Orbitofrontal reward sensitivity and impulsivity in adult attention deficit hyperactivity disorder

NeuroImage

Volumn 60, Issue 1, 2012, Pages 353-361

  Wilbertz, Gregor ^a,b,c   Tebartz van Elst, Ludger ^a   Delgado, Mauricio R ^d   Maier, Simon ^a   Feige, Bernd ^a   Philipsen, Alexandra ^a   Blechert, Jens ^e  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d RUTGERS UNIVERSITY   (United States)

^e UNIVERSITY OF SALZBURG   (Austria)

Author keywords

ADHD; FMRI; Impulsivity; OFC; Reward; Striatum

Indexed keywords

ADULT; AROUSAL; ARTICLE; ATTENTION DEFICIT DISORDER; BEHAVIOR CHANGE; BRAIN RADIATION; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DECISION MAKING; DISEASE SEVERITY; ELECTRODERMAL RESPONSE; ELECTROENCEPHALOGRAM; EMOTIONALITY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HIGH RISK BEHAVIOR; HUMAN; IMPULSIVENESS; MALE; ORBITAL CORTEX; PRIORITY JOURNAL; PSYCHOLOGIC ASSESSMENT; REWARD; RISK ASSESSMENT; SEX DIFFERENCE; TASK PERFORMANCE;

ADULT; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; CEREBRAL CORTEX; FEMALE; HUMANS; IMPULSIVE BEHAVIOR; MALE; REWARD;

EID: 84857129872     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.12.011     Document Type: Article

References (89)

