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/lp/springer-journals/behavioral-sensitivity-of-japanese-children-with-and-without-adhd-to-2NH0l0cQj3
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- Springer Journals
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- Copyright © 2017 by The Author(s)
- Subject
- Biomedicine; Neurosciences; Neurology; Behavioral Therapy; Psychiatry
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- 1744-9081
- DOI
- 10.1186/s12993-017-0131-6
- pmid
- 28946880
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Abstract
Background: Most research on motivational processes in attention deficit hyperactivity disorder (ADHD) has been undertaken in Western Europe and North America. The extent to which these findings apply to other cultural groups is unclear. The current study evaluated the behavioral sensitivity of Japanese children with and without ADHD to changing reward availability. Forty-one school-aged children, 19 diagnosed with DSM-IV ADHD, completed a signal- detection task in which correct discriminations between two stimuli were associated with different reinforcement frequencies. The response alternative associated with the higher rate of reinforcement switched twice during the task without warning. Findings: Both groups of children developed an initial bias toward the more frequently reinforced response alterna- tive. When the reward contingencies switched the response allocation (bias) of the control group children followed suit. The response bias scores of the children with ADHD did not, suggesting impaired tracking of reward availability over time. Conclusions: Japanese children with ADHD adjust their behavioral responses to changing reinforcer availability less than their typically developing peers. This is not explained by poor attention to task or a lack of sensitivity to reward. The current results are consistent with altered sensitivity to changing reward contingencies identified in non-Japa- nese samples of children with ADHD. Irrespective of their country of origin, children with ADHD will likely benefit from behavioral expectations and reinforcement contingencies being made explicit together with high rates of reinforce- ment for appropriate behaviors. Keywords: ADHD, Positive reinforcement, Signal detection, Japan for the disorder in adulthood [2, 3]. Attention deficit Background hyperactivity disorder has been identified across coun - Attention deficit hyperactivity disorder (ADHD) is a tries and cultures [4], with similar prevalence rates and common neurodevelopmental disorder characterized by symptom presentation, including in Japan [5, 6]. elevated levels of inattention, hyperactivity and/or impul- The disorder is known to be highly heritable (see [ 7] for sivity that impair daily functioning. Upwards of 5% of ele- review), however its precise etiology remains uncertain. mentary school-age children are diagnosed with ADHD Altered sensitivity to reward has been hypothesized to [1], 50–65% of whom continue to meet diagnostic criteria contribute to symptoms of ADHD (e.g., [8–13]). Evidence continues to accumulate in support of altered motiva- *Correspondence: furukawa@oist.jp; tripp@oist.jp tional processes in ADHD, although findings across stud - Human Developmental Neurobiology Unit, Okinawa Institute of Science ies are not entirely consistent, highlighting the complex and Technology Graduate University, 1919-1 Tancha, Onna, Okinawa 904-0495, Japan nature of motivational processes [14]. At the behavioral Full list of author information is available at the end of the article © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Furukawa et al. Behav Brain Funct (2017) 13:13 Page 2 of 9 level the most consistent finding is that children with availability, using the signal detection task described by ADHD are more likely to choose small immediate over Alsop et al. [16]. Participating children were required to larger delayed rewards compared with typically develop- identify which of two stimuli were presented by mak- ing children (see [15] for a review). A number of stud- ing the appropriate response on a two-button response ies report the performance enhancing effects of reward, panel. The task began with one type of correct response on a range of cognitive tasks, are larger in children with being rewarded four times as often as the other. Such ADHD than controls (see [16, 17] for reviews). Results unequal arrangement of reward typically produces a from some studies also suggest the performance of chil- response bias (preference) for the more frequently rein- dren with ADHD is more similar to that of controls when forced alternative [29, 30]; that is, the task examines the reinforcement for correct responses is continuous or effects of reward on subsequent behavior, by exploiting near continuous (e.g., [12, 18–22]). instances of uncertainty regarding the correct discrimi- Alsop et al. [16] recently demonstrated