Altered cortico-striatal-thalamic connectivity in relation to spatial working memory capacity in children with ADHD

Frontiers in Psychiatry

Volumn 3, Issue JAN, 2012, Pages

  Mills, Kathryn L ^a,b   Bathula, Deepti ^a,c   Dias, Taciana G Costa ^a   Iyer, Swathi P ^a   Fenesy, Michelle C ^a   Musser, Erica D ^a   Stevens, Corinne A ^a   Thurlow, Bria L ^a   Carpenter, Samuel D ^a   Nagel, Bonnie J ^a   Nigg, Joel T ^a   Fair, Damien A ^a,d  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c INDIAN INSTITUTE OF TECHNOLOGY ROPAR   (India)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

ADHD; Connectivity; fMRI; Striatum; Thalamus; Working memory

Indexed keywords

ARTICLE; ATTENTION DEFICIT DISORDER; BRAIN FUNCTION; BRAIN RADIOGRAPHY; BRAIN REGION; BRAIN SIZE; CHILD; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; LATERAL GENICULATE BODY; MAJOR CLINICAL STUDY; MALE; MENTAL CAPACITY; MENTAL PERFORMANCE; OCCIPITAL CORTEX; PARIETAL CORTEX; PREFRONTAL CORTEX; PREMOTOR CORTEX; PULVINAR; PUTAMEN; SCHOOL CHILD; SOMATOSENSORY CORTEX; SPATIAL MEMORY; TEMPORAL CORTEX; THALAMUS; WORKING MEMORY;

EID: 84861485697     PISSN: None     EISSN: 16640640     Source Type: Journal    
DOI: 10.3389/fpsyt.2012.00002     Document Type: Article

References (67)

