Reduced error signalling in medication-naive children with ADHD: associations with behavioural variability and post-error adaptations

Reduced error signalling in medication-naive children with ADHD: associations with behavioural variability and post-error adaptations

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J Psychiatry Neurosci 2016;41(2):77-87

Kerstin J. Plessen, MD, PhD; Elena A. Allen, PhD; Heike Eichele, MD; Heidi van Wageningen, PhD; Marie Farstad Høvik, MD; Lin Sørensen, PhD; Marius Kalsås Worren, MD; Kenneth Hugdahl, PhD; Tom Eichele, MD, PhD

Abstract

Background: We examined the blood-oxygen level–dependent (BOLD) activation in brain regions that signal errors and their association with intraindividual behavioural variability and adaptation to errors in children with attention-deficit/hyperactivity disorder (ADHD).

Methods: We acquired functional MRI data during a Flanker task in medication-naive children with ADHD and healthy controls aged 8–12 years and analyzed the data using independent component analysis. For components corresponding to performance monitoring networks, we compared activations across groups and conditions and correlated them with reaction times (RT). Additionally, we analyzed post-error adaptations in behaviour and motor component activations.

Results: We included 25 children with ADHD and 29 controls in our analysis. Children with ADHD displayed reduced activation to errors in cingulo-opercular regions and higher RT variability, but no differences of interference control. Larger BOLD amplitude to error trials significantly predicted reduced RT variability across all participants. Neither group showed evidence of post-error response slowing; however, post-error adaptation in motor networks was significantly reduced in children with ADHD. This adaptation was inversely related to activation of the right-lateralized ventral attention network (VAN) on error trials and to task-driven connectivity between the cingulo-opercular system and the VAN.

Limitations: Our study was limited by the modest sample size and imperfect matching across groups.

Conclusion: Our findings show a deficit in cingulo-opercular activation in children with ADHD that could relate to reduced signalling for errors. Moreover, the reduced orienting of the VAN signal may mediate deficient post-error motor adaptions. Pinpointing general performance monitoring problems to specific brain regions and operations in error processing may help to guide the targets of future treatments for ADHD.


Submitted Nov. 27, 2014; Revised Mar. 31, 2015; Accepted May 6, 2015; Early-released Oct. 6, 2015

Affiliations: From the Child and Adolescent Mental Health Centre, Capital Region Psychiatry, Copenhagen, Denmark (Plessen); the Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark (Plessen); the Department of Clinical Medicine, Faculty of Medicine and Odontology, University of Bergen, Bergen, Norway (Plessen, Høvik, Worren); the K.G. Jebsen Center for Research on Neuropsychiatric Disorders, University of Bergen, Bergen, Norway (Plessen, Allen, Sørensen, Hugdahl, Eichele); the Mind Research Network, Albuquerque, New Mexico (Allen, Eichele); the Department of Biological and Medical Psychology, Faculty of Psychology, University of Bergen, Bergen, Norway (Allen, Eichele, Hugdahl, Eichele); the Norwegian School of Economics, Bergen, Norway (van Wageningen); the Division of Psychiatry, Haukeland University Hospital, Bergen, Norway ( Hugdahl); the Department of Radiology, Haukeland University Hospital, Bergen, Norway (Hugdahl); the Section for Clinical Neurophysiology, Haukeland University Hospital, Bergen, Norway (Eichele).

Acknowledgements: We thank Roger Barndon for his technical assistance. This work was supported by grants from the Research Council of Norway (190544/H110), the Western Norway Health Authority (MoodNet and the Network for Anxiety Disorders; 911435, 911607, 911827) and the National Norwegian ADHD network to K. Plessen and from the K.G. Jebsen Foundation to E. Allen, K. Hugdahl and T. Eichele.

Competing interests: K. Hugdahl own shares in NordicNeuroLab Inc., which produces the LCD goggles and audio system used for presenting the stimuli to the participants in this study. No other competing interests declared.

Contributors: K. Plessen, E. Allen, H. Eichele, L. Sørensen, K. Hugdahl and T. Eichele designed the study. K. Plessen, H. Eichele, H. van Wageningen, M. Høvik, L. Sørensen, M. Worren and T. Eichele acquired the data, which K. Plessen, E. Allen, K. Hugdahl and T. Eichele analyzed. K. Plessen, E. Allen and T. Eichele wrote the article, which all authors reviewed and approved for publication.

DOI: 10.1503/jpn.140353

Correspondence to: K.J. Plessen, Child and Adolescent Mental Health Centre, Mental Health Services-Capital Region Psychiatry, Denmark, Lersø Parkallée 107, 2100 København Ø, Denmark; kerstin.plessen@regionh.dk