Literature review paper

Child Neuropsychology, 2012, 18 (2), 182–189 http://www.psypress.com/childneuropsych ISSN: 0929-7049 print / 1744-4136 online http://dx.doi.org/10.1080/09297049.2011.595400

Childhood abuse and neglect and cognitive flexibility in adolescents

Marisa N. Spann1,2 , Linda C. Mayes3,4 , Jessica H. Kalmar2 , Joanne Guiney2,4 , Fay Y. Womer2 , Brian Pittman2 , Carolyn M. Mazure2,3 , Rajita Sinha2,3 , and Hilary P. Blumberg2,4

1Department of Neurosurgery, Yale University School of Medicine, New Haven, CT, USA 2Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA 3Department of Psychology, Yale University, New Haven, CT, USA 4Child Study Center, Yale University School of Medicine, New Haven, CT, USA

Childhood maltreatment (CM) has been associated with diminished executive functioning in chil- dren and adults; however, there is a relative paucity of study of executive function in adolescents exposed to CM. Yet, executive dysfunction in adolescence may have important adverse consequences including increased vulnerability to risky behaviors and impaired school functioning. This study inves- tigates the relationship between self-reported CM and an executive function, cognitive flexibility, in adolescents without identified psychiatric disorders. Effects of physical and emotional, abuse and neglect, maltreatment subtypes were explored. Thirty adolescents ages 12–17 years, 50% females, completed the retrospective self-report Childhood Trauma Questionnaire (CTQ) and were admin- istered the Wisconsin Card Sorting Test (WCST). Correlational analyses assessed the relationship between WCST perseverative error scores norm-referenced for age and education with CTQ total scores. The relationship with nonperseverative errors, as well as with physical and emotional abuse and neglect CM subscores, were explored. Total CTQ scores showed significant associations with perseverative errors on the WCST, but not with nonperseverative errors. Significant associations with perseverative errors were seen for physical abuse and physical neglect among the CTQ subscales. The results suggest both physical abuse and physical neglect are associated with diminished cogni- tive flexibility in adolescents. These effects were detected in adolescents without identified psychiatric diagnoses suggesting the importance of considering executive dysfunction in adolescents exposed to CM who may not meet diagnostic criteria for an Axis I disorder and that tests of perseverative errors, such as those of the WCST, may be sensitive indicators of this dysfunction.

Keywords: Adolescent; Child abuse; Child neglect; Executive function; Cognition.

This work was supported by the National Institute of Health (NIH) Roadmap for Medical Research Common Fund grant UL1-DE19586 (RS) and the NIH Roadmap for Medical Research/Common Fund (RS), National Institute of Drug Abuse RL1DA024856 (HPB, JHK, LCM), K05DA020091 (LCM) and PL1-DA24859 (RS), the National Institute of Mental Health R01MH69747 (HPB), T32MH14276 (JHK), Women’s Health Research at Yale (HPB, CMM), the National Alliance for Research in Schizophrenia and Depression (HPB, JHK), the Attias Family Foundation (HPB), Marcia Simon Kaplan (JHK), and the Klingenstein Foundation (JHK). We thank Susan Quatrano, Philip Markovich, Kathryn Armstrong, Sarah Nicholls, Matthew Freiburger, and Matthew Hirschtritt for their efforts with the research subjects and the research subjects for their participation.

Address correspondence to Hilary P. Blumberg, MD, Department of Psychiatry, Yale University School of Medicine, 300 George Street, Suite 901, New Haven, CT 06511, USA. E-mail: [email protected]

© 2012 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business

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Children and adult victims of abuse and neglect show disruptions in executive functions (Minzenberg, Poole, & Vinogradov, 2008; Perez & Widom, 1994; Porter, Lawson, & Bigler, 2005). The relationship between childhood abuse and neglect with disturbances in executive functions in adolescents has received relatively little study. Yet, adolescence is a period during which a range of executive function abilities mature and reliance on frontal executive functions becomes increasingly necessary. Hence, compromised executive functioning in adolescents can have important adverse consequences.

