Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-23T04:56:04.610Z Has data issue: false hasContentIssue false

Comprehensive Examination of Frontal Regions in Boys and Girls with Attention-Deficit/Hyperactivity Disorder

Published online by Cambridge University Press:  19 September 2011

E. Mark Mahone*
Affiliation:
Department of Neuropsychology, Kennedy Krieger Institute, Baltimore, Maryland Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland
Marin E. Ranta
Affiliation:
Laboratory for Neurocognitive and Imaging Research, Kennedy Krieger Institute, Baltimore, Maryland
Deana Crocetti
Affiliation:
Laboratory for Neurocognitive and Imaging Research, Kennedy Krieger Institute, Baltimore, Maryland
Jessica O'Brien
Affiliation:
Laboratory for Neurocognitive and Imaging Research, Kennedy Krieger Institute, Baltimore, Maryland
Walter E. Kaufmann
Affiliation:
Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland Center for Genetic Disorders of Cognition and Behavior, Kennedy Krieger Institute, Baltimore, Maryland Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, Maryland Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, Maryland Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland Russell H. Morgan Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, Baltimore, Maryland
Martha B. Denckla
Affiliation:
Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, Maryland Department of Pediatrics, Johns Hopkins University School of Medicine, Baltimore, Maryland Developmental Cognitive Neurology, Kennedy Krieger Institute, Baltimore, Maryland
Stewart H. Mostofsky
Affiliation:
Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, Maryland Laboratory for Neurocognitive and Imaging Research, Kennedy Krieger Institute, Baltimore, Maryland Department of Neurology, Johns Hopkins University School of Medicine, Baltimore, Maryland
*
Correspondence and reprint requests to: E. Mark Mahone, Ph.D., Department of Neuropsychology, Kennedy Krieger Institute, 1750 East Fairmount Avenue, Baltimore, MD 21231. E-mail: [email protected]

Abstract

The current study examined regional frontal lobe volumes based on functionally relevant subdivisions in contemporaneously recruited samples of boys and girls with and without attention-deficit/hyperactivity disorder (ADHD). Forty-four boys (21 ADHD, 23 control) and 42 girls (21 ADHD, 21 control), ages 8–13 years, participated. Sulcal–gyral landmarks were used to manually delimit functionally relevant regions within the frontal lobe: primary motor cortex, anterior cingulate, deep white matter, premotor regions [supplementary motor complex (SMC), frontal eye field, lateral premotor cortex (LPM)], and prefrontal cortex (PFC) regions [medial PFC, dorsolateral PFC (DLPFC), inferior PFC, lateral orbitofrontal cortex (OFC), and medial OFC]. Compared to sex-matched controls, boys and girls with ADHD showed reduced volumes (gray and white matter) in the left SMC. Conversely, girls (but not boys) with ADHD showed reduced gray matter volume in left LPM; while boys (but not girls) with ADHD showed reduced white matter volume in left medial PFC. Reduced left SMC gray matter volumes predicted increased go/no–go commission rate in children with ADHD. Reduced left LPM gray matter volumes predicted increased go/no–go variability, but only among girls with ADHD. Results highlight different patterns of anomalous frontal lobe development among boys and girls with ADHD beyond that detected by measuring whole lobar volumes. (JINS, 2011, 17, 1047–1057)

