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Different neural substrates for executive functions in youths with ADHD: a diffusion spectrum imaging tractography study

Published online by Cambridge University Press:  08 January 2016

H.-L. Chiang
Affiliation:
Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei, Taiwan Graduate Institute of Clinical Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan Department of Psychiatry, Far Eastern Memorial Hospital, New Taipei City, Taiwan
Y.-J. Chen
Affiliation:
Institute of Medical Device and Imaging, National Taiwan University College of Medicine, Taipei, Taiwan
C.-Y. Shang
Affiliation:
Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei, Taiwan
W.-Y. I. Tseng*
Affiliation:
Institute of Medical Device and Imaging, National Taiwan University College of Medicine, Taipei, Taiwan Graduate Institute of Brain and Mind Sciences, National Taiwan University College of Medicine, Taipei, Taiwan Department of Medical Imaging, National Taiwan University Hospital, Taipei, Taiwan
S. S.-F. Gau*
Affiliation:
Department of Psychiatry, National Taiwan University Hospital and College of Medicine, Taipei, Taiwan Graduate Institute of Clinical Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan Graduate Institute of Brain and Mind Sciences, National Taiwan University College of Medicine, Taipei, Taiwan
*
*Address for correspondence: S. S.-F. Gau, M.D., Ph.D., Department of Psychiatry, National Taiwan University Hospital and College of Medicine, No. 7, Chung-Shan South Road, Taipei 10002, Taiwan. (Email: gaushufe@ntu.edu.tw) [S.S.-F.G] (Email: wytseng@ntu.edu.tw) [W.-Y.I.T]
*Address for correspondence: S. S.-F. Gau, M.D., Ph.D., Department of Psychiatry, National Taiwan University Hospital and College of Medicine, No. 7, Chung-Shan South Road, Taipei 10002, Taiwan. (Email: gaushufe@ntu.edu.tw) [S.S.-F.G] (Email: wytseng@ntu.edu.tw) [W.-Y.I.T]

Abstract

Background

The relationship between white-matter tracts and executive functions (EF) in attention deficit hyperactivity disorder (ADHD) has not been well studied and previous studies mainly focused on frontostriatal (FS) tracts. The authors explored the microstructural property of several fibre tracts hypothesized to be involved in EF, to correlate their microstructural property with EF, and to explore whether such associations differ between ADHD and typically developing (TD) youths.

Method

We assessed 45 youths with ADHD and 45 individually matched TD youths with a computerized test battery for multiple dimensions of EF. From magnetic resonance imaging, FS tract, superior longitudinal fasciculus (SLF), arcuate fasciculus (AF) and cingulum bundle (CB) were reconstructed by diffusion spectrum imaging tractography. The generalized fractional anisotropy (GFA) values of white-matter tracts were computed to present microstructural property of each tract.

Results

We found lower GFA in the left FS tract, left SLF, left AF and right CB, and poorer performance in set-shifting, sustained attention, cognitive inhibition and visuospatial planning in ADHD than TD. The ADHD and TD groups demonstrated different association patterns between EF and fibre tract microstructural property. Most of the EF were associated with microstructural integrity of the FS tract and CB in TD youths, while with that of the FS tract, SLF and AF in youths with ADHD.

Conclusions

Our findings support that the SLF, AF and CB also involve in a wide range of EF and that the main fibre tracts involved in EF are different in youths with ADHD.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2016 