1. Aggleton, J. P., Hunt, P. R., Nagle, S., and Neave, N. (1996). The effects of selective lesions within the anterior thalamic nuclei on spatial memory in the rat. Behav. Brain Res. 81, 189-198.
2. Baddeley, A. (1996). The fractiona-tion of working memory. Proc. Natl. Acad. Sci. U.S.A. 93, 13468-13472.
3. Behrens, T. E., Johansen-Berg, H., Wool-rich, M. W., Smith, S. M., Wheeler-Kingshott, C. A., Boulby, P. A., Barker, G. J., Sillery, E. L., Shee-han, K., Ciccarelli, O., Thompson, A. J., Brady, J. M., and Matthews, P. M. (2003). Non-invasive map-pingof connections between human thalamus and cortex using diffusion imaging. Nat. Neurosci. 6, 750-757.
4. Bi, G., and Poo, M. (1999). Distributed synaptic modification in neural networks induced by patterned stimulation. Nature 401, 792-796.
5. Biswal, B., Yetkin, F. Z., Haughton, V. M., and Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537-541.
6. Booth, J. R., Burman, D. D., Meyer, J. R., Lei, Z., Trommer, B. L., Davenport, N. D., Li, W., Parrish, T. B., Gitel-man, D. R., and Mesulam, M. M. (2005). Larger deficits in brain networks for response inhibition than for visual selective attention in attention deficit hyperactivity disorder (ADHD). J. Child Psychol. Psychiatry 46, 94-111.
7. Brown, A. B., Biederman, J., Valera, E., Makris, N., Doyle, A., Whitfield-Gabrieli, S., Mick, E., Spencer, T., Faraone, S., and Seidman, L. (2011). Relationship of DAT1 and adult ADHD to task-positive and task-negative workingmemory networks. Psychiatry Res. 193, 7-16.
8. Cao, X., Cao, Q., Long, X., Sun, L., Sui, M., Zhu, C., Zuo, X., Zang, Y., and Wang, Y. (2009). Abnormal resting-state functional connectivity patterns of the putamen in medication-naïve children with attention deficit hyperactivity disorder. Brain Res. 1303, 195-206.
9. Casey, B. J., Castellanos, F. X., Giedd, J. N., Marsh, W. L., Hamburger, S. D., Schubert, A. B., Vauss, Y. C., Vaituzis, A. C., Dickstein, D. P., Sar-fatti, S. E., and Rapoport, J. L. (1997). Implication of right frontostriatal circuitry in response inhibition and attention-deficit/hyperactivity disorder. J. Am. Acad. Child Adolesc. Psychiatry 36, 374-383.
10. Casey, B. J., Nigg, J. T., and Durston, S. (2007). New potential leads in the biology and treatment of attention deficit-hyperactivity disorder. Curr. Opin. Neurol. 20, 119-124.
11. Castellanos, F. X. (1997). Toward a pathophysiology of attention-deficit/hyperactivity disorder. Clin. Pediatr. (Phila). 36, 381-393.
12. Castellanos, F. X., Giedd, J. N., Eck-burg, P., Marsh, W. L., Vaituzis, A. C., Kaysen, D., Hamburger, S. D., and Rapoport, J. L. (1994). Quantitative morphology of the caudate nucleus in attention deficit hyperac-tivity disorder. Am. J. Psychiatry 151, 1791-1796.
13. Castellanos, F. X., Lee, P. P., Sharp, W., Jeffries, N. O., Greenstein, D. K., Clasen, L. S., Blumenthal, J. D., James, R. S., Ebens, C. L., Walter, J. M., Zijdenbos, A., Evans, A. C., Giedd, J. N., and Rapoport, J. L. (2002). Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. JAMA 288, 1740-1748
14. Castellanos, F. X., Margulies, D. S., Kelly, C., Uddin, L. Q., Ghaffari, M., Kirsch, A., Shaw, D., Shehzad, Z., Di Mar-tino, A., Biswal, B., Sonuga-Barke, E. J., Rotrosen, J., Adler, L. A., and Milham, M. P. (2008). Cingulate- precuneus interactions: a new locus of dysfunction in adult attention- deficit/hyperactivity disorder. Biol. Psychiatry 63, 332-337.
15. Castellanos, F. X., and Tannock, R. (2002). Neuroscience of attention-deficit/hyperactivity disorder: the search for endophenotypes. Nat. Rev. Neurosci. 3, 617-628.
16. CeNeS. (1998). Cambridge Neuropsy-chological Test Automated Battery (Version 2.35). Cambridge: CeNeS Cognition.
