Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-21T14:17:55.743Z Has data issue: false hasContentIssue false
  • English
  • Français

Differential engagement of cognitive and affective neural systems in pediatric bipolar disorder and attention deficit hyperactivity disorder

Published online by Cambridge University Press:  22 October 2009

ALESSANDRA M. PASSAROTTI ,
JOHN A. SWEENEY  and
MANI N. PAVULURI
ALESSANDRA M. PASSAROTTI*
Affiliation:
Center for Cognitive Medicine, University of Illinois Medical Center at Chicago, Chicago, IL Institute for Juvenile Research, University of Illinois Medical Center at Chicago, Chicago, IL
JOHN A. SWEENEY
Affiliation:
Center for Cognitive Medicine, University of Illinois Medical Center at Chicago, Chicago, IL Department of Bioengineering, University of Illinois Medical Center at Chicago, Chicago, IL
MANI N. PAVULURI
Affiliation:
Center for Cognitive Medicine, University of Illinois Medical Center at Chicago, Chicago, IL Institute for Juvenile Research, University of Illinois Medical Center at Chicago, Chicago, IL
*
*Correspondence and reprint requests to: Alessandra M. Passarotti, Institute for Juvenile Research and Center for Cognitive Medicine, University of Illinois at Chicago, 912 South Wood Street (M/C 913), Chicago, IL 60612. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

This fMRI study investigates the neural bases of cognitive control of emotion processing in pediatric bipolar disorder (PBD) and attention deficit hyperactivity disorder (ADHD). Seventeen un-medicated PBD patients, 15 un-medicated ADHD patients, and 14 healthy controls (HC) (mean age = 13.78 ± 2.47) performed an emotional valence Stroop Task, requiring them to match the color of an emotionally valenced word to the color of either of two adjacent circles. Both patient groups responded significantly slower than HC, but there were no group differences in accuracy. A voxel-wise analysis of variance on brain activation revealed a significant interaction of group by word valence [F(2,41) = 4.44; p = .02]. Similar group differences were found for negative and positive words. For negative versus neutral words, both patient groups exhibited greater activation in dorsolateral prefrontal cortex (DLPFC) and parietal cortex relative to HC. The PBD group exhibited greater activation in ventrolateral prefrontal cortex (VLPFC) and anterior cingulate cortex (ACC) relative to HC. The ADHD group exhibited decreased VLPFC activation relative to HC and the PBD group. During cognitive control of emotion processing, PBD patients deployed the VLPFC to a greater extent than HC. The ADHD patients showed decreased VLPFC engagement relative to both HC and PBD patients. (JINS, 2010, 16, 106–117.)

Keywords

Functional magnetic resonance imaging (fMRI)BipolarADHDAttentionEmotionStroopChildAdolescentDevelopment
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 16 , Issue 1 , January 2010 , pp. 106 - 117
Copyright
Copyright © The International Neuropsychological Society 2009