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References

Ashburner, J, Friston, KJ (2011). Diffeomorphic registration using geodesic shooting and Gauss-Newton optimisation. Neuroimage 55, 954967.Google Scholar
Bidwell, LC, Willcutt, EG, Defries, JC, Pennington, BF (2007). Testing for neuropsychological endophenotypes in siblings discordant for attention-deficit/hyperactivity disorder. Biological Psychiatry 62, 991998.Google Scholar
Chamberlain, SR, Robbins, TW, Winder-Rhodes, S, Muller, U, Sahakian, BJ, Blackwell, AD, Barnett, JH (2011). Translational approaches to frontostriatal dysfunction in attention-deficit/hyperactivity disorder using a computerized neuropsychological battery. Biological Psychiatry 69, 11921203.CrossRefGoogle ScholarPubMed
Chien, YL, Gau, SS, Chiu, YN, Tsai, WC, Shang, CY, Wu, YY (2014). Impaired sustained attention, focused attention, and vigilance in youths with autistic disorder and Asperger's disorder. Research in Autism Spectrum Disorders 8, 881889.Google Scholar
Coghill, DR, Hayward, D, Rhodes, SM, Grimmer, C, Matthews, K (2014). A longitudinal examination of neuropsychological and clinical functioning in boys with attention deficit hyperactivity disorder (ADHD): improvements in executive functioning do not explain clinical improvement. Psychological Medicine 44, 10871099.Google Scholar
de Luis-Garcia, R, Cabus-Pinol, G, Imaz-Roncero, C, Argibay-Quinones, D, Barrio-Arranz, G, Aja-Fernandez, S, Alberola-Lopez, C (2015). Attention deficit/hyperactivity disorder and medication with stimulants in young children: a DTI study. Progress in Neuro-Psychopharmacology and Biological Psychiatry 57, 176184.Google Scholar
de Zeeuw, P, Mandl, RC, Hulshoff Pol, HE, van Engeland, H, Durston, S (2012). Decreased frontostriatal microstructural organization in attention deficit/hyperactivity disorder. Human Brain Mapping 33, 19411951.Google Scholar
Dibbets, P, Evers, EA, Hurks, PP, Bakker, K, Jolles, J (2010). Differential brain activation patterns in adult attention-deficit hyperactivity disorder (ADHD) associated with task switching. Neuropsychology 24, 413423.CrossRefGoogle ScholarPubMed
Downes, JJ, Roberts, AC, Sahakian, BJ, Evenden, JL, Morris, RG, Robbins, TW (1989). Impaired extra-dimensional shift performance in medicated and unmedicated Parkinson's disease: evidence for a specific attentional dysfunction. Neuropsychologia 27, 13291343.Google Scholar
Fassbender, C, Schweitzer, JB (2006). Is there evidence for neural compensation in attention deficit hyperactivity disorder? A review of the functional neuroimaging literature. Clinical Psychology Review 26, 445465.Google Scholar
Gau, SS, Chiu, CD, Shang, CY, Cheng, AT, Soong, WT (2009). Executive function in adolescence among children with attention-deficit/hyperactivity disorder in Taiwan. Journal of Developmental and Behavioral Pediatrics 30, 525534.Google Scholar
Gau, SS, Chong, MY, Chen, TH, Cheng, AT (2005). A 3-year panel study of mental disorders among adolescents in Taiwan. American Journal of Psychiatry 162, 13441350.Google Scholar
Gau, SS, Huang, WL (2014). Rapid visual information processing as a cognitive endophenotype of attention deficit hyperactivity disorder. Psychological Medicine 44, 435446.CrossRefGoogle ScholarPubMed
Gau, SS, Lin, YJ, Cheng, AT, Chiu, YN, Tsai, WC, Soong, WT (2010). Psychopathology and symptom remission at adolescence among children with attention-deficit-hyperactivity disorder. Australian & New Zealand Journal of Psychiatry 44, 323332.CrossRefGoogle ScholarPubMed
Gau, SS, Shang, CY (2010 a). Executive functions as endophenotypes in ADHD: evidence from the Cambridge Neuropsychological Test Battery (CANTAB). Journal of Child Psychology and Psychiatry 51, 838849.CrossRefGoogle ScholarPubMed