1. Aase H., Sagvolden T. Infrequent, but not frequent, reinforcers produce more variable responding and deficient sustained attention in young children with attention-deficit/hyperactivity disorder (ADHD). J. Child Psychol. Psychiatry 2006, 47:457-471.
2. Association AP Diagnostic and Statistical Manual of Mental Disorders 1994, American Psychiatric Association, Washington, DC. 4th edition.
3. Barkley R.A. Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol. Bull. 1997, 121:65-94.
4. Bechara A., Tranel D., Damasio H. Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain 2000, 123(Pt 11):2189-2202.
5. Berridge K.C., Kringelbach M.L. Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology (Berl) 2008, 199:457-480.
6. Berridge K.C., Robinson T.E., Aldridge J.W. Dissecting components of reward: 'liking', 'wanting', and learning. Curr. Opin. Pharmacol. 2009, 9:65-73.
7. Biederman J., Faraone S.V., Spencer T., Wilens T., Mick E., Lapey K.A. Gender differences in a sample of adults with attention deficit hyperactivity disorder. Psychiatry Res. 1994, 53:13-29.
8. Biederman J., Faraone S.V., Monuteaux M.C., Bober M., Cadogen E. Gender effects on attention-deficit/hyperactivity disorder in adults, revisited. Biol. Psychiatry 2004, 55:692-700.
9. Biederman J., Monuteaux M.C., Mick E., Spencer T., Wilens T.E., et al. Young adult outcome of attention deficit hyperactivity disorder: a controlled 10-year follow-up study. Psychol. Med. 2006, 36:167-179.
10. Bitsakou P., Psychogiou L., Thompson M., Sonuga-Barke E.J. Delay Aversion in Attention Deficit/Hyperactivity Disorder: an empirical investigation of the broader phenotype. Neuropsychologia 2009, 47:446-456.
11. Bledsoe J., Semrud-Clikeman M., Pliszka S.R. A magnetic resonance imaging study of the cerebellar vermis in chronically treated and treatment-naive children with attention-deficit/hyperactivity disorder combined type. Biol. Psychiatry 2009, 65:620-624.
12. Brand M., Kalbe E., Labudda K., Fujiwara E., Kessler J., Markowitsch H.J. Decision-making impairments in patients with pathological gambling. Psychiatry Res. 2005, 133:91-99.
13. Carmona S., Hoekzema E., Ramos-Quiroga J.A., Richarte V., Canals C., et al. Response inhibition and reward anticipation in medication-naive adults with attention-deficit/hyperactivity disorder: a within-subject case-control neuroimaging study. Hum. Brain Mapp 2011, 10.1002/hbm.21368.
14. Christiansen H., Kis B., Hirsch O., Philipsen A., Henneck M., et al. German validation of the Conners Adult ADHD Rating Scales-self-report (CAARS-S) I: factor structure and normative data. Eur. Psychiatry 2011, 26:100-107.
15. Christiansen H., Kis B., Hirsch O., Matthies S., Hebebrand J., et al. German validation of the Conners Adult ADHD Rating Scales (CAARS) II: reliability, validity, diagnostic sensitivity and specificity. Eur. Psychiatry 2011.
16. Conners C.K. Clinical use of rating scales in diagnosis and treatment of attention-deficit/hyperactivity disorder. Pediatr. Clin. North Am. 1999, 46:857-870. vi.
17. Conzelmann A., Mucha R.F., Jacob C.P., Weyers P., Romanos J., et al. Abnormal affective responsiveness in attention-deficit/hyperactivity disorder: subtype differences. Biol. Psychiatry 2009, 65:578-585.
18. Cross C.P., Copping L.T., Campbell A. Sex differences in impulsivity: a meta-analysis. Psychol. Bull. 2011, 137:97-130.
19. Cubillo A., Halari R., Smith A., Taylor E., Rubia K. A review of fronto-striatal and fronto-cortical brain abnormalities in children and adults with Attention Deficit Hyperactivity Disorder (ADHD) and new evidence for dysfunction in adults with ADHD during motivation and attention. Cortex 2011, 10.1016/j.cortex.2011.04.007.
20. de Zwaan M., Gruss B., Muller A., Graap H., Martin A., et al. The estimated prevalence and correlates of adult ADHD in a German community sample. Eur. Arch. Psychiatry Clin. Neurosci 2011, 10.1007/s00406-011-0211-9.
21. Delgado M.R., Nystrom L.E., Fissell C., Noll D.C., Fiez J.A. Tracking the hemodynamic responses to reward and punishment in the striatum. J. Neurophysiol. 2000, 84:3072-3077.
22. Delgado M.R., Stenger V.A., Fiez J.A. Motivation-dependent responses in the human caudate nucleus. Cereb. Cortex 2004, 14:1022-1030.