Type
Regular Articles
Copyright
Copyright © The International Neuropsychological Society 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akkal, D., Dum, R.P., Strick, P.L. (2007). Supplementary motor area and presupplementary motor area: Targets of basal ganglia and cerebellar output. Journal of Neuroscience, 27, 1065910673.CrossRefGoogle ScholarPubMed
Alexander, G.E., Crutcher, M.D. (1990). Functional architecture of basal ganglia circuits: Neural substrates of parallel processing. Trends in Neuroscience, 13, 266271.CrossRefGoogle ScholarPubMed
Anderson, S.W., Bechara, A., Damasio, H., Tranel, D., Damasio, A.R. (1999). Impairment of social and moral behavior related to early damage in human prefrontal cortex. Nature Neuroscience, 2, 10321037.CrossRefGoogle ScholarPubMed
Basser, P.J., Pierpaoli, C. (1996). Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. Journal of Magnetic Resonance B, 111, 209219.Google Scholar
Biederman, J., Mick, E., Faraone, S.V. (2000). Age-dependent decline of symptoms of attention deficit hyperactivity disorder: Impact of remission definition and symptom type. American Journal of Psychiatry, 157, 816818.Google Scholar
Cahill, L. (2006). Why sex matters for neuroscience. Nature Reviews Neuroscience, 7, 477484.Google Scholar
Carmona, S., Proal, E., Haekzema, E.A., Gispert, J.D., Picado, M., Moreno, I., Vilarroya, O. (2009). Ventro-striatal reductions underpin symptoms of hyperactivity and impulsivity in attention-deficit/hyperactivity disorder. Biological Psychiatry, 66, 972977.Google Scholar
Castellanos, F.X., Giedd, J.N., Berquin, P.C., Walter, J.M., Sharp, W., Tran, T., Rapoport, J.L. (2001). Quantitative brain magnetic resonance imaging in girls with attention-deficit/hyperactivity disorder. Archives of General Psychiatry, 58, 289295.CrossRefGoogle ScholarPubMed
Castellanos, F.X., Geidd, J.N., Marsh, W.L., Hamburger, S.D., Vaituzis, A.C., Dickstein, D.P., Rapoport, J.L. (1996). Quantitative brain magnetic resonance imaging in attention-deficit hyperactivity disorder. Archives of General Psychiatry, 53, 607616.CrossRefGoogle ScholarPubMed
Cole, W., Mostofsky, S., Larson, J., Denckla, M., Mahone, E.M. (2008). Age-related changes in motor subtle signs among girls and boys with ADHD. Neurology, 71, 15141520.CrossRefGoogle ScholarPubMed
Conners, C.K. (1997). Conners’ Rating Scales – Revised. North Tonawanda, New York: Multi-Health Systems Inc.Google Scholar
Desikan, R.S., Segonne, F., Fischl, B., Quin, B.T., Dickerson, B.C., Blacker, D., Killiany, R.J. (2007). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage, 31, 968980.Google Scholar
Ellison-Wright, I., Ellison-Wright, Z., Bullmore, E. (2008). Structural brain change in attention deficit hyperactivity disorder identified by meta-analysis. BMC Psychiatry, 8, 51.CrossRefGoogle ScholarPubMed
Filipek, P.A., Semrud-Clikeman, M., Steingard, R.J., Renshaw, P.F., Kennedy, D.N., Biederman, J. (1997). Volumetric MRI analysis comparing subjects having attention-deficit hyperactivity disorder with normal controls. Neurology, 48, 589601.CrossRefGoogle ScholarPubMed
Fischl, B., Liu, A., Dale, A.M. (2001). Automated manifold surgery: Constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Transactions on Medical Imaging, 20, 7080.Google Scholar
Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Segonne, F., Salat, D.H., Dale, A.M. (2004). Automatically parcellating the human cerebral cortex. Cerebral Cortex, 14, 1122.Google Scholar
Fredericksen, K.A., Cutting, L.E., Kates, W.R., Mostofsky, S.H., Cooper, K.L., Lanham, D.C., Kaufman, W.E. (2002). Disproportionate increases of white matter in right frontal lobe in Tourette syndrome. Neurology, 58, 8589.CrossRefGoogle ScholarPubMed
Gogtay, N., Gied, J.N., Lusk, L., Hayashi, K.M., Greenstein, D., Vaituzis, A.C., Thompson, P.M. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences of the United States of America, 101, 81748179.CrossRefGoogle ScholarPubMed
Halperin, J.M., Schulz, K.P. (2006). Revisiting the role of the prefrontal cortex in attention-deficit/hyperactivity disorder. Psychological Bulletin, 132, 560581.Google Scholar
