Cited by 452Attention Deficit Hyperactivity DisorderNeural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on Behavior

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Revisiting the role of the prefrontal cortex in the pathophysiology of attention-deficit/hyperactivity disorder.

Halperin, Jeffrey M., Schulz, Kurt P.·2006·Psychological Bulletin

DOI 10.1037/0033-2909.132.4.560

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Abstract

Most neural models for the pathophysiology of attention-deficit/hyperactivity disorder (ADHD) have centered on the prefrontal cortex and its interconnections with the striatum and other subcortical structures. However, research only partially supports these models, and they do not correspond with the development of the prefrontal cortex and its interrelated neurocircuitry. The neural and functional development of the prefrontal cortex more closely parallels recovery from ADHD as indicated by the developmental remission of symptomatology. The authors hypothesize that ADHD is due to noncortical dysfunction that manifests early in ontogeny, remains static throughout the lifetime, and is not associated with the remission of symptomatology. Data supporting this neurodevelopmental model of prefrontal cortex function in ADHD are reviewed. Research and treatment implications are discussed.

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“The trajectory of functional development, however, is nonlinear, and progresses in a region-specific manner that coincides with maturation of different brain systems (Halperin and Schulz 2006).”
Background
OUP accepted manuscript
Berger, I., Slobodin, O., & Cassuto, H. (2016) · Archives of Clinical Neuropsychology · doi:10.1093/arclin/acw101 · Cited by 131
“The first is a subcortical dysfunction that persists across development and the second is a frontal dysfunction that improves with time (Halperin & Schulz, 2006).”
Changing ASD-ADHD symptom co-occurrence across the lifespan with adolescence as crucial time window: Illustrating the need to go beyond childhood
Hartman, C. A., Geurts, H. M., Franke, B., Buitelaar, J. K., & Rommelse, N. N. J. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.09.003 · Cited by 111
Speed, Variability, and Timing of Motor Output in ADHD: Which Measures are Useful for Endophenotypic Research?
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“…by the cerebellum, basal ganglia and their reciprocal connections with the cerebral cortex (Handy et al. 2003; Harrington et al. 1998; Ivry 1996; Nenadic et al. 2003), subcortical regions in addition to cortical regions might be important in the etiology of ADHD (Halperin and Schulz 2006).”
Background
Heterogeneity in development of aspects of working memory predicts longitudinal attention deficit hyperactivity disorder symptom change.
Karalunas, S. L., Gustafsson, H. C., Dieckmann, N. F., Tipsord, J., Mitchell, S. H., & Nigg, J. T. (2017) · Journal of Abnormal Psychology · doi:10.1037/abn0000292 · Cited by 104
“…functioning) during middle childhood and adolescence contributes to ADHD symptom improvements observed during this same time period for some children (Doehnert, Brandeis, Imhof, Drechsler, & Steinhausen, 2010; El-Sayed, Larsson, Persson, Santosh, & Rydelius, 2003; Halperin & Schulz, 2006).”
Decomposing attention-deficit/hyperactivity disorder (ADHD)-related effects in response speed and variability.
Karalunas, S. L., Huang-Pollock, C. L., & Nigg, J. T. (2012) · Neuropsychology · doi:10.1037/a0029936 · Cited by 104
“Indeed, each of these component processes have been variously hypothesized to be involved in ADHD (Banaschewski et al., 2008; Halperin & Schulz, 2006; Hurks et al., 2005; Klimkeit, Mattingley, Sheppard, Lee, & Bradshaw, 2005; Lajoie et al., 2005; Sergeant, 2000; Sergeant & Scholten, 1985; Steger et…”
The Separation of ADHD Inattention and Hyperactivity-Impulsivity Symptoms: Pathways from Genetic Effects to Cognitive Impairments and Symptoms
Kuntsi, J., Pinto, R., Price, T. S., van der Meere, J. J., Frazier-Wood, A. C., & Asherson, P. (2014) · Journal of Abnormal Child Psychology · doi:10.1007/s10802-013-9771-7 · Cited by 106
“The two cognitive impairments in ADHD may also interplay throughout development, leading to different outcomes for ADHD as individuals pass from childhood into adulthood (Halperin and Schulz 2006; Halperin et al. 2008).”
BackgroundMethod
The executive control network and symptomatic improvement in attention-deficit/hyperactivity disorder
Francx, W., Oldehinkel, M., Oosterlaan, J., Heslenfeld, D., Hartman, C. A., Hoekstra, P. J., Franke, B., Beckmann, C. F., Buitelaar, J. K., & Mennes, M. (2015) · Cortex · doi:10.1016/j.cortex.2015.08.012 · Cited by 102