that children nation between stimuli. In this study the ratio of avail- with ADHD are less sensitive to changing reward avail- able reinforcers for correct discriminations on the two ability than typically developing children, when rates response alternatives switched twice during the task. of reinforcement are low and changes are not signaled. Based on the findings of Alsop et al. [16], and the avail - Their findings are consistent with earlier reports that able evidence of altered reward sensitivity in children the behavior of children with ADHD does not match the with ADHD in non-Western cultures [25–27], we pre- reinforcement contingencies operating as well as that of dict the response allocation of Japanese children with controls [23, 24]. These findings may help explain the dif - ADHD will match reward contingencies less closely than ficulty children with ADHD have in adapting their behav - that of their typically developing peers. Such an outcome ior to shifting situational demands in everyday life, where would be of particular clinical relevance in Japan, where expectations for their behavior often change without conformity is highly valued and the ability to adapt ones warning (e.g., playing outside vs. sitting in a restaurant) behavior to situational demands is especially important, and appropriate behavior is not continuously reinforced. but where behavioral expectations are seldom made To date, the majority of studies assessing motivational explicit [31]. processes in children with ADHD have been undertaken The overall sensitivity of the two groups of Japanese in Western countries. Only a small number of studies children to the asymmetric reward distribution is more have evaluated reward sensitivity in children with ADHD difficult to predict. Praise is used sparingly in Japan [32– from other cultural groups (e.g., South Africa [25], Japan 34] and how this experience will impact the children’s [26], China [27]). Aase et al. [25] described reinforcers sensitivity to reward availability in the current task is as being less efficient in establishing stimulus control unclear. Any differences in the reinforcement sensitiv - in children with ADHD compared with controls in the ity of typically developing Japanese children, compared Limpopo district of South Africa. Masunami et al. [26] to their Western peers, would need to be considered in reported Japanese children with ADHD paid more atten- interpreting the data from the children with ADHD. tion to reward than their typically developing peers while completing a variant of the Iowa Gambling Task. Most Methods recently, Yu et al. [27] demonstrated Chinese children Participants with ADHD show a stronger preference than controls for Data from 41 children, 19 meeting DSM-IV diagnostic smaller immediate rewards over larger delayed rewards criteria for ADHD (all boys) and 22 typically develop- in temporal discounting and choice delay paradigms. ing children (50.0% boys) living in Okinawa, Japan, are The results of these studies suggest the association included in the study. Within the ADHD group, 10 chil- between ADHD and altered reward processing is not dren were diagnosed with inattentive type, one with a Western cultural phenomenon. However, further hyperactive/impulsive type and eight with combined research is needed to confirm the presence of altered type ADHD. Four children were prescribed stimulant motivational processing in children with ADHD across medication, which was discontinued for at least 24 h cultures, preferably using the same paradigms so that prior to study participation. Table 1 presents the sample findings can be directly compared. This becomes increas - characteristics. ingly important as Western-styled behavior management Inclusion criteria for the study were estimated IQ programs are progressively adopted in non-Western scores above 70, participation in regular education countries [28]. classes , normal or corrected vision, no past or current In the current study we evaluate the sensitivity of Japanese children with and without ADHD to unequal Special education classrooms or day services in Japan tend to serve chil- frequency of reward and to changing reinforcement dren with significant functional impairments. Furukawa et al. Behav Brain Funct (2017) 13:13 Page 3 of 9 Table 1 Participant characteristics Control ADHD (n = 22) (n = 19) Mean sd Range Mean sd Range Age (months) 122.73 20.48 86–149 107.74 14.78 89–137 Estimated IQ 98.00 12.29 84–121 104.47 14.91 77–126 Boys, n (%) 11 (50%) 19 (100%) Stimulant medication (concerta), n – 4 Subtype, n: inattentive/hyperactivity_impulsivity/combined – 10/1/8 Comorbidity, n: oppositional defiant disorder 3 Language/Tic/asperger disorder 1/1/2 The mean age was significantly higher for the control than ADHD group (t(39) = 2.65, p < .05) Given that DSM-5 allows comorbid diagnosis of ASD with ADHD, children demonstrating symptoms of DSM-IV asperger disorder were included in