Gau, SS, Shang, CY (2010 b). Improvement of executive functions in boys with attention deficit hyperactivity disorder: an open-label follow-up study with once-daily atomoxetine. International Journal of Neuropsychopharmacology 13, 243256.CrossRefGoogle ScholarPubMed
Gau, SS, Shang, CY, Liu, SK, Lin, CH, Swanson, JM, Liu, YC, Tu, CL (2008). Psychometric properties of the Chinese version of the Swanson, Nolan, and Pelham, version IV scale – parent form. International Journal of Methods in Psychiatric Research 17, 3544.CrossRefGoogle Scholar
Gau, SS, Tseng, WL, Tseng, WY, Wu, HY (2014). Association between microstructural integrity of frontostriatal tracts and school functioning: ADHD symptoms and executive function as mediators. Psychological Medicine 30, 115.Google Scholar
Ge, H, Yin, X, Xu, J, Tang, Y, Han, Y, Xu, W, Pang, Z, Meng, H, Liu, S (2013). Fiber pathways of attention subnetworks revealed with tract-based spatial statistics (TBSS) and probabilistic tractography. PLoS ONE 8, e78831.CrossRefGoogle ScholarPubMed
Hamilton, LS, Levitt, JG, O'Neill, J, Alger, JR, Luders, E, Phillips, OR, Caplan, R, Toga, AW, McCracken, J, Narr, KL (2008). Reduced white matter integrity in attention-deficit hyperactivity disorder. Neuroreport 19, 17051708.Google Scholar
Hart, H, Radua, J, Nakao, T, Mataix-Cols, D, Rubia, K (2013). Meta-analysis of functional magnetic resonance imaging studies of inhibition and attention in attention-deficit/hyperactivity disorder: exploring task-specific, stimulant medication, and age effects. JAMA Psychiatry 70, 185198.Google Scholar
Hsu, YC, Hsu, CH, Tseng, WY (2012). A large deformation diffeomorphic metric mapping solution for diffusion spectrum imaging datasets. Neuroimage 63, 818834.Google Scholar
Ikuta, T, Shafritz, KM, Bregman, J, Peters, BD, Gruner, P, Malhotra, AK, Szeszko, PR (2014). Abnormal cingulum bundle development in autism: a probabilistic tractography study. Psychiatry Research 221, 6368.Google Scholar
Kantarci, K, Senjem, ML, Avula, R, Zhang, B, Samikoglu, AR, Weigand, SD, Przybelski, SA, Edmonson, HA, Vemuri, P, Knopman, DS, Boeve, BF, Ivnik, RJ, Smith, GE, Petersen, RC, Jack, CR Jr. (2011). Diffusion tensor imaging and cognitive function in older adults with no dementia. Neurology 77, 2634.Google Scholar
King, JB, Yurgelun-Todd, D, Stoeckel, A, DiMuzio, JM, Lopez-Larson, MP (2015). Sex differences in white matter integrity in youths with attention-deficit/hyperactivity disorder: a pilot study. Frontiers in Neuroscience 9, 232.Google Scholar
Konrad, K, Neufang, S, Hanisch, C, Fink, GR, Herpertz-Dahlmann, B (2006). Dysfunctional attentional networks in children with attention deficit/hyperactivity disorder: evidence from an event-related functional magnetic resonance imaging study. Biological Psychiatry 59, 643651.Google Scholar
Kucukboyaci, NE, Girard, HM, Hagler, DJ Jr., Kuperman, J, Tecoma, ES, Iragui, VJ, Halgren, E, McDonald, CR (2012). Role of frontotemporal fiber tract integrity in task-switching performance of healthy controls and patients with temporal lobe epilepsy. Journal of the International Neuropsychological Society 18, 5767.Google Scholar
Kuo, LW, Chen, JH, Wedeen, VJ, Tseng, WY (2008). Optimization of diffusion spectrum imaging and q-ball imaging on clinical MRI system. Neuroimage 41, 718.Google Scholar
Lawrence, KE, Levitt, JG, Loo, SK, Ly, R, Yee, V, O'Neill, J, Alger, J, Narr, KL (2013). White matter microstructure in subjects with attention-deficit/hyperactivity disorder and their siblings. Journal of the American Academy of Child and Adolescent Psychiatry 52, 431440, e434.Google Scholar