23. Dibbets P., Evers L., Hurks P., Marchetta N., Jolles J. Differences in feedback- and inhibition-related neural activity in adult ADHD. Brain Cogn. 2009, 70:73-83.
24. Diler R.S., Daviss W.B., Lopez A., Axelson D., Iyengar S., Birmaher B. Differentiating major depressive disorder in youths with attention deficit hyperactivity disorder. J. Affect. Disord. 2007, 102:125-130.
25. Douglas V.I., Parry P.A. Effects of reward and nonreward on frustration and attention in attention deficit disorder. J. Abnorm. Child Psychol. 1994, 22:281-302.
26. Eakin L., Minde K., Hechtman L., Ochs E., Krane E., et al. The marital and family functioning of adults with ADHD and their spouses. J. Atten. Disord. 2004, 8:1-10.
27. Ebert D., Krause J., Roth-Sackenheim C. ADHD in adulthood-guidelines based on expert consensus with DGPPN support. Nervenarzt 2003, 74:939-946.
28. Elkins I.J., McGue M., Iacono W.G. Prospective effects of attention-deficit/hyperactivity disorder, conduct disorder, and sex on adolescent substance use and abuse. Arch. Gen. Psychiatry 2007, 64:1145-1152.
29. Fahrenberg J., Myrtek M., Schumacher J., Brähler E. Fragebogen zur Lebenszufriedenheit (FLZ). Handanweisung 2000, Hogrefe, Göttingen.
30. Fang X., Massetti G.M., Ouyang L., Grosse S.D., Mercy J.A. Attention-deficit/hyperactivity disorder, conduct disorder, and young adult intimate partner violence. Arch. Gen. Psychiatry 2010, 67:1179-1186.
31. Faraone S.V., Biederman J. What is the prevalence of adult ADHD? Results of a population screen of 966 adults. J. Atten. Disord. 2005, 9:384-391.
32. Ferguson S.A., Boctor S.Y. Cocaine responsiveness or anhedonia in rats treated with methylphenidate during adolescence. Neurotoxicol. Teratol. 2010, 32:432-442.
33. First M.B., Pincus H.A. The DSM-IV text revision: rationale and potential impact on clinical practice. Psychiatr. Serv. 2002, 53:288-292.
34. Fischer M., Barkley R.A., Smallish L., Fletcher K. Hyperactive children as young adults: driving abilities, safe driving behavior, and adverse driving outcomes. Accid. Anal. Prev. 2007, 39:94-105.
35. Flory K., Molina B.S., Pelham W.E., Gnagy E., Smith B. Childhood ADHD predicts risky sexual behavior in young adulthood. J. Clin. Child Adolesc. Psychol. 2006, 35:571-577.
36. Frank M.J., Santamaria A., O'Reilly R.C., Willcutt E. Testing computational models of dopamine and noradrenaline dysfunction in attention deficit/hyperactivity disorder. Neuropsychopharmacology 2007, 32:1583-1599.
37. Groen Y., Wijers A.A., Mulder L.J., Waggeveld B., Minderaa R.B., Althaus M. Error and feedback processing in children with ADHD and children with Autistic Spectrum Disorder: an EEG event-related potential study. Clin. Neurophysiol. 2008, 119:2476-2493.
38. Haenlein M., Caul W.F. Attention deficit disorder with hyperactivity: a specific hypothesis of reward dysfunction. J. Am. Acad. Child Adolesc. Psychiatry 1987, 26:356-362.
39. Hariri A.R., Brown S.M., Williamson D.E., Flory J.D., de Wit H., Manuck S.B. Preference for immediate over delayed rewards is associated with magnitude of ventral striatal activity. J. Neurosci. 2006, 26:13213-13217.
40. Hautzinger M., Keller F., Kühner C. BDI-II; Beck Depressions-Inventar Revision 2006, Harcourt Test Services, Frankfurt am Main.
41. Herrmann M.J., Schreppel T., Biehl S.C., Jacob C., Heine M., et al. Emotional deficits in adult ADHD patients: an ERP study. Soc. Cogn. Affect. Neurosci. 2009, 4:340-345.
42. Holroyd C.B., Baker T.E., Kerns K.A., Muller U. Electrophysiological evidence of atypical motivation and reward processing in children with attention-deficit hyperactivity disorder. Neuropsychologia 2008, 46:2234-2242.
43. Hoogman M., Aarts E., Zwiers M., Slaats-Willemse D., Naber M., et al. Nitric oxide synthase genotype modulation of impulsivity and ventral striatal activity in adult ADHD patients and healthy comparison subjects. Am. J. Psychiatry 2011, 168:1099-1106.
44. Kahnt T., Heinzle J., Park S.Q., Haynes J.D. The neural code of reward anticipation in human orbitofrontal cortex. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:6010-6015.
45. Knutson B., Adams C.M., Fong G.W., Hommer D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J. Neurosci. 2001, 21:RC159.