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

REFERENCES

Adler, C.M., DelBello, M.P., Mills, N.P., Schmithorst, V., Holland, S., & Strakowski, S.M. (2005). Comorbid ADHD is associated with altered patterns of neuronal activation in adolescents with bipolar disorder performing a simple attention task. Bipolar Disorders, 7, 577–588.CrossRefGoogle ScholarPubMed
Altshuler, L.L., Bartzokis, G., Grieder, T., Curran, J., Jimenez, T., Leight, K., et al. (2000). An MRI study of temporal lobe structures in men with bipolar disorder or schizophrenia. Biological Psychiatry, 48, 147–162.CrossRefGoogle ScholarPubMed
American Psychiatric Association. (1994). Diagnostic and Statistical Manual of Mental Disorders IV (4th ed.). Washington, DC: American Psychiatric Association Press.Google Scholar
Annett, M. (1970). A classification of hand preference by association analysis. British Journal of Psychology, 61, 303–321.CrossRefGoogle ScholarPubMed
Aron, A.R., Fletcher, P.C., Bullmore, E.T., Sahakian, B.J., & Robbins, T.W. (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nature Neuroscience, 6, 115–116.CrossRefGoogle ScholarPubMed
Barkley, R.A. (1997). Behavioral inhibition, sustained attention, and executive functions: Constructing a unifying theory of ADHD. Psychological Bulletin, 121, 65–94.CrossRefGoogle ScholarPubMed
Blumberg, H.P., Leung, H.C., Skudlarski, P., Lacadie, C., Fredericks, C.A., Harris, B.C., et al. (2003). A functional magnetic resonance imaging study of bipolar disorder: State and trait-related dysfunction in ventral prefrontal cortices. Archives of General Psychiatry, 60, 599–607.CrossRefGoogle ScholarPubMed
Botvinick, M., Braver, T.S., Barch, D.M., Carter, C.S., & Cohen, J.D. (2001). Conflict monitoring and cognitive control. Psychological Review, 108, 624–652.CrossRefGoogle ScholarPubMed
Braaten, E.B., & Rosén, L.A. (2000). Self-regulation of affect in attention-deficit hyperactivity disorder (ADHD) and non-ADHD boys: Differences in empathic responding. Journal of Consulting and Clinical Psychology, 68, 313–321.CrossRefGoogle ScholarPubMed
Bradley, M.M., & Lang, P.J. (1999). Affective Norms for English Words (ANEW): Stimuli, Instruction Manual and Affective Ratings. Gainsville, FL: University of Florida Center for Research in Psychophysiology.Google Scholar
Bush, G., Frazier, J.A., Rauch, S.L., Seidman, L.J., Whalen, P.J., Jenike, M.A., et al. (1999). Anterior cingulate cortex dysfunction in attention-deficit/hyperactivity disorder revealed by fMRI and the counting Stroop. Biological Psychiatry, 45, 1542–1552.CrossRefGoogle ScholarPubMed
Bush, G., Luu, P., & Posner, M.I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Science, 4, 215–222.CrossRefGoogle ScholarPubMed
Casey, R.J. (1996). Emotional competence in children with externalizing and internalizing disorders. In Lewis, M. & Sullivan, M. (Eds.), Emotional Development in Atypical Children (pp. 161–183). Hillsdale, NJ: Erlbaum.Google Scholar
Casey, B.J., Castellanos, F.X., Giedd, J.N., Marsh, W.L., Hamburger, S.D., Schubert, A.B., et al. (1997). Implication of right frontostriatal circuitry in response inhibition and attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 36, 374–383.CrossRefGoogle ScholarPubMed
Chang, K., Adleman, N.E., Dienes, K., Simeonova, D.I., Menon, V., Reiss, A. (2004). Anomalous prefrontal-subcortical activation in familial pediatric bipolar disorder: a functional magnetic resonance imaging investigation. Archives of General Psychiatry 61, 781–792.CrossRefGoogle ScholarPubMed
Compton, R.J., Banich, M.T., Mohanty, A., Milham, M.P., Herrington, J., Miller, G.A., et al. (2003). Paying attention to emotion: An fMRI investigation of cognitive and emotional Stroop task. Cognitive Affective and Behavioral Neuroscience, 3, 81–96.CrossRefGoogle Scholar
Cox, R.W. (1996). AFNI. Software for analysis and visualization of functional magnetic resonance neuroimages. Computational Biomedical Research, 29, 162–173.CrossRefGoogle ScholarPubMed
