL-YVversus self-report Antisocial Process Screening Device), andchoice of covariates (age, brain volume, and substance depen-dence versus full-scale IQ estimate and hyperactivity-inattentionsymptoms). We have previously shown that there is substan-tial disagreement between various procedures for assessingpsychopathic traits in high-risk youth (Fink et al. 2012) andthere are likely differences in the severity of psychopathictraits from forensic samples compared to community samples.Choice of covariates and the relationships among covariatesand outcome variables are also likely to affect the results ofVBM studies. In particular, the influence of group differencesin brain volume is a critical variable to examine (De Brito et al.2009). Furthermore, there are multiple ways of quantifyingsubstance use. Here we used two measures, substance depen-dence and years of regular substance use, to remove varianceassociated with the potential effects of substance use on brainstructure. Psychopathy and substance use disorders are highlycomorbid (O’Neill et al. 2003; Smith and Newman 1990), andthere is evidence that psychopathic traits can develop early inlife (Frick et al. 1994), often prior to the initiation of substanceuse. Thus it is possible that by removing variance associatedwith substance use we also removed variance associated withpsychopathic traits. Future studies need to consider carefullythe above factors and determine how potential moderatingvariables may influence the outcomes reported.

There are a number of potential study limitations thatshould be kept in mind. Similar to incarcerated adolescentsin general, the incarcerated female youth sample had a numberof comorbidities with psychopathy, including ADHD, anxi-ety,2 and depressive disorders. Here psychopathy scores werenot different between ADHD and depressive disorder groups,and in the analyses that included anxiety diagnosis, resultswere substantively the same as in the primary analyses. How-ever, it is always possible that variance associated with thesecomorbidities was not entirely accounted for (Miller andChapman 2001).

The present sample size (N =39) is similar to other pub-lished studies of psychopathy, but relatively small comparedto recent VBM studies of males (Ns>190; Ermer et al. 2012,2013). Thus, it is possible that any differences between thepresent sample and other recent VBM studies may be due tolack of power. Also, we employed a dimensional model toexamine psychopathy-related effects on brain structure andwe did not include a direct comparison to a healthy controlgroup. Thus, it is important for future studies to examine

2 Note that including anxiety diagnosis in the analyses revealed moreregions that were significantly negatively associated with psychopathictraits compared to the analyses without anxiety diagnosis.

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psychopathy-related effects in non-clinical healthy controlsamples. Despite these potential limitations, the consistencybetween the present psychopathy-related results in an incar-cerated female youth sample and those found in adult andadolescent male samples provides strong evidence of a unitarydisorder across both age and sex.

In summary, this is the first study of regional gray matterdifferences in adolescent female incarcerated offenders usingthe PCL-YV. We believe that identification of these at-riskyouth is crucial for successful treatment. In line with recentstudies showing positive treatment outcomes for some of themost severe male adolescent offenders (Caldwell et al. 2006a),female adolescents with psychopathic traits could benefit fromearly identification and intensive treatment as well.

Acknowledgments This research was supported by NIMH R01MH071896 (PI: KAK). EE was supported by NIMH NRSA F32MH086247. We are grateful to the staff and clients (and parents) at theYouth Diagnostic and Detention Facility and the New Mexico Children,Youth and Families Department for their support and assistance in mak-ing this research possible.

Conflict of Interest The authors declare that they have no conflict ofinterest.

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