Lebel, C, Warner, T, Colby, J, Soderberg, L, Roussotte, F, Behnke, M, Davis Eyler, F, Sowell, ER (2013). White matter microstructure abnormalities and executive function in adolescents with prenatal cocaine exposure. Psychiatry Research 213, 161168.Google Scholar
Lin, CP, Wedeen, VJ, Chen, JH, Yao, C, Tseng, WY (2003). Validation of diffusion spectrum magnetic resonance imaging with manganese-enhanced rat optic tracts and ex vivo phantoms. Neuroimage 19, 482495.Google Scholar
Lin, HY, Gau, SS, Huang-Gu, SL, Shang, CY, Wu, YH, Tseng, WY (2014). Neural substrates of behavioral variability in attention deficit hyperactivity disorder: based on ex-Gaussian reaction time distribution and diffusion spectrum imaging tractography. Psychological Medicine 44, 17511764.Google Scholar
Liston, C, Malter Cohen, M, Teslovich, T, Levenson, D, Casey, BJ (2011). Atypical prefrontal connectivity in attention-deficit/hyperactivity disorder: pathway to disease or pathological end point? Biological Psychiatry 69, 11681177.Google Scholar
Lo, YC, Soong, WT, Gau, SS, Wu, YY, Lai, MC, Yeh, FC, Chiang, WY, Kuo, LW, Jaw, FS, Tseng, WY (2011). The loss of asymmetry and reduced interhemispheric connectivity in adolescents with autism: a study using diffusion spectrum imaging tractography. Psychiatry Research 192, 6066.Google Scholar
Luciana, M, Nelson, CA (1998). The functional emergence of prefrontally-guided working memory systems in four- to eight-year-old children. Neuropsychologia 36, 273293.Google Scholar
Makris, N, Buka, SL, Biederman, J, Papadimitriou, GM, Hodge, SM, Valera, EM, Brown, AB, Bush, G, Monuteaux, MC, Caviness, VS, Kennedy, DN, Seidman, LJ (2008). Attention and executive systems abnormalities in adults with childhood ADHD: a DT-MRI study of connections. Cerebral Cortex 18, 12101220.Google Scholar
Martino, J, De Witt Hamer, PC, Berger, MS, Lawton, MT, Arnold, CM, de Lucas, EM, Duffau, H (2013). Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study. Brain Structure and Function 218, 105121.Google Scholar
Mostofsky, SH, Cooper, KL, Kates, WR, Denckla, MB, Kaufmann, WE (2002). Smaller prefrontal and premotor volumes in boys with attention-deficit/hyperactivity disorder. Biological Psychiatry 52, 785794.Google Scholar
Ni, HC, Lin, YJ, Gau, SS, Huang, HC, Yang, LK (2013). An open-label, randomized trial of methylphenidate and atomoxetine treatment in adults with ADHD. Journal of Attention Disorders 16, 19591973.Google Scholar
Pavuluri, MN, Yang, S, Kamineni, K, Passarotti, AM, Srinivasan, G, Harral, EM, Sweeney, JA, Zhou, XJ (2009). Diffusion tensor imaging study of white matter fiber tracts in pediatric bipolar disorder and attention-deficit/hyperactivity disorder. Biological Psychiatry 65, 586593.Google Scholar
Peters, BD, Ikuta, T, Derosse, P, John, M, Burdick, KE, Gruner, P, Prendergast, DM, Szeszko, PR, Malhotra, AK (2014). Age-related differences in white matter tract microstructure are associated with cognitive performance from childhood to adulthood. Biological Psychiatry 75, 248256.Google Scholar
Peters, BD, Szeszko, PR, Radua, J, Ikuta, T, Gruner, P, DeRosse, P, Zhang, JP, Giorgio, A, Qiu, D, Tapert, SF, Brauer, J, Asato, MR, Khong, PL, James, AC, Gallego, JA, Malhotra, AK (2012). White matter development in adolescence: diffusion tensor imaging and meta-analytic results. Schizophrenia Bulletin 38, 13081317.Google Scholar
Peterson, DJ, Ryan, M, Rimrodt, SL, Cutting, LE, Denckla, MB, Kaufmann, WE, Mahone, EM (2011). Increased regional fractional anisotropy in highly screened attention-deficit hyperactivity disorder (ADHD). Journal of Child Neurology 26, 12961302.Google Scholar
Reese, TG, Heid, O, Weisskoff, RM, Wedeen, VJ (2003). Reduction of eddy-current-induced distortion in diffusion MRI using a twice-refocused spin echo. Magnetic Resonance in Medicine 49, 177182.CrossRefGoogle ScholarPubMed