46. Konrad A., Dielentheis T.F., El Masri D., Bayerl M., Fehr C., et al. Disturbed structural connectivity is related to inattention and impulsivity in adult attention deficit hyperactivity disorder. Eur. J. Neurosci. 2010, 31:912-919.
47. Kringelbach M.L., Rolls E.T. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog. Neurobiol. 2004, 72:341-372.
48. Kringelbach M.L., Jenkinson N., Green A.L., Owen S.L., Hansen P.C., et al. Deep brain stimulation for chronic pain investigated with magnetoencephalography. Neuroreport 2007, 18:223-228.
49. Lehrl S. Mehrfachwahl-Wortschatz-Intelligenztest MWT-B (5. Auflage, 2005) 1977, Spitta, Balingen.
50. Lodge D.J. The medial prefrontal and orbitofrontal cortices differentially regulate dopamine system function. Neuropsychopharmacology 2011, 36:1227-1236.
51. Luman M., Van Meel C.S., Oosterlaan J., Sergeant J.A., Geurts H.M. Does reward frequency or magnitude drive reinforcement-learning in attention-deficit/hyperactivity disorder?. Psychiatry Res. 2009, 168:222-229.
52. Luman M., Tripp G., Scheres A. Identifying the neurobiology of altered reinforcement sensitivity in ADHD: a review and research agenda. Neurosci. Biobehav. Rev. 2010, 34:744-754.
53. Mannuzza S., Klein R.G., Bessler A., Malloy P., Hynes M.E. Educational and occupational outcome of hyperactive boys grown up. J. Am. Acad. Child Adolesc. Psychiatry 1997, 36:1222-1227.
54. Mannuzza S., Klein R.G., Klein D.F., Bessler A., Shrout P. Accuracy of adult recall of childhood attention deficit hyperactivity disorder. Am. J. Psychiatry 2002, 159:1882-1888.
55. Mansour A., Khachaturian H., Lewis M.E., Akil H., Watson S.J. Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain. J. Neurosci. 1987, 7:2445-2464.
56. May J.C., Delgado M.R., Dahl R.E., Stenger V.A., Ryan N.D., et al. Event-related functional magnetic resonance imaging of reward-related brain circuitry in children and adolescents. Biol. Psychiatry 2004, 55:359-366.
57. Mena J.D., Sadeghian K., Baldo B.A. Induction of hyperphagia and carbohydrate intake by mu-opioid receptor stimulation in circumscribed regions of frontal cortex. J. Neurosci. 2011, 31:3249-3260.
58. Mitchell S.H. Measures of impulsivity in cigarette smokers and non-smokers. Psychopharmacology (Berl) 1999, 146:455-464.
59. Paloyelis Y., Asherson P., Mehta M.A., Faraone S.V., Kuntsi J. DAT1 and COMT effects on delay discounting and trait impulsivity in male adolescents with attention deficit/hyperactivity disorder and healthy controls. Neuropsychopharmacology 2010, 35:2414-2426.
60. Patton J.H., Stanford M.S., Barratt E.S. Factor structure of the Barratt impulsiveness scale. J. Clin. Psychol. 1995, 51:768-774.
61. Pecina S., Smith K.S., Berridge K.C. Hedonic hot spots in the brain. Neuroscientist 2006, 12:500-511.
62. Plichta M.M., Vasic N., Wolf R.C., Lesch K.P., Brummer D., et al. Neural hyporesponsiveness and hyperresponsiveness during immediate and delayed reward processing in adult attention-deficit/hyperactivity disorder. Biol. Psychiatry 2009, 65:7-14.
63. Prossin A.R., Love T.M., Koeppe R.A., Zubieta J.K., Silk K.R. Dysregulation of regional endogenous opioid function in borderline personality disorder. Am. J. Psychiatry 2010, 167:925-933.
64. Rachlin H., Raineri A., Cross D. Subjective probability and delay. J. Exp. Anal. Behav. 1991, 55:233-244.
65. Richards J.B., Zhang L., Mitchell S.H., de Wit H. Delay or probability discounting in a model of impulsive behavior: effect of alcohol. J. Exp. Anal. Behav. 1999, 71:121-143.
66. Robbins T.W., Everitt B.J. Drug addiction: bad habits add up. Nature 1999, 398:567-570.
67. Roesch M.R., Calu D.J., Burke K.A., Schoenbaum G. Should I stay or should I go? Transformation of time-discounted rewards in orbitofrontal cortex and associated brain circuits. Ann. N. Y. Acad. Sci. 2007, 1104:21-34.
68. Rubia K., Halari R., Christakou A., Taylor E. Impulsiveness as a timing disturbance: neurocognitive abnormalities in attention-deficit hyperactivity disorder during temporal processes and normalization with methylphenidate. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009, 364:1919-1931.