the study if they satisfied other inclusion criteria. However, those demonstrating symptoms consistent with autistic disorder were excluded from the study due to accompanying cognitive impairments head injury, neurological disorder or psychosis. Comor- Parent and teacher reports were reviewed for other inclu- bid conditions were allowed if these inclusion criteria sion criteria. were met. Children in the ADHD group were recruited through a university research clinic, where they com- Experimental task pleted multi-method, multi-informant research diagnos- The experimental task and procedure used is described tic assessments. Data from semi-structured diagnostic in detail in Alsop et al. [16] and illustrated in Fig. 1. After interviews (K-SADS-PL, disruptive behavior disorder instructions and a short demonstration of the task, chil- section) [35, 36], parent and teacher completed rating dren indicated whether there were “more red” or “more scales for ADHD symptoms (SNAP) [37, 38], and obser- blue” characters in a checkerboard pictured on a com- vations of the child’s behavior were used to make a clini- puter screen (10 × 10 arrays containing either more red cal diagnosis of ADHD. Parent and teacher completed or more blue faces in a ratio of 54:46), using a two-button broadband rating scales (CBCL/TRF) [39–42] and back- response panel. They were advised that correct responses ground questionnaires screened for other behavioral and only sometimes earn rewards. A multi-element reinforce- emotional problems, neurological and medical condi- ment system was used to maximize reward effective - tions. Cognitive functioning was assessed with the ness: the message “Well done!” and an animated cartoon WISC-III or WISC-IV [43–46]. appearing on screen, verbal praise from the examiner, Children were required to display six or more symp- and colored tokens placed in a clear plastic container toms of inattention and/or hyperactivity/impulsivity in next to the child. Following incorrect and non-rewarded at least one setting, evidence of symptoms in a second correct responses, the screen was blank and the experi- setting, and functional impairment. Symptoms were menter remained silent. All children received a prize at not summed across informants. Assessments were car- the end of the session irrespective of their performance ried out by a team including a US-licensed, Japanese- on the task. speaking clinical psychologist (EF), and clinicians with Successive blocks of eight trials contained an equal advanced counseling or other relevant degrees, all flu - number of each array type, randomized within blocks. ent in Japanese and experienced in working with chil- The computer determined quasi-randomly which correct dren with ADHD. Control group children were recruited responses were reinforced. At the start of the session, through invitation letters sent home to parents through correct identifications of one stimulus (“more blue”) were public schools. These children completed an abbreviated rewarded four times more often than correct identifica - IQ assessment (WISC-III Vocabulary/Block Design). tions of the other stimulus (“more red”). After the child Their parents and teachers completed the behavior rat - had received 20 rewards with this distribution, the com- ing scales, which were used to rule out the presence of puter reversed the contingencies and correct identifica - ADHD or other significant behavioral or emotional dis - tions of “more red” stimuli were reinforced four times as orders. Those demonstrating fewer than four symptoms often. After another 20 rewards, the original reward dis- of inattention or hyperactivity/impulsivity were included. tribution was reinstated, with the game ending after the Furukawa et al. Behav Brain Funct (2017) 13:13 Page 4 of 9 Fig. 1 Experimental task timeline children received a further 20 rewards. Each successive receive reinforcements 1–10 and 11–20 (reward distri- block of ten reinforcements contained eight reinforce- bution 4:1), reinforcements 21–30 and 31–40 (reward ments for correct identification of one array type and two distribution 1:4), and reinforcements 41–50 and 51–60 for correct identification of the other, randomized within (reward distribution 4:1). each block. Mean scores for response bias, discriminability and median response time for the six blocks (2 blocks each for Data collection and analysis the initial, reversal and reinstatement phases) were ana- Three measures of performance were calculated for each lyzed with SPSS GLM. Mixed ANOVA was conducted to child: median response time, discriminability between examine the main effects of Block (i.e., changes in bias, stimuli (logd) i.e., accuracy, and response bias (logb) i.e., discriminability or response time over the 6 blocks) and the systematic preference for the more frequently rein- Group (i.e., the difference in bias, discriminability or forced alternative [29]. response time between the ADHD