17. Dickstein, S. G., Bannon, K., Castel-lanos, F. X., and Milham, M. P. (2006). The neural correlates of attention deficit hyperactivity disorder: an ALE meta-analysis. J. Child Psychol. Psychiatry 47, 1051-1062.
18. Dosenbach, N. U., Fair, D. A., Miezin, F. M., Cohen, A. L., Wenger, K. K., Dosenbach, R. A. T., Fox, M. D., Sny-der, A. Z., Vincent, J. L., Raichle, M. E., Schlaggar, B. L., and Petersen, S. E. (2007). Distinct brain networks for adaptive and stable task control in humans. Proc. Natl. Acad. Sci. U.S.A. 104, 11073-11078.
19. Dosenbach, N. U., Visscher, K. M., Palmer, E. D., Miezin, F. M., Wenger, K. K., Kang, H. C., Burgund, E. D., Grimes, A. L., Schlaggar, B. L., and Petersen, S. E. (2006). A core system for the implementation of task sets. Neuron 50, 799-812.
20. Doyle, A. E., Faraone, S. V., Seidman, L. J., Willcutt, E. G., Nigg, J. T., Waldman, I. D., Pennington, B. F., Peart, J., and Biederman, J. (2005). Are endophenotypes based on measures of executive functions useful for molecular genetic studies of ADHD? J. Child Psychol. Psychiatry 46, 774-803.
21. Durston, S., Tottenham, N. T., Thomas, K. M., Davidson, M. C., Eigsti, I. M., Yang, Y., Ulug, A. M., and Casey, B. J. (2003). Differential patterns of striatal activation in young chil dren with and without ADHD. Biol. Psychiatry 53, 871-878.
22. Ellison-Wright, I., Ellison-Wright, Z., and Bullmore, E. (2008). Structural brain change in attention deficit hyperactivity disorder identified by metaanalysis. BMC Psychiatry 8, 51. doi: 10.1186/1471-244X-8-51
23. Fair, D. A., Bathula, D., Mills, K. L., Dias, T. G., Blythe, M. S., Zhang, D., Sny-der, A. Z., Raichle, M. E., Stevens, A. A., Nigg, J. T., and Nagel, B. J. (2010a). Maturing thalamocortical functional connectivity across devel opment. Front. Syst. Neurosci. 4:10. doi: 10.3389/fnsys.2010.00010
24. Fair, D. A., Posner, J., Nagel, B. J., Bathula, D., Dias, T. G., Mills, K. L., Blythe, M. S., Giwa, A., Schmitt, C. F., and Nigg, J. T. (2010b). Atypical default network connectivity in youth with attention- deficit/hyperactivity disorder. Biol. Psychiatry 68, 1084-1091.
25. Fair, D. A., Cohen, A. L., Dosenbach, N. U., Church, J. A., Miezin, F. M., Barch, D. M., Raichle, M. E., Petersen, S. E., and Schlaggar, B. L. (2008). The maturing architecture of the brain's default network. Proc. Natl. Acad. Sci. U.S.A. 105, 4028-4032.
26. Fair, D. A., Cohen, A. L., Power, J. D., Dosenbach, N. U., Church, J. A., Miezin, F. M., Schlaggar, B. L., and Petersen, S. E. (2009). Functional brain networks develop from a "local to distributed" organization. PLoS Comput. Biol. 5, e1000381. doi: 10.1371/journal.pcbi.1000381
27. Fair, D. A., Dosenbach, N. U., Church, J. A., Cohen, A. L., Brahmbhatt, S., Miezin, F. M., Barch, D. M., Raichle, M. E., Petersen, S. E., and Schlaggar, B. L. (2007a). Development of distinct control networks through segregation and integration. Proc. Natl. Acad. Sci. U.S.A. 104, 13507-13512.
28. Fair, D. A., Schlaggar, B. L., Cohen, A. L., Miezin, F. M., Dosenbach, N. U., Wenger, K. K., Fox, M. D., Snyder, A. Z., Raichle, M. E., and Petersen, S. E. (2007b). A method for using blocked and event-related fMRI data to study "resting state" functional connectivity. Neuroimage 35, 396-405.
29. Finke, K., Schwarzkopf, W., Müller, U., Frodl, T., Müller, H. J., Schneider, W. X., Engel, R. R., Riedel, M., Möller, H. J., and Hennig-Fast, K. (2011). Disentangling the adult attention-deficit hyperactiv-ity disorder endophenotype: parametric measurement of attention. J. Abnorm. Psychol. 120, 890-901.
30. Forman, S. D., Cohen, J. D., Fitzgerald, M., Eddy, W. F., Mintun, M. A., and Noll, D. C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn. Reson. Med. 33, 636-647.