69. Rubia K., Halari R., Cubillo A., Mohammad A.M., Brammer M., Taylor E. Methylphenidate normalises activation and functional connectivity deficits in attention and motivation networks in medication-naive children with ADHD during a rewarded continuous performance task. Neuropharmacology 2009, 57:640-652.
70. Rubia K., Smith A.B., Halari R., Matsukura F., Mohammad M., et al. Disorder-specific dissociation of orbitofrontal dysfunction in boys with pure conduct disorder during reward and ventrolateral prefrontal dysfunction in boys with pure ADHD during sustained attention. Am. J. Psychiatry 2009, 166:83-94.
71. Sagvolden T., Johansen E.B., Aase H., Russell V.A. A dynamic developmental theory of attention-deficit/hyperactivity disorder (ADHD) predominantly hyperactive/impulsive and combined subtypes. Behav. Brain Sci. 2005, 28:397-419. discussion - 68.
72. Scheres A., Milham M.P., Knutson B., Castellanos F.X. Ventral striatal hyporesponsiveness during reward anticipation in attention-deficit/hyperactivity disorder. Biol. Psychiatry 2007, 61:720-724.
73. Sescousse G., Redoute J., Dreher J.C. The architecture of reward value coding in the human orbitofrontal cortex. J. Neurosci. 2010, 30:13095-13104.
74. Shaw P., Sharp W.S., Morrison M., Eckstrand K., Greenstein D.K., et al. Psychostimulant treatment and the developing cortex in attention deficit hyperactivity disorder. Am. J. Psychiatry 2009, 166:58-63.
75. Simon V., Czobor P., Balint S., Meszaros A., Bitter I. Prevalence and correlates of adult attention-deficit hyperactivity disorder: meta-analysis. Br. J. Psychiatry 2009, 194:204-211.
76. Solanto M.V., Abikoff H., Sonuga-Barke E., Schachar R., Logan G.D., et al. The ecological validity of delay aversion and response inhibition as measures of impulsivity in AD/HD: a supplement to the NIMH multimodal treatment study of AD/HD. J. Abnorm. Child Psychol. 2001, 29:215-228.
77. Sonuga-Barke E.J. Causal models of attention-deficit/hyperactivity disorder: from common simple deficits to multiple developmental pathways. Biol. Psychiatry 2005, 57:1231-1238.
78. Spielberger C.D., Gorusch R.L., Lushene R.E. Manual for the State-Trait Anxiety Inventory 1970, Consulting Psychologists Press, Palo Alto, CA.
79. Strohle A., Stoy M., Wrase J., Schwarzer S., Schlagenhauf F., et al. Reward anticipation and outcomes in adult males with attention-deficit/hyperactivity disorder. Neuroimage 2008, 39:966-972.
80. Tripp G., Wickens J.R. Research review: dopamine transfer deficit: a neurobiological theory of altered reinforcement mechanisms in ADHD. J. Child Psychol. Psychiatry 2008, 49:691-704.
81. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15:273-289.
82. Valera E.M., Brown A., Biederman J., Faraone S.V., Makris N., et al. Sex differences in the functional neuroanatomy of working memory in adults with ADHD. Am. J. Psychiatry 2010, 167:86-94.
83. van Meel C.S., Oosterlaan J., Heslenfeld D.J., Sergeant J.A. Telling good from bad news: ADHD differentially affects processing of positive and negative feedback during guessing. Neuropsychologia 2005, 43:1946-1954.
84. van Meel C.S., Heslenfeld D.J., Oosterlaan J., Luman M., Sergeant J.A. ERPs associated with monitoring and evaluation of monetary reward and punishment in children with ADHD. J. Child Psychol. Psychiatry 2011, 52:942-953.
85. Weafer J., Milich R., Fillmore M.T. Behavioral components of impulsivity predict alcohol consumption in adults with ADHD and healthy controls. Drug Alcohol Depend. 2011, 113:139-146.
86. Wender P.H. The minimal brain dysfunction syndrome in children. I. The syndrome and its relevance for psychiatry. II. A psychological and biochemical model for the syndrome. J. Nerv. Ment. Dis. 1972, 155:55-71.
87. Wender P.H., Wolf L.E., Wasserstein J. Adults with ADHD. An overview. Ann. N. Y. Acad. Sci. 2001, 931:1-16.
88. Winstanley C.A., Zeeb F.D., Bedard A., Fu K., Lai B., et al. Dopaminergic modulation of the orbitofrontal cortex affects attention, motivation and impulsive responding in rats performing the five-choice serial reaction time task. Behav. Brain Res. 2010, 210:263-272.
89. Zaitsev M., Hennig J., Speck O. Point spread function mapping with parallel imaging techniques and high acceleration factors: fast, robust, and flexible method for echo-planar imaging distortion correction. Magn. Reson. Med. 2004, 52:1156-1166.