J Neural Transm (2009) 116:117120 DOI 10.

1007/s00702-008-0154-0

BIOLOGICAL CHILD AND ADOLESCENT PSYCHIATRY - SHORT COMMUNICATION

Emotional memory in ADHD patients with and without comorbid ODD/CD

Kerstin Krauel Emrah Duzel Hermann Hinrichs Thomas Rellum Stephanie Santel Lioba Baving

Received: 26 March 2008 / Accepted: 26 October 2008 / Published online: 19 November 2008 Springer-Verlag 2008

Abstract The present study investigated whether children and adolescents with attention decit hyperactivity disorder (ADHD) and comorbid oppositional deant disorder (ODD) or conduct disorder (CD) show a memory bias for negative emotional pictures. Subjects participated in an incidental memory paradigm involving neutral, positive and negative pictures. In ADHD only patients, memory performance was enhanced to the level of healthy control subjects both by positive and negative pictures, whereas in ADHD patients with comorbid ODD/CD, memory performance was only normalized by negative pictures.

Keywords

ADHD Memory Emotion ODD/CD

Introduction Patients with attention decit hyperactivity disorder (ADHD) show early and persistent decits in attentional functions, impulse and motor control. As many as 4060% of ADHD patients are also diagnosed with comorbid oppositional deant disorder (ODD) or conduct disorder (CD) (Maughan et al. 2004) leading to more severe and chronical impairment in school performance, family functioning and peer relationships than patients with ADHD only (Kuhne et al. 1997). Patients with ADHD ? ODD/CD are often characterized by negative emotionality and appear to preferentially process negative information, especially in ambiguous social situations (Waschbusch et al. 2002). However, there is also evidence that this patient group is less affected by negative emotional information, since rating studies as well as psychophysiological studies suggest that they perceive negative pictures or aversive stimuli as less intense and less arousing than children with ADHD only or healthy control subjects (Herpertz et al. 2005; Sharp et al. 2006). Whether or not negative emotional content is differently processed by ADHD patients ? ODD/CD is highly relevant, since processing biases inevitably affect the interpretation of environmental information and are crucial for decision making and motivating behavior (Lemerise and Arsenio 2000). Episodic memory performance is a sensitive measure for the subjective relevance of an episode or event, since meaningful information is preferably transferred into memory even in the absence of intentional encoding (LaBar and Cabeza 2006). If ADHD patients ? ODD/CD

K. Krauel (&) H. Hinrichs Department of Neurology and Center for Advanced Imaging, University of Magdeburg, Leipziger Strasse 44, 39120 Magdeburg, Germany e-mail: kerstin.krauel@med.ovgu.de E. Duzel Institute of Cognitive Neuroscience, University College London, London, UK E. Duzel Institute of Cognitive Neurology and Dementia Research, University of Magdeburg, Magdeburg, Germany T. Rellum S. Santel Department of Child and Adolescent Psychiatry, University of Magdeburg, Magdeburg, Germany L. Baving Department of Child and Adolescent Psychiatry and Psychotherapy, Center for Integrative Psychiatry, Kiel, Germany L. Baving Department of Child and Adolescent Psychiatry, University Medical Center, Utrecht, The Netherlands

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indeed preferentially process negative information, they should show a stronger memory bias for negative pictures than healthy control children and patients with ADHD only.

Patients and methods Thirty male ADHD patients and 25 male healthy control subjects participated in the study. All subjects and their parents were interviewed with the Revised Schedule for Affective Disorders and Schizophrenia for School-Age Children: Present and Lifetime Version (Delmo et al. 2000). Patients who met present or lifetime criteria for any other psychiatric disorder than ODD or CD were excluded from the sample. Control subjects were excluded if there was evidence of any previous or current psychiatric disorder. Fourteen patients met diagnostic criteria for ADHD only according to the DSM-IV, 16 patients were additionally diagnosed with ODD (N = 8) or CD (N = 8). Healthy control subjects (13.9 years, SD = 1.8), ADHD only (13.9 years, SD = 1.3) and ADHD patients ? ODD/ CD (13.2 years, SD = 1.2) did not differ in age or intelligence (ADHD only: IQ = 107.6, SD = 10.4; ADHD ? ODD/CD: IQ = 105.0, SD = 9.5; healthy control subjects: IQ = 111.3, SD = 10.5). ADHD subjects tended to score higher on the anxious/depressed scale of the Youth Self Report (Achenbach 1991) than healthy control subjects (F(2,47) = 3.13, p \ 0.1), but single comparisons did not reach signicance and T values were below 60 for all groups. In each ADHD groups, about 40% of the participants received stimulant medication (ADHD only: 5/14; ADHD ? ODD/CD: 7/16), which was discontinued at least 24 h prior to the experiment. All subjects and their parents provided written informed assent/consent after complete description of the study. Subjects were reimbursed for their participation in the study with a voucher of 6 per hour. The experiment was divided into an incidental encoding phase and an immediate recognition memory test. The stimulus material (n = 360) contained pictures from the International Affective Picture System (Lang et al. 2001) as well as similar pictures from other sources. Fifty percent of the pictures were of neutral content, 25% of positive and 25% of negative content. In the encoding phase, pictures were presented in the course of two tasks that were unrelated to the emotional content of the picture: subjects either had to decide whether a rectangle or an oval was superimposed on the picture or whether or not there was a human being in the picture. Decisions were rendered via button press. Pictures were presented for 600 ms and were preceded by a xation cross and an instruction slide (duration: 1,000 ms) reminding the subjects of their current

task. The duration of the xation cross varied between 2,400 and 6,400 ms. In the recognition test, pictures from the encoding phase (n = 240) were presented along with 120 new stimuli in randomized order (stimulus duration: 1,000 ms, xation cross: 3,000 ms). Subjects had to judge via mouse click whether the picture was old or new. Recognition performance (corrected hitrate) was measured by subtracting false alarms, new pictures misjudged as old, from correctly recognized old items to correct for response biases. Effects of GROUP and stimulus VALENCE on performance data during encoding and recognition were analyzed in two-way ANOVAs with repeated measurements separately for encoding (correct responses averaged across both encoding tasks, reaction times) and recognition measures (corrected hitrate, reaction times).