Desman, C., Schneider, A., Ziegler-Kirbach, E., Petermann, F., Mohr, B., & Hampel, P. (2006). Behavioural inhibition and emotion regulation among boys with ADHD during a go-/nogo-task. Praxis der Kinderpsychologie und Kinderpsychiatrie, 55, 328–349.Google ScholarPubMed
Dickstein, D.P., Garvey, M., Pradella, A.G., Greenstein, D.K., Sharp, W.S., Castellanos, F.X., et al. (2005). Neurologic examination abnormalities in children with bipolar disorder or attention deficit/hyperactivity disorder. Biological Psychiatry, 58, 517–524.CrossRefGoogle ScholarPubMed
Dickstein, D.P., Rich, B.A., Roberson-Nay, R., Berghorst, L., Vinton, D., Pine, D.S., et al. (2007). Neural activation during encoding of emotional faces in pediatric bipolar disorder. Bipolar Disorders, 9, 679–692.CrossRefGoogle ScholarPubMed
Doyle, A.E., Willcutt, E.G., Seidman, L.J., Biederman, J., Chouinard, V.A., Silva, J., et al. (2005). Attention-deficit/hyperactivity disorder endophenotypes. Biological Psychiatry, 57, 1324–1335.CrossRefGoogle ScholarPubMed
DuPaul, G.J., Power, T.J., Anastopulous, A.D., & Reid, R. (1998). ADHD Rating Scale, Vol. IV. New York: Guilford Press.Google Scholar
Eddy, W.F., Fitzgerald, M., Genovese, C.R., Mockus, A., & Noll, D.C. (1996). Functional image analysis software - computational olio. In Prat, A. (Ed.), Proceedings in Computational Statistics (pp. 39–49). Heidelberg: Physica-Verlag.Google Scholar
Frangou, S., Haldane, M., Roddy, D., & Kumari, V. (2005). Evidence for deficit in tasks of ventral, but not dorsal, prefrontal executive function as an endophenotypic marker for bipolar disorder. Biological Psychiatry, 58, 838–839.CrossRefGoogle Scholar
Friedman, S.R., Rapport, L.J., Lumley, M., Tzelepis, A., VanVoorhis, A., Stettner, L., et al. (2003). Aspects of social and emotional competence in adult attention-deficit/hyperactivity disorder. Neuropsychology, 17, 50–58.CrossRefGoogle ScholarPubMed
Galanter, C.A., & Leibenluft, E. (2008). Frontiers between attention deficit hyperactivity disorder and bipolar disorder. Child and Adolescent Psychiatric Clinics of North America, 17, 325–346.CrossRefGoogle ScholarPubMed
Geller, B., Warner, K., Williams, M., & Zimerman, B. (1998). Prepubertal and young adolescent bipolarity versus ADHD: Assessment and validity using the WASH-U-KSADS, CBCL, and TRF. Journal of Affective Disorders, 51, 93–100.CrossRefGoogle Scholar
Gilhooly, K.J., & Logie, R.H. (1980). Age of acquisition, imagery, concreteness, familiarity and ambiguity measures for 1,944 words. Behaviour Research Methods and Instrumentation, 12, 395–427.CrossRefGoogle Scholar
Gruber, S.A., Rogowska, J., & Yurgelun-Todd, D.A. (2004). Decreased activation of the anterior cingulate in bipolar patients: An fMRI study. Journal of Affective Disorders, 82, 191–201.CrossRefGoogle ScholarPubMed
Kemmotsu, N., Villalobos, M.E., Gaffrey, M.S., Courchesne, E., & Muller, R.A. (2005). Activity and functional connectivity of inferior frontal cortex associated with response conflict. Cognitive Brain Research, 24, 335–342.CrossRefGoogle ScholarPubMed
Klein, G.S. (1964). Semantic power measured through the interference of words with color-naming. American Journal of Psychology, 77, 576–588.CrossRefGoogle ScholarPubMed
Konishi, S., Nakajima, K., Uchida, I., Kikyo, H., Kameyama, M., & Miyashita, Y. (1999). Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. Brain, 122, 981–991.CrossRefGoogle ScholarPubMed
Lagopoulos, J., & Malhi, G.S. (2007). A functional magnetic resonance imaging study of emotional Stroop in euthymic bipolar disorder. NeuroReport, 18, 1583–1587.CrossRefGoogle ScholarPubMed
Lawrence, N.S., Williams, A.M., Surguladze, S., Giampietro, V., Brammer, M.J., Andrew, C., et al. (2004). Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression. Biological Psychiatry, 55, 578–587.CrossRefGoogle ScholarPubMed
MacDonald, A.W., Cohen, J.D., Stenger, V.A., & Carter, C.S. (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288, 1835–1838.CrossRefGoogle ScholarPubMed