31. Fox, M. D., and Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700-711.
32. Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., and Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U.S.A. 102, 9673-9678.
33. Gau, S. S., and Shang, C. Y. (2010). Executive functions as endopheno-types in ADHD: evidence from the Cambridge Neuropsychological Test Battery (CANTAB). J. Child Psychol. Psychiatry 51, 838-849.
34. Giedd, J. N., Blumenthal, J., Mol-loy, E., and Castellanos, F. X. (2001). Brain imaging of attention deficit/hyperactivity disorder. Ann. N. Y. Acad. Sci. 931, 33-49.
35. Haber, S. N., and Calzavara, R. (2009). The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res. Bull. 78, 69-74.
36. Insel, T., Cuthbert, B., Garvey, M., Heinssen, R., Pine, D. S., Quinn, K., Sanislow, C., and Wang, P. (2010). Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am. J. Psychiatry 167, 748-751.
37. Ivanov, I., Bansal, R., Hao, X., Zhu, H., Kellendonk, C., Miller, L., Sanchez-Pena, J., Miller, A. M., Chakravarty, M. M., Klahr, K., Durkin, K, Green-hill, L. L., and Peterson, B. S. (2010). Morphological abnormalities of the thalamus in youths with attention deficit hyperactivity disorder. Am. J. Psychiatry 167, 397-408.
38. Jones, E. G. (2007). The Thalamus. Cambridge: University Press.
39. Konrad, K., Neufang, S., Hanisch, C., Fink, G. R., and Herpertz-Dahlmann, B. (2006). Dysfunctional attentional networks in children with attention deficit/hyperactivity disorder: evidence from an event-related functional magnetic resonance imaging study. Biol. Psychiatry 59, 643-651.
40. Lancaster, J. L., Rainey, L. H., Summer-lin, J. L., Freitas, C. S., Fox, P. T., Evans, A. C., Toga, A. W., and Mazz-iotta, J. C. (1997). Automated labeling of the human brain: a preliminary report on the development and evaluation of a forward-transform method. Hum. Brain Mapp. 5, 238-242.
41. Lancaster, J. L., Woldorff, M. G., Parsons, L. M., Liotti, M., Freitas, C. S., Rainey, L., Kochunov, P. V., Nicker-son, D., Mikiten, S. A., and Fox, P. T. (2000). Automated Talairach Atlas labels for functional brain mapping. Hum. Brain Mapp. 10, 120-131.
42. Liston, C., Cohen, M. M., Teslovich, T., Levenson, D., and Casey, B. J. (2011). Atypical prefrontal connectivity in attention-deficit/hyperactivity disorder: pathway to disease or pathological end point? Biol. Psychiatry 69, 1168-1177.
43. Miezin, F. M., Maccotta, L., Ollinger, J. M., Petersen, S. E., and Buck-ner, R. L. (2000). Characterizing the hemodynamic response: effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing. Neuroimage 11, 735-759.
44. Milner, B. (1971). Interhemispheric differences in the localization of psychological processes in man. Br. Med. Bull. 27, 272-277.
45. Nigg, J. T. (2005). Neuropsychologic theory and findings in attention-deficit/hyperactivity disorder: the state of the field and salient challenges for the coming decade. Biol. Psychiatry 57, 1424-1435.
46. Nigg, J. T., and Casey, B. J. (2005). An integrative theory of attention-deficit/hyperactivity disorder based on the cognitive and affective neu-rosciences. Dev. Psychopathol. 17, 785-806.
47. Parent, A., and Hazrati, L. N. (1995). Functional anatomy of the basal ganglia I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res. Brain Res. Rev. 20, 91-127.
48. Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., and Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59, 2142-2154.
49. Rhodes, S. M., Park, J., Seth, S., and Coghill, D. R. (2012). A comprehensive investigation of memory impairment in attention deficit hyperactivity disorder and opposi-tional defiant disorder. J. Child Psy-chol. Psychiatry 53, 128-137.