Results During encoding, all subjects showed more correct responses in trials with neutral and negative pictures than in trials with positive pictures (correct responses: VALENCE: F(2,102) = 4.71, p \ 0.05). Reaction times were faster in response to neutral than to positive and negative pictures. Negative pictures were associated with the slowest reaction times in all subjects (reaction time: VALENCE: F(2,102) = 19.64, p \ 0.001). During recognition, there were no overall differences between the groups with regard to general memory performance. The interaction between GROUP and VALENCE, however, showed that valence differentially affected memory performance in controls and the patient groups (VALENCE 9 GROUP: F(4,104) = 4.88, p \ 0.01; see Fig. 1). Healthy control subjects tended to remember neutral pictures better than ADHD only (t(37) = -1.72, p \ 0.10) and ADHD patients ? ODD/CD (t(39) = -1.94,

Fig. 1 Recognition memory performance (corrected hitrate (%), mean standard deviation) for ADHD only, ADHD ? ODD/CD and healthy control subjects (? p \ 0.1, * p \ 0.05)

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p \ 0.10). ADHD only patients did not differ from healthy subjects in recognition performance for positive pictures (t(37) = 0.62, p [ 0.5), while ADHD patients ? ODD/CD remembered fewer positive pictures than healthy control subjects (t(39) = 2.52, p \ 0.05). Recognition performance for negative pictures, however, did not differ between the groups. A separate comparison of ADHD patients with ODD vs. with CD showed that recognition performance in both comorbid ODD as well as CD followed the same pattern (VALENCE 9 ODD/CD: F(1,14) \ 1, p [ 0.9). Emotional pictures were recognized better than neutral pictures, with negative pictures leading to better recognition rates than positive pictures (VALENCE: F(2,104) = 92.46, p \ 0.001). This was mainly due to the memory performance in both patient groups (corrected hitrate for negative versus positive pictures: ADHD only: t(13) = 3.01, p \ 0.01; ADHD ? ODD/CD: t(15) = 5.23, p \ 0.001), since healthy control subjects showed comparable recognition performance for positive and negative pictures. All subjects responded faster to positive than to neutral and negative pictures during the recognition test (VALENCE: F(2,104) = 3.62, p \ 0.05).

Discussion ADHD patients with and without ODD/CD tended to show lower recognition memory for neutral pictures than healthy control subjects. This is in line with various ndings that ADHD patients perform below ability when stimuli or task conditions are not engaging or salient enough (Konrad et al. 2000). Patients with ADHD only consequently proted from both types of emotional salience. ADHD patients with comorbid ODD/CD, however, only reached normal recognition rates for negative pictures but lacked a comparably strong effect for positive pictures. This is interesting, since positive pictures have been similarly rated in healthy control subjects and ADHD subjects with and without comorbid ODD/CD (Herpertz et al. 2005). Some studies even found higher arousal ratings for positive pictures in children scoring high in oppositional deant behaviour (Sharp et al. 2006). Evidence for a lower afnity to positive emotional stimuli was only found in one study for a subgroup of high-aggressive children with ODD/CD compared to low-aggressive children with ODD/CD and healthy control subjects (van Goozen et al. 2002). Recent studies have suggested that ADHD with ODD/ CD related conduct problems constitutes a distinct subtype with high heritability and more severe symptoms of inattention, hyperactivity and impulsivity (Banaschewski et al. 2003; Christiansen et al. 2008). The concurrence of high ADHD and ODD symptoms has been shown to aggravate negative interactive behaviour in families with ADHD

children (Edwards et al. 2001). In regard to peers, longitudinal studies have stressed that peer rejection leads to changes in processing patterns in aggressive children which in turn predict exacerbation of antisocial behaviour (Dodge et al. 2003). Concomitant psychosocial risks such as harsh parenting, maternal depression or social distress (Shaw et al. 2001, 2005) can furthermore intensify the adverse feedback mechanism between difcult individual and environmental factors. The lack of positive interaction in different environments could foster a hypervigilance in ADHD youth with ODD/CD to negative information and a loss of sensitivity to positive cues which in turn affects their ability to experience enjoyment (Kuhne et al. 1997). However, stimulant treatment as well as behavior modication have been found to increase positive mood and reduce oppositional behavior across different settings in ADHD patients with comorbid ODD and/or CD (Kolko et al. 1999), augmenting the probability to be accepted and liked by their peers (Whalen et al. 1989). Furthermore, authorative parenting beliefs, comprising rm structuring in the presence of warmth and responsiveness, are closely associated with social acceptance in ADHD children (Hinshaw et al. 1997). It is important to note that also in patients with ADHD only negative contents were remembered better than positive information. This is in line with a recent study (dAcremont and Van der Linden 2007) in a non-clinical sample that showed an association between a memory bias for faces previously presented with an angry expression and increased reports of conduct problems as well as of inattention and hyperactivity. However, proting from positive emotionality could present a protective factor in the ADHD only patient group, preventing the development of more severe psychopathology (Casey 1996).
Acknowledgements The authors thank Iris Mann, Susanne Hoppe, Katharina Sa, Tina Schmidt, and Stefanie Waskewitz for their assistance during data collection and evaluation, and Christian Bethke-Jaenicke for his support in recruiting participants. The study was nancially supported by the German Research Foundation (SFB 426, D5).

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