and control group), Discriminability between the stimuli was calculated by and the interaction effects. The bias scores were expected the equation: to change with the two shifts in the contingency sched- ule, therefore polynomial contrasts examined quadratic 1 Blue Red Correct Correct log d = log · and linear trends in the bias scores over the six blocks, 2 Blue Red Incorrect Incorrect separately for the ADHD and control groups. Post-hoc and response bias by: pairwise comparisons were performed when significant univariate effects were observed. There were differences 1 Blue Red Correct Incorrect log b = log · in the mean age and IQ, and gender, between the ADHD 2 Blue Red Incorrect Correct and control groups. Although the difference in IQ scores where Blue denotes the number of correct did not reach statistical significance, given the small sam - Correct responses following presentations of the “more blue” ple size, IQ was entered as a covariate along with age and array, Red denotes the number of incorrect gender, when the two groups were compared on the per- Incorrect responses following presentation of the “more red” array, formance measures. and so forth. Response bias scores were calculated rela- tive to the response alternative that was reinforced more Results frequently during the initial phase. Mean response dis- Response bias criminability and response bias and median response Mixed ANOVA indicated a significant univariate time scores were calculated for all trials completed to Block × Group interaction effect (F(5, 180) = 2.64, Furukawa et al. Behav Brain Funct (2017) 13:13 Page 5 of 9 p < .05) for bias, controlling for age, IQ and gender through sixth blocks of the task (p < .05, Bonferroni (Fig. 2). For both groups, their bias scores were sig- correction). nificantly different from zero during the first block (p < .001). The bias scores of the two groups were sig - Response time nificantly different from one another during blocks two Mixed ANOVA indicated a trend toward a main effect of and six (p < .05, Bonferroni correction). Two polynomial Group (F(1, 36) = 3.50, p < .10), after controlling for age, contrasts were performed to assess quadratic and linear IQ and gender (Fig. 4). Pairwise comparisons show that trends in the bias scores over the six blocks, separately children in the ADHD group responded more quickly for the control and ADHD groups. For the control group, than those in the control group during the first block of there were significant quadratic (F(1, 21) = 9.50, p < .01) the initial phase (p < .05, Bonferroni correction). and linear (F(1, 21) = 12.02, p < .01) effects. Pairwise comparisons indicated a significant difference in the bias Discussion scores for the second and forth blocks (the second half The current study assessed the behavioral sensitivity of of the initial and reversal phases; p < .01, Bonferroni cor- Japanese children with ADHD and their typically devel- rection). Mean bias scores decreased across both blocks oping peers to unequal frequency of reward and chang- of the reversal phase, increasing during the first block of ing reinforcement contingencies using signal-detection the reinstatement phase. For the ADHD group, only the methodology. Both groups of children initially developed linear trend was significant (F(1, 18) = 31.68, p < .001). a preference (response bias) for the more frequently rein- For this group the bias score for the first block was sig - forced alternative, demonstrating their behavioral sensi- nificantly larger than the bias scores for the two reinstate - tivity to the asymmetric reward distribution. ment blocks (p < .05). As the task progressed the response allocation of the typically developing children reflected the availability Discriminability of reward, i.e., as the reward contingencies changed the Mixed ANOVA indicated a significant main effect of children’s response bias scores changed with them. The Group (F(1, 36) = 10.81, p < .01) after controlling for overall response pattern that emerged was very similar to age, IQ and gender (Fig. 3). Discriminability scores were that reported by Alsop et al. [16] for their New Zealand significantly higher for the control group for the second control subjects. Cross-culturally, typically developing Fig. 2 Mean response bias scores and standard errors for the ADHD and control groups during the initial, reversal and reinstatement phases Furukawa et al. Behav Brain Funct (2017) 13:13 Page 6 of 9 Fig. 3 Mean discriminability scores and standard errors for the ADHD and control groups during the initial, reversal and reinstatement phases Fig. 4 Median response time and standard errors for the ADHD and control groups during the initial, reversal and reinstatement phases Furukawa et al. Behav Brain Funct (2017) 13:13 Page 7 of 9 children respond similarly to changing reinforcer avail- with ADHD have difficulty adapting their behavior to ability, altering their response allocation