Prepubertal children have demonstrated decreases in executive function performance on neuropsychological tests, including measures of attention, adaptive response inhi- bition and cognitive flexibility, in association with physical abuse and neglect (Beers & De Bellis, 2002; De Bellis, Hooper, Spratt, & Woolley, 2009; Deprince, Weinzierl, & Combs, 2009; Nolin & Ethier, 2007; Pears & Fisher, 2005; Prasad, Kramer, & Ewing-Cobbs, 2005). This suggests that physical abuse and neglect may adversely affect maturation of executive functions. Alterations in the developmental trajectory of executive function could lead to enduring developmental effects in adolescence and adulthood.

Associations between trauma and executive function have been demonstrated con- sistently in adults (Brandes et al., 2002; Diamond, Muller, Rondeau, & Rich, 2001; Gil, Calev, Greenberg, Kugelmass, & Lerer, 1990; Stein, Kennedy, & Twamley, 2002; Twamley, Hami, & Stein, 2004). The studies focused largely on adults with psychiatric disorders, pre- dominantly with posttraumatic stress disorder (PTSD) and often did not assess effects of childhood abuse and neglect specifically. Studies of adults with a history of childhood mal- treatment (CM) and without a psychiatric condition support the presence of adverse effects on aspects of executive functioning in the absence of psychopathology, including cognitive flexibility (Brandes et al., 2002; Navalta, Polcari, Webster, Boghossian, & Teicher, 2006; Stein et al., 2002; Twamley et al., 2004).

The findings in children and adults exposed to CM implicate abnormalities in execu- tive functioning in adolescents exposed to CM; however, there are limited prior studies of executive functioning in adolescents exposed to CM, and specifically of cognitive flexibility. In one study, female adolescents with PTSD who had been sexually abused demonstrated increased cognitive interference on a color-word Stroop task (Freeman & Beck, 2000). A study of adolescent boys in a therapeutic school who had a history of child- hood physical abuse demonstrated difficulties in learning to avoid maladaptive responses on a passive avoidance learning task, as compared to boys in the therapeutic school who had not been abused and boys in local public schools (Mezzacappa, Kindlon, & Earls, 2001). These studies support the presence of vulnerability to executive function prob- lems in adolescents exposed to CM and suggest difficulties in the development of adaptive cognitive flexibility in adolescents exposed to CM; although this function was not tested specifically.

The current study investigates the relationship between self-reported history of CM on the Childhood Trauma Questionnaire (CTQ) and cognitive flexibility as assessed by perseverative errors measured on the Wisconsin Card Sorting Test (WCST), the WCST measures most sensitive to disturbances in frontal executive function (Greve, Stickle, Love, Bianchini, & Stanford, 2005; Heaton, Chelune, Talley, Kay, & Curtis, 1993). The adoles- cents were without psychiatric diagnoses, diminishing potential confounds of psychiatric symptoms. It was hypothesized that higher CTQ scores would be associated with more perseverative errors on the WCST.

184 M. N. SPANN ET AL.

METHODS

Participants consisted of 15 male and 15 female adolescents, ages 12–17 years, with a mean age of 14.8 years (SD = 1.6) from the greater New Haven commu- nity. The adolescents were all enrolled in school and had a mean ninth grade level of education. Ethnic distribution was Caucasian (40%), Black (37%), Latino (10%), and Multiracial (13%). Mean socioeconomic status (SES), estimated using the Hollingshead Social Status Scale (Hollingshead, 1975), was 39.5 (SD = 13.6), which falls in approx- imately the middle range of SES scores. Participants did not meet criteria for a major Axis I disorder as confirmed by administration of the revised Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version 2.0 (K-SADS-PL; Kaufman, Birmaher, Brent, Rau, & Ryan, 1996) to the participants and a parent or guardian. There was no history of psychiatric disorder in a first-degree relative as assessed by the Family History Screen for Epidemiologic Studies (Lish, Weissman, Adams, Hoven, & Bird, 1995). No participant had a history of major medical disorder or neurological disorder, loss of consciousness for 5 or more minutes or intelligence quotient below 70.

After a complete description of the research, written informed consent was obtained from parents/guardians. Written informed assent was obtained from minors. This research was approved by the institutional review board of the Yale School of Medicine.