Hill, D., Yeo, R., Campbell, R., Hart, B., Vigil, J., Brooks, W. (2003). Magnetic resonance imaging correlates of attention-deficit/hyperactivity disorder in children. Neuropsychology, 17, 496506.Google Scholar
Hollingshead, A.B. (1975). Four factor index of social status. New Haven, CT: Yale University, Department of Sociology.Google Scholar
Hynd, G.W., Semrud-Clikeman, M., Lorys, A., Novey, E.S., Eliopulos, D. (1990). Brain morphology in developmental dyslexia and attention deficit disorder/hyperactivity. Archives of Neurology, 47, 919926.Google Scholar
Kates, W.R., Frederikse, M., Mostofsky, S.H., Folley, B.S., Cooper, K., Mazur-Hopkins, P., Kaufman, W.E. (2002). MRI parcellation of the frontal lobe in boys with attention deficit hyperactivity disorder or Tourette syndrome. Psychiatry Research, 116, 6381.Google Scholar
Kelly, A.M., Margulies, D.S., Castellanos, F.X. (2007). Recent advances in structural and functional brain imaging studies of attention-deficit/hyperactivity disorder. Current Psychiatry Reports, 9, 401407.CrossRefGoogle ScholarPubMed
Kramer, J.H., Quitania, L., Dean, D., Neuhaus, J., Rosen, H.J., Halabi, C., Miller, B.L. (2007). Magnetic resonance imaging correlates of set shifting. Journal of the International Neuropsychological Society, 13, 386392.CrossRefGoogle ScholarPubMed
Lenroot, R.K., Gogtay, N., Greenstein, D.K., Wells, E.M., Wallace, G.L., Clasen, L.S., Gied, J.N. (2007). Sexual dimorphism of brain developmental trajectories during childhood and adolescence. Neuroimage, 36, 10651073.CrossRefGoogle ScholarPubMed
Lijffijt, M., Kenemans, J.L., Verbaten, M.N., Van Engeland, H. (2005). A meta-analytic review of stopping performance in attention-deficit/hyperactivity disorder: Deficient inhibitory motor control? Journal Abnormal Psychology, 114, 216222.Google Scholar
Mackie, S., Shaw, P., Lenroot, R., Pierson, R., Greenstein, D.K., Nugent, T.F., Rapoport, J.L. (2007). Cerebellar development and clinical outcome in attention deficit hyperactivity disorder. American Journal of Psychiatry, 164, 647655.Google Scholar
Macneil, L.K., Xavier, P., Garvey, M.A., Gilbert, D.L., Ranta, M.E., Denckla, M.B., Mostofksy, S.H. (2011). Quantifying excessive mirror overflow in children with attention-deficit/hyperactivity disorder. Neurology, 76, 622628.Google Scholar
Mahone, E.M., Wodka, E.L. (2008). The neurobiological profile of girls with ADHD. Developmental Disabilities Research Reviews, 14, 276284.CrossRefGoogle ScholarPubMed
Makris, N., Meyer, J.W., Bates, J.F., Yeterian, E.H., Kennedy, D.N., Caviness, V.S. (1999). MRI based topographic parcellation of human cerebral white matter and nuclei II. Rationale and applications with systematics of cerebral connectivity. Neuroimage, 9, 1845.Google Scholar
Marsh, R., Gerber, A.J., Peterson, B.S. (2008). Neuroimaging studies of normal brain development and their relevance for understanding childhood neuropsychiatric disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 47, 12331251.CrossRefGoogle ScholarPubMed
McAuliffe, M., Lalonde, E., McGarry, D., Gandler, W., Csaky, K., & Trus, B. (2001). Medical image processing, analysis and visualization in clinical research. Paper presented at the IEEE Symposium on computer-based medical systems.CrossRefGoogle Scholar
Miller, B.T., D'Esposito, M. (2005). Searching for “the top” in top-down control. Neuron, 48, 535538.Google Scholar
Mink, J.W. (1996). The basal ganglia: Focused selection and inhibition of competing motor programs. Progress in Neurobiology, 50, 381425.Google Scholar
Mostofsky, S., Cooper, K., Kates, W., Denckla, M., Kaufman, W. (2002). Smaller prefrontal and premotor volumes in boys with ADHD. Biological Psychiatry, 52, 785794.CrossRefGoogle Scholar
Mostofsky, S.H., Reis, A.L., Lockhart, P., Denckla, M.B. (1998). Evaluation of cerebellar size in attention deficit hyperactivity disorder. Journal of Child Neurology, 13, 434439.Google Scholar
Mostofsky, S.H., Simmonds, D.J. (2008). Response inhibition and response selection: Two sides of the same coin. Journal of Cognitive Neuroscience, 20, 751761.Google Scholar