“…c t Background: One neurodevelopmental theory hypothesizes remission of attention-deficit/ hyperactivity disorder (ADHD) to result from improved prefrontal top-down control, while ADHD, independent of the current diagnosis, is characterized by stable non-cortical deficits (Halperin & Schulz, 2006).”
Background
How Do Trait Dimensions Map onto ADHD Symptom Domains?
Martel, M. M., Nigg, J. T., & von Eye, A. (2009) · Journal of Abnormal Child Psychology · doi:10.1007/s10802-008-9255-3 · Cited by 105
“As a result, top-down circuitry might have an increasingly important influence on descending neural circuitry during late adolescence (Halperin and Schultz 2006), allowing individuals to more efficiently control affect and affectively-driven behavior such as hyperactivity (Sowell et al.”
Influential
Training Executive, Attention, and Motor Skills: A Proof-of-Concept Study in Preschool Children With ADHD
Halperin, J. M., Marks, D. J., Bedard, A.-C. V., Chacko, A., Curchack, J. T., Yoon, C. A., & Healey, D. M. (2013) · Journal of Attention Disorders · doi:10.1177/1087054711435681 · Cited by 106
“As such, it has been hypothesized that enhancement of experience-dependent neurodevelopment can be used to facilitate recovery or a diminution of symptoms over the life span (Halperin & Healey, 2011; Halperin & Schulz, 2006).”
BackgroundSelf-citation
Are Motor Inhibition and Cognitive Flexibility Dead Ends in ADHD?
Rommelse, N. N. J., Altink, M. E., de Sonneville, L. M. J., Buschgens, C. J. M., Buitelaar, J., Oosterlaan, J., & Sergeant, J. A. (2007) · Journal of Abnormal Child Psychology · doi:10.1007/s10802-007-9146-z · Cited by 103
“It might be that the (pre)frontal lobes are not causally involved in the disorder, but contribute to the age related recovery of symptoms frequently observed in ADHD patients (Halperin and Schulz 2006).”
Background
ADHD performance reflects inefficient but not impulsive information processing: A diffusion model analysis.
Metin, B., Roeyers, H., Wiersema, J. R., van der Meere, J. J., Thompson, M. J. J., & Sonuga-Barke, E. J. S. (2013) · Neuropsychology · doi:10.1037/a0031533 · Cited by 107
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“(Biederman et al., 2000; Faraone et al., 2006; Halperin and Schulz, 2006).”
BackgroundResultInfluential
Implementation Intentions Facilitate Response Inhibition in Children with ADHD
Gawrilow, C., & Gollwitzer, P. M. (2008) · Cognitive Therapy and Research · doi:10.1007/s10608-007-9150-1 · Cited by 103
“…a somewhat incoherent picture, with some studies failing to find differences on several measures of executive functioning and other studies only allowing vague inferences regarding the exact nature of the executive dysfunction observed (Halperin & Schulz, 2006; Wu, Anderson, & Castiello, 2006).”
Cognitive enhancers for the treatment of ADHD
Bidwell, L. C., McClernon, F. J., & Kollins, S. H. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.05.002 · Cited by 104
“Weaknesses in these prefrontal regions are thought to interact with dysfunction in subcortical regions, including striatal regions and the cerebellum, in order produce requisite EF deficits in ADHD patients (Halperin and Schulz, 2006).”
Background
An Open Trial of a Metacognitive Executive Function Training for Young Children With ADHD
Tamm, L., Nakonezny, P. A., & Hughes, C. W. (2014) · Journal of Attention Disorders · doi:10.1177/1087054712445782 · Cited by 98
Emerging Support for a Role of Exercise in Attention-Deficit/Hyperactivity Disorder Intervention Planning
Berwid, O. G., & Halperin, J. M. (2012) · Current Psychiatry Reports · doi:10.1007/s11920-012-0297-4 · Cited by 113
“deficits through ‘top down’ regulatory control [14].”
Self-citation
Inefficient cognitive control in adult ADHD: evidence from trial-by-trial Stroop test and cued task switching performance
King, J. A., Colla, M., Braß, M., Heuser, I., & von Cramon, D. (2007) · Behavioral and Brain Functions · doi:10.1186/1744-9081-3-42 · Cited by 109
Integrating Impairments in Reaction Time and Executive Function Using a Diffusion Model Framework
Karalunas, S. L., & Huang‐Pollock, C. L. (2013) · Research on Child and Adolescent Psychopathology · doi:10.1007/s10802-013-9715-2 · Cited by 107
“All have been hypothesized to be involved in ADHD (Banaschewski et al. 2008; Halperin and Schulz 2006; Hurks et al. 2005; Klimkeit et al. 2005; Lajoie et al. 2005; Sergeant 2000; Sergeant and Scholten 1985; Steger et al. 2001).”
Systematic Review and Meta-analysis: The Science of Early-Life Precursors and Interventions for Attention-Deficit/Hyperactivity Disorder
Shephard, E., Zuccolo, P. F., Idrees, I., Godoy, P. B. G., Salomone, E., Ferrante, C., Sorgato, P., Catão, L. F. C. C., Goodwin, A., Bolton, P., et al. (2021) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2021.03.016 · Cited by 96