All subjects completed the CTQ (Bernstein et al., 1994, 2003; Bernstein & Fink, 1998), a 28-item retrospective self-report questionnaire. In the CTQ, the CM domains of physical abuse, sexual abuse, emotional abuse, physical neglect, and emotional neglect are each assessed by five items that participants rate on a 5-point scale ranging from “never true” to “very often true” according to the frequency with which each event occurred. Physical abuse is defined as bodily assaults on a child by an older person that poses a risk for or results in injury, sexual abuse as sexual contact, or conduct between a child and an older person; emotional abuse is defined as verbal assaults on a child’s sense of worth or well-being, or any humiliating, demeaning, or threatening behavior directed toward a child by an older person; physical neglect is defined as failure of caregivers to provide a child’s basic physical needs; and emotional neglect is defined as the failure of caretakers to provide basic psychological and emotional needs (Bernstein et al., 1994). Scores across the five CM domains are summed for a Total CTQ score; the five subscales scores permit assessments for effects in each of the five abuse and neglect domains. Internal consistency has ranged from .76 to .92 (Bernstein et al., 1994, 1997, 2003; Bernstein & Fink, 1998; Messman-Moore & Brown, 2004; Wolfe, Scott, Wekerle, & Pittman, 2001).

Each subject was also administered the Wisconsin Card Sorting Test (WCST; Heaton et al., 1993). The perseverative error subscore of the WCST has been shown to be highly sensitive to frontal lobe dysfunction (Greve et al., 2005; Heaton et al., 1993; Lezak, Howieson, & Loring, 2004; Sutker, Moan, & Allain, 1983) and was utilized for this study. Nonperseverative errors were also explored. Perseverative and nonperseverative norm- referenced scores, which adjust for age and level of education, served as the dependent measures in analyses.

Correlation analyses and t-tests were performed to assess for potential effects of age and gender on CTQ and WCST scores. Pearson Correlation analyses assessed the rela- tionships between CTQ total scores and WCST perseverative and nonperseverative errors. Findings were considered significant for p < .025, adjusted for the two WCST performance measures. For the WCST measure(s) showing significant associations with Total CTQ,

CHILDHOOD MALTREATMENT AND COGNITIVE FLEXIBILITY 185

associations were explored for CTQ physical abuse, physical neglect, emotional abuse, and emotional neglect subscores. As only three subjects reported a history of sexual abuse, effects of these were not tested in analyses. All significant findings are reported below. Analyses were conducted using SAS, version 9.1 (SAS, 2004).

RESULTS AND DISCUSSION

The current study provides evidence supportive of associations between self-reported CM and diminished cognitive flexibility in adolescents. Specifically, higher Total CTQ scores were associated with increased perseverative errors (lower norm-referenced scores), r = !.42, p = .02 (Figure 1), but did not show significant associations with nonpersevera- tive errors. Correlations between norm-referenced scores for perseverative errors and CTQ subscores were significant for physical abuse, r = !.43, p = .019 and physical neglect r = !.46, p = .011. There were no significant associations between age and CTQ Total or subscores, or between gender and either WCST or CTQ scores. There were also no signif- icant associations between emotional abuse and neglect and perseverative error scores. These results suggest that both childhood physical abuse and neglect may negatively impact the development of cognitive flexibility leading to dysfunction in the adolescent epoch.

The findings are consistent with reports of executive dysfunction in prepubertal chil- dren in association with physical abuse and neglect. This suggests that this dysfunction may persist during the adolescent period and/or may influence the trajectory of execu- tive development into adolescence. Determining whether executive dysfunction progresses from the prepubertal to adolescent epoch will require longitudinal studies that cross these developmental stages.

The finding in the adolescents of an association between perseverative errors and physical neglect is relatively novel. Prior reports of effects of early physical abuse on executive functioning in adults, as discussed above, suggest that these alterations may extend beyond childhood. Enduring effects of childhood physical neglect in adulthood have received little study. The current results suggest that physical neglect in childhood may also adversely affect the development of specific executive function capacities and

140 130 120 110 100

P e rs

ev e ra

ti ve

E rr

o rs

90 80 70 60 50

20 30 CTQ Total Scores

40 50

Figure 1 The association between Childhood Trauma Questionnaire scores and WCST performance. The graph shows Wisconsin Card Sorting perseverative error scores norm-referenced to adjust for age and education as a function of total scores on the Childhood Trauma Questionnaire (CTQ Total Scores). The negative associations were significant indicating reports of higher childhood maltreatment were associated with lower performance, that is, more perseverative errors.