to match the situational demands when levels of reinforcement are prevailing reinforcement contingencies. In both studies, relatively low and contingency changes are not signaled. the lower response bias scores seen in the reinstatement We previously suggested such a disparity might arise phase of the task likely reflect the children’s accumulated as children with ADHD have difficulty adjusting their experience of reward over the initial and reversal phases internal representations of reinforcement contingencies of the task (i.e., their “reinforcement history” on the task). under low rates of partial reinforcement [8, 48]. Addi- The similarity of the control group findings from New tional studies are needed to confirm the robustness of Zealand and Japan suggests the signal detection task is the observed effect together with theoretical and empiri - relevant to children from different cultural groups. cal research to address its underlying neurobiology. The - The response bias pattern of the Japanese children with ory-driven computational models could be developed to ADHD suggests their ability to track changing reward address questions regarding how prior experience with availability is impaired. After developing a significant reward interacts with the prevailing contingencies to response bias toward the more frequently reinforced influence subsequent actions in those with and without alternative during the first half of the initial phase, the ADHD. Alongside such theoretical work, neuroimaging children’s bias score dropped to near zero. This was fol - and animal studies might examine frontostriatal activity lowed by a slight increase in bias during the first half patterns in response to changing contingencies during a of the reversal phase, then a slow decrease across the conditional-discrimination task such as the signal-detec- remainder of the task. These data suggest a loss of behav - tion paradigm. ioral control by the asymmetric reward distribution. The overall similarity of the results to those reported Although the exact response pattern differed, Alsop et al. by Alsop et al. [16], lends weight to the current find - [16] also reported impaired tracking of reinforcement ings. The study does, however, have limitations, includ - contingencies in New Zealand and American children ing small sample sizes. The final ADHD sample is smaller with ADHD. In the current study, it is not clear why the than expected given the number of families who initially children stopped responding to the asymmetric reward volunteered to participate. Compared with many coun- distribution so early in the task. However, the failure of tries, ADHD has a shorter history of recognition in Japan the children to match their response allocation to the [5, 49]. This coupled with the stigma attached to men - reinforcement contingencies operating is consistent with tal health concerns may have increased the severity and the difficulty children with ADHD have adapting their complexity of the problems seen in children whose fami- behavior when setting demands change (e.g., “often runs lies volunteered for the study. Families of children expe- about or climbs in situations where it is inappropriate” riencing pronounced difficulties may have been more [47]). willing to participate in research offering comprehensive Poorer behavioral tracking of the reinforcement con- multi-method, multi-informant assessments. The result tingencies by the ADHD group does not reflect a lack being the exclusion of a number of children who did not of sensitivity to reinforcement. As noted, both groups meet the study criteria. of children developed a clear bias toward the more fre- Groups in the current study were not well matched for quently reinforced response alternative early in the task. age, IQ or gender, in part reflecting the challenges of data Nor does it reflect difficulty completing the signal detec - collection. As potential confounds, all three variables tion task. Although discriminability scores were sig- were included as covariates in the analyses, resulting in nificantly lower for the children with ADHD, possibly more conservative probability estimates, but no change reflecting less attention to the stimuli, their mean accu - in the findings. Importantly, within the control group racy exceeded 70% across all phases of the task. The chil - there were no significant gender differences for age, IQ, dren with ADHD initially responded more quickly on the response bias or discriminability. The assessment and task than controls, the latter’s response times decreasing diagnostic practices followed international guidelines to a similar level with time on task. While the response and care was taken to rule out any psychiatric or neu- speed of the ADHD group may have impacted their dis- rodevelopmental disorders amongst the control group. criminability, it does not show a consistent relationship We are therefore confident of group