50. Shannon, B. J., Raichle, M. E., Snyder, A. Z., Fair, D. A., Mills, K. L., Zhang, D., Bache, K., Calhoun, V. D., Nigg, J. T., Nagel, B. J., Stevens, A. A., and Kiehl, K. A. (2011). Premotor functional connectivity predicts impulsivity in juvenile offenders. Proc. Natl. Acad. Sci. U.S.A. 108, 11241-11245.
51. Silk, T. J., Vance, A., Rinehart, N., Brad-shaw, J. L., and Cunnington, R. (2009). Structural development of the basal ganglia in attention deficit hyperactivity disorder: a diffusion tensor imaging study. Psychiatry Res. 172, 220-225.
52. Smyser, C. D., Inder, T. E., Shimony, J. S., Hill, J. E., Degnan, A. J., Snyder, A. Z., and Neil, J. J. (2010). Longitudinal analysis of neural network development in preterm infants. Cereb. Cortex 20, 2852-2862.
53. Sonuga-Barke, E. J. (2005). Causal models of attention-deficit/hyperactivity disorder: from common simple deficits to multiple developmental pathways. Biol. Psychiatry 57, 1231-1238.
54. Talairach, J., and Tournoux, P. (1988). Co-Planar Stereotaxic Atlas of the Human Brain. New York: Thieme Medical Publishers, Inc.
55. Teicher, M. H., Anderson, C. M., Polcari, A., Glod, C. A., Maas, L. C., and Ren-shaw, P. F. (2000). Functional deficits in basal ganglia of children with attention-deficit/hyperactivity disorder shown with functional magnetic resonance imaging relaxome-try. Nat. Med. 6, 470-473.
56. Tillman, C., Eninger, L., Forssman, L., and Bohlin, G. (2011). The relation between working memory components and ADHD symptoms from a developmental perspective. Dev. Neuropsychol. 36, 181-198.
57. Uddin, L. Q., Kelly, A. M., Biswal, B. B., Margulies, D. S., Shehzad, Z., Shaw, D., Ghaffari, M., Rotrosen, J., Adler, L. A., Castellanos, F. X., and Mil-ham, M. P. (2008). Network homogeneity reveals decreased integrity of default-mode network in ADHD. J. Neurosci. Methods 169, 249-254.
58. Van Dijk, K. R., Sabuncu, M. R., and Buckner, R. L. (2011). The influence of head motion on intrinsic functional connectivity MRI. Neuroim-age 59, 431-438.
59. Van Essen, D. C. (2005). A population-average, landmark- and surface-based (PALS) atlas of human cerebral cortex. Neuroimage 28, 635-662.
60. Van Essen, D. C., Dickson, J., Harwell, J., Hanlon, D., Anderson, C. H., and Drury, H. A. (2001). An integrated software suite for surface-based analyses of cerebral cortex. J. Am. Med. Inform. Assoc. 41, 1359-1378.
61. Van Essen, D. C., and Drury, H. A. (1997). Structural and functional analyses of human cerebral cortex using a surface-based atlas. J. Neu-rosci. 17, 7079-7102.
62. Wang, L., Zhu, C., He, Y., Zang, Y., Cao, Q., Zhang, H., Zhong, Q., and Wang, Y. (2009). Altered small-world brain functional networks in children with attention-deficit/hyperactivity disorder. Hum. Brain Mapp. 30, 638-649.
63. Westerberg, H., Hirvikoski, T., Forss-berg, H., and Klingberg, T. (2004). Visuo-spatial working memory span: a sensitive measure of cognitive deficits in children with ADHD. Child Neuropsychol. 10, 155-161.
64. Willcutt, E. G., Doyle, A. E., Nigg, J. T., Faraone, S. V., and Pen-nington, B. F. (2005). Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biol. Psychiatry 57, 1336-1346.
65. Zang, Y. F., He, Y., Zhu, C. Z., Cao, Q. J., Sui, M. Q., Liang, M., Tian, L. X., Jiang, T. Z., and Wang, Y. F. (2007). Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev. 29, 83-91.
66. Zhang, D., Snyder, A. Z., Fox, M. D., Sansbury, M. W., Shimony, J. S., and Raichle, M. E. (2008). Intrinsic functional relations between human cerebral cortex and thalamus. J. Neu-rophysiol. 100, 1740-1748.
67. Zhang, D., Snyder, A. Z., Shimony, J. S., Fox, M. D., and Raichle, M. E. (2009). Noninvasive functional and structural connectivity mapping of the human thalamo-cortical system. Cereb. Cortex 20, 1187-1194.