Nachev, P., Kennard, C., Husain, M. (2008). Functional role of the supplementary and pre-supplementary motor areas. Nature Reviews Neuroscience, 9, 856869.CrossRefGoogle ScholarPubMed
Qiu, A., Crocetti, D., Adler, A., Mahone, E.M., Denckla, M.B., Miller, M.I., Mostofsky, S.H. (2009). Basal ganglia volume and shape in children with attention deficit hyperactivity disorder. American Journal of Psychiatry, 166, 7482.CrossRefGoogle ScholarPubMed
Ranta, M.E., Crocetti, D., Claus, J.A., Kraut, M.A., Mostofsky, S.H., Kaufman, W.E. (2009). Manual MRI parcellation of the frontal lobe. Psychiatry Research, 172(2), 147154.Google Scholar
Reich, W., Welner, Z., Herjanic, B. (1997). The diagnostic interview for children and adolescents-IV. North Tonawanda: Multi-Health Systems.Google Scholar
Rubia, K., Overmeyer, S., Taylor, E., Brammer, M., Williams, S.C., Simmons, A., Bullmore, E.T. (2000). Functional frontalisation with age: Mapping neurodevelopmental trajectories with fMRI. Neuroscience and Biobehavioral Reviews, 24, 1319.CrossRefGoogle ScholarPubMed
Ryan, M., Martin, R.B., Denckla, M.B., Mostofsky, S.H., Mahone, E.M. (2010). Interstimulus jitter facilitates response control in children with ADHD. Journal of the International Neuropsychological Society, 16, 388393.CrossRefGoogle ScholarPubMed
Segonne, F., Dale, A.M., Busa, E., Glessner, M., Salat, D., Hahn, H.K., et al. (2004). A hybrid approach to the skull stripping problem in MRI. Neuroimage, 22, 10601075.Google Scholar
Segonne, F., Grimson, E., Fischl, B. (2005). A genetic algorithm for the topology correction of cortical surfaces. Information Processing in Medical Imaging, 19, 393405.Google Scholar
Shaw, P., Eckstrand, K., Sharp, W., Blumenthal, J., Lerch, J.P., Greenstein, D., Rapoport, J.L. (2007). Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proceedings of the National Academy of Sciences of the United States of America, 104, 1964919654.Google Scholar
Shaw, P., Lalonde, F., Lepage, C., Rabin, C., Eckstrand, K., Sharp, W., Raporport, J. (2009). Development of cortical asymmetry in typically developing children and its disruption in attention-deficit/hyperactivity disorder. Archives of General Psychiatry, 66, 888896.Google Scholar
Shaw, P., Sharp, W.S., Morrison, M., Eckstrand, K., Greenstein, D.K., Classen, L.S., Rapaport, J.L. (2009). Psychostimulant treatment and the developing cortex in attention deficit hyperactivity disorder. American Journal of Psychiatry, 166, 5863.Google Scholar
Tiemeier, H., Lenroot, R.K., Greenstein, D.K., Tran, L., Pierson, R., Gied, J.N. (2010). Cerebellum development during childhood and adolescence: A longitudinal morphometric MRI study. Neuroimage, 49, 6370.Google Scholar
Wechsler, D.L. (1991). Wechsler intelligence scale for children, third edition. San Antonio, TX: The Psychological Corporation.Google Scholar
Wechsler, D.L. (2003). Wechsler intelligence scale for children, fourth edition. San Antonio, TX: The Psychological Corporation.Google Scholar
Wellington, T.M., Semrud-Clikeman, M., Gregory, A.L., Murphy, J.M., Lancaster, J.L. (2006). Magnetic resonance imaging volumetric analysis of the putamen in children with ADHD: Combined type versus control. Journal of Attention Disorders, 10, 171180.CrossRefGoogle ScholarPubMed
Wodka, E.L., Mahone, E.M., Blankner, J.G., Larson, J.C., Fotedar, S., Denckla, M.B., Mostofsky, S.H. (2007). Evidence that response inhibition is a primary deficit in ADHD. Journal of Clinical and Experimental Neuropsychology, 29, 345356.Google Scholar
Wolosin, S.M., Richardson, M.E., Hennessey, J.G., Denckla, M.B., Mostofsky, S.H. (2009). Abnormal cerebral cortex structure in children with ADHD. Human Brain Mapping, 30, 175184.Google Scholar
Yang, P., Wang, P.N., Chuang, K.H., Jong, Y.J., Chao, T.C., Wu, M.T. (2008). Absence of gender effect on children with attention-deficit/hyperactivity disorder as assessed by optimized voxel-based morphometry. Psychiatry Research, 164, 245253.Google Scholar
Supplementary material: PDF

Mahone Supplementary Tables

Mahone Supplementary Tables

Download Mahone Supplementary Tables(PDF)
PDF 92.7 KB