membership in our with bias scores, arguing against impulsive responding sample. In addition, the rate and pattern of comorbidity leading to poorer tracking of reward availability. in the ADHD sample argues against other disorders While the mechanisms underlying the poor align- explaining the current findings. ment between reward availability and response alloca- tion in children with ADHD remains to be determined, The mean response time was faster for females throughout the task (F (1, the current study provides further evidence that children 20) = 4.69, p < .05). Furukawa et al. Behav Brain Funct (2017) 13:13 Page 8 of 9 The signal detection task used in the current study has will help refine behavioral and pharmacological treat - good ecological validity. Just as in children’s every day ments and ensure their appropriateness for different cul - experiences, not all instances of correct behavior (i.e., tural groups. successful discriminations) were rewarded and changes Authors’ contributions in reward availability were unsignaled [16]. These condi - GT and BA designed the original paradigm, EF and SS supervised data collec- tions may be especially relevant to the study of ADHD tion, GT, BA and EF analyzed and interpreted the data. All authors contrib- uted to the writing of manuscript. All authors read and approved the final in Japan, where the use of praise is less normative [32– manuscript. 34]. As a more homogeneous population, societal roles are strongly tied to an individual’s identity and behavior Author details Human Developmental Neurobiology Unit, Okinawa Institute of Science [50], with children and adults expected to know the rules and Technology Graduate University, 1919-1 Tancha, Onna, Okinawa 904-0495, without them always being explicitly stated. Behavioral 2 Japan. Department of Psychology, University of Otago, Dunedin, New sensitivity to situational demands would be important in Zealand. maintaining group harmony. Acknowledgements The present findings suggest similarities between Japa - The authors thank all the children, families, and teachers who took part, as well nese and Western children with ADHD that go beyond as members of the OIST Children’s Research Center in Japan who assisted with assessment and data collection. symptom presentation. The results are consistent with reduced sensitivity to unsignaled contingency changes Competing interests identified in non-Japanese samples of children with The authors declare that they have no competing interests. ADHD. Parents and teachers of Japanese children with Availability of data and materials ADHD should be advised of the importance of reducing The datasets used and/or analyzed during the current study are available from ambiguity regarding behavioral expectations, irrespec- the corresponding author on reasonable request. tive of normative practices. Although Japanese culture has Consent for publication many daily rituals marking the transition from one set- Not applicable. ting to another (e.g., all students stand up and bow as the Ethics approval and consent to participate teacher enters the classroom), children with ADHD would Ethical approval for the study was obtained from the Human Subjects benefit from explicit information regarding behavioral Research Review Committee at the Okinawa Institute of Science and Technol- expectations in different settings and when these change. ogy (OIST ) Graduate University in Japan. Participating parents, teachers, and children were volunteers and provided written consent. Furthermore, it should not be assumed that children with ADHD will carry this information forward to new envi- Funding ronments, or that a failure to adapt behavior to situational The study was supported by the internal subsidy funding from the OIST Graduate University. demands is evidence of misbehavior. For children with ADHD, frequent, immediate and consistent reward for Publisher’s Note appropriate behavior is recommended across cultures. Springer Nature remains neutral with regard to jurisdictional claims in pub- lished maps and institutional affiliations. Conclusion Received: 10 June 2017 Accepted: 18 September 2017 The current results provide additional evidence that chil - dren with ADHD do not track reward contingencies as consistently as typically developing children, when rates of reinforcement are low and the contingencies change without warning. The similarity of the findings, across References 1. Polanczyk GV, Willcutt EG, Salum GA, Kieling C, Rohde LA. ADHD preva- studies and cultures, using the same paradigm and diag- lence estimates across three decades: an updated systematic review and nostic procedures, offers further evidence for altered meta-regression analysis. Int J Epidemiol. 2014;43:434–42. reward sensitivity playing a role in the pathophysiology 2. 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Journal
Behavioral and Brain Functions – Springer Journals
Published: Sep 25, 2017