Malhi, G.S., Lagopoulos, J., Sachdev, P.S., Ivanovski, B., & Shnier, R. (2005). An emotional Stroop functional MRI study of euthymic bipolar disorder. Bipolar Disorders, 7(Suppl. 5), 58–69.CrossRefGoogle ScholarPubMed
Manes, F., Sahakian, B., Clark, L., Rogers, R., Antoun, N., Aitken, M., et al. (2002). Decision-making processes following damage to the prefrontal cortex. Brain, 125, 624–639CrossRefGoogle ScholarPubMed
Menon, V., Adleman, N.E., White, C.D., Glover, G.H., & Reiss, A.L. (2001). Error-related brain activation during a go/no-go response inhibition task. Human Brain Mapping, 12, 131–143.3.0.CO;2-C>CrossRefGoogle Scholar
Passarotti, A.M., Sweeney, J.A., Pavuluri, M.N. (in press). Neural correlates of response inhibition deficits in pediatric bipolar disorder and attention deficit hyperactivity disorder. Psychiatry Research: Neuroimaging.Google Scholar
Pavuluri, M.N., O’Connor, M.M., Harral, E.M., & Sweeney, J.A. (2007). Affective neural circuitry during facial emotion processing in pediatric bipolar disorder. Biological Psychiatry, 62, 158–167.CrossRefGoogle ScholarPubMed
Pavuluri, M.N., Shenkel, L.S., Aryal, S., Harral, E., Hill, K., Herbener, E.S., et al. (2006). Neurocognitive function in unmedicated manic and medicated euthymic pediatric bipolar patients. American Journal of Psychiatry, 163, 286–293.CrossRefGoogle ScholarPubMed
Pavuluri, M.N., O’Connor, M.M., Harral, E.M., & Sweeney, J.A. (2008). An fMRI study of the interface between affective and cognitive neural circuitry in pediatric bipolar disorder. Psychiatry Research, 162, 244–245.CrossRefGoogle ScholarPubMed
Pavuluri, M.N., & Passarotti, A.M. (2008). Neural bases of emotional processing in pediatric bipolar disorder. Expert Review of Neurotherapeutics, 8, 1381–1387.CrossRefGoogle ScholarPubMed
Pavuluri, M.N., Passarotti, A.M., Harral, E.M. & Sweeney, J.A. (2009). An fMRI study of the neural correlates of incidental versus directed emotion processing in Pediatric Bipolar Disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 48 (3), 308–318.CrossRefGoogle ScholarPubMed
Petrides, M. & Pandya, D.N. (2002). Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and cortico-cortical connection patterns in the monkey. European Journal of Neuroscience, 16, 291–310.CrossRefGoogle Scholar
Posner, J., Russel, J.A., Gerber, A., Gorman, D., Colibazzi, T., Yu, S., et al. (2009). The neurophysiological bases of emotion: An fMRI study of affective circumplex using emotion-denoting words. Human Brain Mapping, 30, 883–895.CrossRefGoogle ScholarPubMed
Poznanski, E., Grossman, J., Buchsbaum, Y., Banegas, M., Freeman, L., & Gibbons, R. (1984). Preliminary studies of the reliability and validity of the children’s depression rating scale. Journal of the American Academy of Child and Adolescent Psychiatry, 23, 191–197.Google ScholarPubMed
Psychological Corporation. (1999). Wechsler Abbreviated Scale of Intelligence (WASI). San Antonio, TX: Harcourt Brace & Company.Google Scholar
Rapport, L.J., Friedman, S., Tzelepis, A., & VanVoorhis, A. (2002). Experienced emotion and affect recognition in adult attention-deficit hyperactivity disorder. Neuropsychology, 16, 102–110.CrossRefGoogle ScholarPubMed
Rich, B.A., Vinton, D.T., Roberson-Nay, R., Hommer, R.E., Berghorst, L.H., McClure, E.B., et al. (2006). Limbic hyperactivation during processing of neutral facial expressions in children with bipolar disorder. Proceedings of the National Academy of Sciences of the United States America, 103, 8900–8905.CrossRefGoogle ScholarPubMed
Rosenthal, R. (1991). Meta-analytic procedures for social research, Newbury ParkCASageCrossRefGoogle Scholar
Roth, R.M., Koven, N.S., Randolph, J.J., Flashman, L.A., Heather, S., Ricketts, S.M., et al. (2006). Functional magnetic resonance imaging of executive control in bipolar disorder. NeuroReport, 17, 1085–1089.CrossRefGoogle ScholarPubMed
Rubia, K., Overmeyer, S., Taylor, E., Brammer, M., Williams, S.C., Simmons, A., et al. (1999). Hypofrontality in attention deficit hyperactivity disorder during higher-order motor control: A study with functional MRI. American Journal of Psychiatry, 156, 891–896.CrossRefGoogle ScholarPubMed