Shang, CY, Gau, SS, Liu, CM, Hwu, HG (2011). Association between the dopamine transporter gene and the inattentive subtype of attention deficit hyperactivity disorder in Taiwan. Progress in Neuro-Psychopharmacology and Biological Psychiatry 35, 421428.Google Scholar
Shang, CY, Wu, YH, Gau, SS, Tseng, WY (2013). Disturbed microstructural integrity of the frontostriatal fiber pathways and executive dysfunction in children with attention deficit hyperactivity disorder. Psychological Medicine 43, 10931107.Google Scholar
Silk, TJ, Vance, A, Rinehart, N, Bradshaw, JL, Cunnington, R (2009). White-matter abnormalities in attention deficit hyperactivity disorder: a diffusion tensor imaging study. Human Brain Mapping 30, 27572765.Google Scholar
Takahashi, M, Iwamoto, K, Fukatsu, H, Naganawa, S, Iidaka, T, Ozaki, N (2010). White matter microstructure of the cingulum and cerebellar peduncle is related to sustained attention and working memory: a diffusion tensor imaging study. Neuroscience Letters 477, 7276.Google Scholar
Tamm, L, Barnea-Goraly, N, Reiss, AL (2012). Diffusion tensor imaging reveals white matter abnormalities in attention-deficit/hyperactivity disorder. Psychiatry Research 202, 150154.Google Scholar
Tseng, WL, Gau, SS (2013). Executive function as a mediator in the link between attention-deficit/hyperactivity disorder and social problems. Journal of Child Psychology and Psychiatry 54, 9961004.Google Scholar
Tuch, DS (2004). Q-ball imaging. Magnetic Resonance in Medicine 52, 13581372.Google Scholar
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, Mazoyer, B, Joliot, M (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273289.Google Scholar
van Ewijk, H, Heslenfeld, DJ, Zwiers, MP, Buitelaar, JK, Oosterlaan, J (2012). Diffusion tensor imaging in attention deficit/hyperactivity disorder: a systematic review and meta-analysis. Neuroscience and Biobehavioral Reviews 36, 10931106.CrossRefGoogle ScholarPubMed
Veazie, PJ (2006). When to combine hypotheses and adjust for multiple tests. Health Services Research 41, 804818.Google Scholar
Vestergaard, M, Madsen, KS, Baare, WF, Skimminge, A, Ejersbo, LR, Ramsoy, TZ, Gerlach, C, Akeson, P, Paulson, OB, Jernigan, TL (2011). White matter microstructure in superior longitudinal fasciculus associated with spatial working memory performance in children. Journal of Cognitive Neuroscience 23, 21352146.Google Scholar
Wakana, S, Nagae-Poetscher, LM, Jiang, H, van Zijl, P, Golay, X, Mori, S (2005). Macroscopic orientation component analysis of brain white matter and thalamus based on diffusion tensor imaging. Magnetic Resonance in Medicine 53, 649657.Google Scholar
Wedeen, VJ, Wang, RP, Schmahmann, JD, Benner, T, Tseng, WY, Dai, G, Pandya, DN, Hagmann, P, D'Arceuil, H, de Crespigny, AJ (2008). Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. Neuroimage 41, 12671277.CrossRefGoogle ScholarPubMed
Wu, YH, Gau, SS, Lo, YC, Tseng, WY (2014). White matter tract integrity of frontostriatal circuit in attention deficit hyperactivity disorder: association with attention performance and symptoms. Human Brain Mapping 35, 199212.Google Scholar
Yang, HN, Tai, YM, Yang, LK, Gau, SS (2013). Prediction of childhood ADHD symptoms to quality of life in young adults: adult ADHD and anxiety/depression as mediators. Research in Developmental Disabilities 34, 31683181.Google Scholar
Yeh, FC, Verstynen, TD, Wang, Y, Fernandez-Miranda, JC, Tseng, WY (2013). Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS ONE 8, e80713.Google Scholar
Yeh, FC, Wedeen, VJ, Tseng, WY (2011). Estimation of fiber orientation and spin density distribution by diffusion deconvolution. Neuroimage 55, 10541062.Google Scholar
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