Hyperactivity and sensation seeking as autoregulatory attempts to stabilize brain arousal in ADHD and mania?
Geissler, J. M., Romanos, M., Hegerl, U., & Hensch, T. (2014) · ADHD Attention Deficit and Hyperactivity Disorders · doi:10.1007/s12402-014-0144-z · Cited by 110
“Other authors suspected structural alterations in regions involved in modulating arousal (e.g. formatio reticularis; Halperin and Schulz 2006) to be disruptive to vigilance regulation in ADHD.”
Background
Executive function predicts school readiness in autistic and typical preschool children
Pellicano, E., Kenny, L., Brede, J., Klaric, E., Lichwa, H., & McMillin, R. (2017) · Cognitive Development · doi:10.1016/j.cogdev.2017.02.003 · Cited by 106
Cerebellar involvement in autism and ADHD
Bruchhage, M. M. K., Bucci, M. P., & Becker, E. B. E. (2018) · Handbook of clinical neurology · doi:10.1016/b978-0-444-64189-2.00004-4 · Cited by 99
An Evolutionary Perspective on Learning Disability in Mathematics
Geary, D. C. (2007) · Developmental Neuropsychology · doi:10.1080/87565640701360924 · Cited by 106
“There is considerable heterogeneity within these diagnostic categories which may, in part, be due to variation in the underlying brain systems that contribute to the behavioral and cognitive features of these disorders (e.g., Halperin & Schulz, 2006).”
Background
Improving Outcomes for Youth with ADHD: A Conceptual Framework for Combined Neurocognitive and Skill-Based Treatment Approaches
Chacko, A., Kofler, M., & Jarrett, M. (2014) · Clinical Child and Family Psychology Review · doi:10.1007/s10567-014-0171-5 · Cited by 93
“Finally, some models hypothesize that executive functioning impairments are unrelated to core ADHD behavioral symptoms (Halperin and Schulz 2006), but rather serve ontogenetic compensatory mechanisms (Rajendran et al. 2013).”
Is hyperactivity ubiquitous in ADHD or dependent on environmental demands? Evidence from meta-analysis
Kofler, M. J., Raiker, J. S., Sarver, D. E., Wells, E. L., & Soto, E. F. (2016) · Clinical Psychology Review · doi:10.1016/j.cpr.2016.04.004 · Cited by 88
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Altered circadian profiles in attention-deficit/hyperactivity disorder: An integrative review and theoretical framework for future studies
Imeraj, L., Sonuga-Barke, E. J. S., Antrop, I., Roeyers, H., Wiersema, R., Bal, S., & Deboutte, D. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.04.007 · Cited by 90
“It has been hypothesized that such an autonomic imbalance -low parasympathetic activity and a relative sympathetic dominance- reflects low heart rate variability, a marker for prefrontal hypoactivity (Thayer and Sternberg, 2006) as seen in ADHD (Arnsten, 1998; Halperin and Schulz, 2006; Himelstein et al., 2000; Valera…”
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The hierarchical factor model of ADHD: invariant across age and national groupings?
Toplak, M. E., Sorge, G. B., Flora, D. B., Chen, W., Banaschewski, T., Buitelaar, J. K., Ebstein, R. P., Eisenberg, J., Franke, B., Gill, M., et al. (2011) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2011.02500.x · Cited by 89
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Authors: Halperin, J. M., & Schulz, K. P.
Affiliations: Queens College, CUNY (US)
Icahn School of Medicine at Mount Sinai (US)
ORCID: Halperin, Jeffrey M.
Schulz, Kurt P.
Venue: Psychological Bulletin
Publisher: American Psychological Association (APA)
Published: 2006
Volume: 132
Issue: 4
Pages: 560-581
ISSN: 0033-2909 (ISSN-L)
1939-1455
DOI: 10.1037/0033-2909.132.4.560
OpenAlex: W2139377807
Semantic Scholar: 9b63dbee33341e428d6c3a9a7c386b7dd42c7191
Cited by: 446
References: 298
Citations by year: 2026: 6 · 2025: 13 · 2024: 21 · 2023: 14 · 2022: 22 · 2021: 21 · 2020: 34 · 2019: 14 · 2018: 18 · 2017: 26 · 2016: 30 · 2015: 25 · 2014: 30 · 2013: 35 · 2012: 25
FWCI: 2.39
Type: journal article
Language: en
Open access: closed
Locations: Psychological Bulletin (publishedVersion)
PubMed (publishedVersion)
Funders: William T. Grant Foundation (97183497)
National Institute of Mental Health (RO1 MH60698; RO1 MH068206; R21 MH066360)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Attention Deficit Hyperactivity Disorder
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: attention deficit hyperactivity disorder, prefrontal cortex, neurodevelopmental model, striatum, symptom remission, ADHD pathophysiology
MeSH terms: Attention Deficit Disorder with Hyperactivity, Humans, Prefrontal Cortex

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Revisiting the role of the prefrontal cortex in the pathophysiology of attention-deficit/hyperactivity disorder.

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