186 M. N. SPANN ET AL.

the dysfunction persists at least into adolescence. This highlights the necessity for further studies of adolescents and adults exposed to physical neglect, as well as physical abuse, in childhood.

The neurobiological mechanisms that may mediate the effects of CM on execu- tive function development cannot be determined from this study. Late childhood and adolescence are critical periods in the development of prefrontal cortical regions that subserve the maturation of executive functions, such as cognitive flexibility (Anderson, Anderson, Northam, Jacobs, & Catroppa, 2001; Bourgeois, Goldman-Rakic, & Rakic, 1994; Erickson, Akil, Levey, & Lewis, 1998; Klingberg, Vaidya, Gabrieli, Moseley, & Hedehus, 1999; Lewis, 1997; Luciana, Conklin, Hooper, & Yarger, 2005; Paus, 2004; Welsh, Pennington, & Groisser, 1991). Structural MRI studies show reduced brain frontal lobe volume in children exposed to CM (Cicchetti & Toth, 2005; De Bellis, 2005; Minzenberg et al., 2008; Weiss, Longhurst, & Mazure, 1999). Mechanisms theorized to mediate these effects include those related to the hypothalamic-pituitary-adrenal (HPA) axis (Maciejewski & Mazure, 2006; Weiss et al., 1999). Together, these data suggest adverse effects of CM on frontal development may underlie the effects reported herein. Physical neglect has received less study than physical abuse. However, it has the potential to have potent effects on frontal developmental as effects could derive both from emo- tional aspects of the neglect, effects on HPA functioning, as well as from deprivation of basic physical needs, such as nutrition and activity, critical for healthy neurodevelopment. Future studies of mechanisms that mediate effects of physical abuse and neglect on frontal maturation and associated executive functions are needed.

Small sample size is an important limitation of this study. Another limitation is the risk of potential recall bias as CM history was based on retrospective self-report. Although the CTQ has shown excellent reliability and validity in adolescent and adult community and psychiatric samples (Bernstein & Fink, 1998; Bernstein et al., 2003; Paivio & Cramer, 2004; Scher, Stein, Asmundson, McCreary, & Forde, 2001), multiple informant data or assessment of the specific ages of the CM were not available. Future studies that investigate specific ages at which the abuse and neglect occurred would be important in understanding the critical periods during which abuse and neglect influence adolescent dysfunction and the developmental mechanisms that mediate the effects. A further limitation is our focus on cognitive flexibility. Future studies that include both more comprehensive executive function testing, as well as that parse specific functions that may contribute to persevera- tive responses, could permit examination of the scope of executive dysfunction and more specifically define the abilities most affected. Identification of skills more likely to be pre- served could aid researchers in constructing intervention strategies for CM exposure that draw on intact cognitive capacities that could potentially compensate for and minimize dysfunction.

The current study begins to fill the gap in the CM literature by providing evidence that adolescents exposed to childhood physical abuse and neglect may not express symp- toms that meet full Diagnostic and Statistical Manual of Mental Disorders, fourth edition (DSM-IV ; American Psychiatric Association, 2000) criteria for an Axis I disorder but may have alterations in the development of executive functions, including the focus of this study, cognitive flexibility. This is important as executive dysfunction may present challenges to adolescents, such as difficulty with school performance and diminished ability to adap- tively inhibit behavior that in turn could contribute to increased engagement in risk-taking behaviors as well as elevated risk for psychiatric disorders (Batten, Aslan, Maciejewski, & Mazure, 2004; Maciejewski & Mazure, 2006; Weiss et al., 1999; Widom, 1999). Findings

CHILDHOOD MALTREATMENT AND COGNITIVE FLEXIBILITY 187

on the perseverative responses measure of the WCST suggest that such tests may provide sensitive indicators of difficulties in adolescents who have been exposed to CM that may otherwise elude detection during more standard clinical examinations.

Original manuscript received September 23, 2010 Revised manuscript accepted January 24, 2011

First published online September 26, 2011

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