Rubia, K., Taylor, E., Smith, H., Oksannen, H., Overmeyer, S., & Newman, S. (2001). Neuropsychological analyses of impulsiveness in childhood hyperactivity. British Journal of Psychiatry, 179, 138–143.CrossRefGoogle ScholarPubMed
Shah, M.P., Wang, F., Kalmar, J.H., Chepenik, L.G., Tie, K., Pittman, B., et al. (2009). Role of variation in the serotonin transporter protein gene (SLC6A4) in trait disturbances in the ventral anterior cingulate in bipolar disorder. Neuropsychopharmacology, 34, 1301–1310.CrossRefGoogle ScholarPubMed
Schulz, K.P., Fan, J., Tang, C.Y., Newcorn, J.H., Buchsbaum, M.S., Cheung, A.M., et al. (2004). Response inhibition in adolescents diagnosed with attention deficit hyperactivity disorder during childhood: An event-related FMRI study. American Journal of Psychiatry, 161, 1650–1657.CrossRefGoogle ScholarPubMed
Schulz, K.P., Tang, C.Y., Fan, J., Marks, D.J., Newcorn, J.H., Cheung, A.M., et al. (2005). Differential prefrontal cortex activation during inhibitory control in adolescents with and without childhood attention-deficit/hyperactivity disorder. Neuropsychology, 19, 390–402.CrossRefGoogle ScholarPubMed
Seidman, L.J., Valera, E.M., & Bush, G. (2004). Brain function and structure in adults with attention-deficit/hyperactivity disorder. Psychiatry Clinics of North America, 27, 323–347.CrossRefGoogle ScholarPubMed
Seidman, L.J., Valera, E.M., Macris, N., Monuteux, M.C., Boriel, D.L., Kelkar, K., Kennedy, D.N., Caviness, V.S., Bush, G., Aleardi, M., Faraone, S.V., Biederman, J. (2006). Dorsolateral prefrontal and anterior cingulated cortex volumetric abnormalities in adults with attention-deficit/hyperactivity disorder identified by magnetic resonance imaging. Biological Psychiatry 60, 1071–1080.CrossRefGoogle ScholarPubMed
Singh, M.K., DelBello, M.P., Kowatch, R.A., & Strakowski, S.M. (2006). Co-occurrence of bipolar and attention-deficit hyperactivity disorder in children. Bipolar Disorders, 8, 710–720.CrossRefGoogle ScholarPubMed
Skirrow, C., McLoughlin, G., Kuntsi, J., & Asherson, P. (2009). Behavioral, Neurocognitive and treatment overlap between attention-deficit/hyperactivity disorder and mood instability. Expert Review of Neurotherapeutics, 9, 489–503.CrossRefGoogle ScholarPubMed
Stormark, K.M., Nordy, H., & Hugdahl, K. (1995). Attentional shifts to emotionally charged cues: Behavioral and ERP data. Cognition and Emotion, 9, 507–523.CrossRefGoogle Scholar
Strakowski, S.M., Adler, C.M., Holland, S.K., Mills, N.P., DelBello, M.P., & Eliassen, J.C. (2005). Abnormal FMRI brain activation in euthymic bipolar disorder patients during a counting Stroop interference task. American Journal of Psychiatry, 162, 1697–1705.CrossRefGoogle ScholarPubMed
Talairach, J., & Tournoux, P. (1988). Co-Planar Stereotactic Atlas of the Human Brain. New York: Thieme Medical Publishers.Google Scholar
Tamm, L., Menon, V., Ringel, J., & Reiss, A.L. (2004). Event-related fMRI evidence of frontotemporal involvement in aberrant response inhibition and task switching in attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 43, 1430–1440.CrossRefGoogle ScholarPubMed
Vaidya, C.J., Austin, G., Kirkorian, G., Ridlehuber, H.W., Desmond, J.E., Glover, G.H., et al. (1998). Selective effects of methylphenidate in attention deficit hyperactivity disorder: A functional magnetic resonance study. Proceedings of The National Academy of Sciences of the United States America 95, 14494–14499.CrossRefGoogle ScholarPubMed
Young, R.C., Biggs, J.T., Ziegler, V.E., & Meyer, D.A. (1978). A rating scale for mania: Reliability, validity and sensitivity. British Journal of Psychiatry, 133, 429–435CrossRefGoogle ScholarPubMed
Ward, B. (2000). ALPHASIM (National Institute Of Health, Bethesda). http://afni.nimh.nih.gov/pub/dist/doc/manual/AlphaSim.pdf.Google Scholar
Williams, J.M., Matthews, A., & McLead, C. (1996). The emotional Stroop task and psychopathology. Psychological Bulletin, 120, 3–24.CrossRefGoogle ScholarPubMed