Task-load-dependent activation of dopaminergic midbrain areas in the absence of reward

Journal of Neuroscience

Volumn 31, Issue 13, 2011, Pages 4955-4961

  Boehler, Carsten N ^a,b   Hopf, Jens Max ^c,d   Krebs, Ruth M ^a,b   Stoppel, Christian M ^c   Schoenfeld, Mircea A ^c,d   Heinze, Hans Jochen ^c,d   Noesselt, Toemme ^c  

^a GHENT UNIVERSITY   (Belgium)

^b DUKE UNIVERSITY   (United States)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

^d LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BRAIN ACTIVATION; BRAIN FUNCTION; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; HUMAN; HUMAN EXPERIMENT; MALE; MESENCEPHALON; MOTIVATION; NORMAL HUMAN; PREDICTION; PRIORITY JOURNAL; REWARD; SUBSTANTIA NIGRA; TASK PERFORMANCE; VISUAL DISCRIMINATION;

ADULT; DOPAMINE; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MESENCEPHALON; NERVE NET; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; REWARD; WEIGHT-BEARING; YOUNG ADULT;

EID: 79955708902     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4845-10.2011     Document Type: Article

References (63)

1. Adcock RA, Thangavel A, Whitfield-Gabrieli S, Knutson B, Gabrieli JD (2006) Reward-motivated learning: mesolimbic activation precedes memory formation. Neuron 50:507-517.
2. Ahsan RL, Allom R, Gousias IS, Habib H, Turkheimer FE, Free S, Lemieux L, Myers R, Duncan JS, Brooks DJ, Koepp MJ, Hammers A (2007) Volumes, spatial extents and a probabilistic atlas of the human basal ganglia and thalamus. Neuroimage 38:261-270.
3. Argyelan M, Carbon M, Ghilardi MF, Feigin A, Mattis P, Tang C, Dhawan V, Eidelberg D (2008) Dopaminergic suppression of brain deactivation responses during sequence learning. J Neurosci 28:10687-10695.
4. Arnsten AF, Cai JX, Steere JC, Goldman-Rakic PS (1995) Dopamine D2 receptor mechanisms contribute to age-related cognitive decline: the effects of quinpirole on memory and motor performance in monkeys. J Neurosci 15:3429-3439.
5. Arnsten AF, Vijayraghavan S, Wang M, Gamo NJ, Paspalas CD (2009) Dopamine's influence on prefrontal cortical cognition: actions and circuits in behaving primates. In: Dopamine handbook (Iversen L, Iversen S, Dunnett S, Bjorklund A, eds), pp 230-248. New York: Oxford UP.
6. Berridge KC (2007) The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berl) 191:391-431.
7. Bjork JM, Hommer DW (2007) Anticipating instrumentally obtained and passively-received rewards: a factorial fMRI investigation. Behav Brain Res 177:165-170.
8. Björklund A, Dunnett SB (2007) Dopamine neuron systems in the brain: an update. Trends Neurosci 30:194-202.
9. Braver TS, Cohen JD (2000) On the control of control: the role of dopamine in regulating prefrontal function and working memory. In: Attention and performance XVIII (Monsell S, Driver J, eds), pp 713-738. Cambridge, MA: MIT.
10. Braver TS, Gray JR, Burgess GC (2007) Explaining the many varieties of working memory variation: dual mechanisms of cognitive control. In: Variation in working memory (Conway AR, Jarrold C, Kane MJ, Miyake A, Towse JN, eds), pp 76-106. Oxford Oxford Univerity.
11. Brown RG, Marsden CD (1988) Internal versus external cues and the control of attention in Parkinson's disease. Brain 111:323-345.
12. Bullmore E, Suckling J, Zelaya F, Long C, Honey G, Reed L, Routledge C, Ng V, Fletcher P, Brown J, Williams SC (2003) Practice and difficulty evoke anatomically and pharmacologically dissociable brain activation dynamics. Cereb Cortex 13:144-154.
13. Bunzeck N, Düzel E (2006) Absolute coding of stimulus novelty in the human substantia nigra/VTA. Neuron 51:369-379.
14. Cabestrero R, Crespo A, Quirós P (2009) Pupillary dilation as an index of task demands. Percept Mot Skills 109:664-678.
15. Cho SS, Strafella AP (2009) rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex. PLoS One 4:e6725.
16. Clark CR, Geffen GM, Geffen LB (1987) Catecholamines and attention. II. Pharmacological studies in normal humans. Neurosci Biobehav Rev 11:353-364.
17. Cools R (2006) Dopaminergic modulation of cognitive function-implications for L-DOPA treatment in Parkinson's disease. Neurosci Biobehav Rev 30:1-23.
18. Croxson PL, Walton ME, O'Reilly JX, Behrens TE, Rushworth MF (2009) Effort-based cost-benefit valuation and the human brain. J Neurosci 29:4531-4541.
19. Czernecki V, Pillon B, Houeto JL, Pochon JB, Levy R, Dubois B (2002) Motivation, reward, and Parkinson's disease: influence of dopatherapy. Neuropsychologia 40:2257-2267.
20. Dale AM (1999) Optimal experimental design for event-related fMRI. Hum Brain Mapp 8:109-114.
21. D'Ardenne K, McClure SM, Nystrom LE, Cohen JD (2008) BOLD responses reflecting dopaminergic signals in the human ventral tegmental area. Science 319:1264-1267.
22. Dommett E, Coizet V, Blaha CD, Martindale J, Lefebvre V, Walton N, Mayhew JE, Overton PG, Redgrave P (2005) How visual stimuli activate dopaminergic neurons at short latency. Science 307:1476-1479.
23. Dosenbach NU, Visscher KM, Palmer ED, Miezin FM, Wenger KK, Kang HC, Burgund ED, Grimes AL, Schlaggar BL, Petersen SE (2006) A core system for the implementation of task sets. Neuron 50:799-812.
24. Duncan J, Owen AM (2000) Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci 23:475-483.
25. Düzel E, Bunzeck N, Guitart-Masip M, Wittmann B, Schott BH, Tobler PN (2009) Functional imaging of the human dopaminergic midbrain. Trends Neurosci 32:321-328.
26. Engelmann JB, Damaraju E, Padmala S, Pessoa L (2009) Combined effects of attention and motivation on visual task performance: transient and sustained motivational effects. Front Hum Neurosci 3:4.
27. Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481-1489.
28. Fernández-Ruiz JJ, Hernández ML, de Miguel R, Ramos JA (1991) Nigrostriatal and mesolimbic dopaminergic activities were modified throughout the ovarian cycle of female rats. J Neural Transm Gen Sect 85:223-229.
29. Frank MJ, O'Reilly RC (2006) A mechanistic account of striatal dopamine function in human cognition: psychopharmacological studies with cabergoline and haloperidol. Behav Neurosci 120:497-517.
30. Greicius MD, Krasnow B, Reiss AL, Menon V (2003) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci U S A 100:253-258.
31. Haber SN, Knutson B (2010) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35:4-26.
32. Hinrichs H, Scholz M, Tempelmann C, Woldorff MG, Dale AM, Heinze HJ (2000) Deconvolution of event-related fMRI responses in fast-rate experimental designs: tracking amplitude variations. J Cogn Neurosci 12[Suppl 2]:76-89.
33. Horvitz JC (2000) Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 96:651-656.
34. Kanowski M, Rieger JW, Noesselt T, Tempelmann C, Hinrichs H (2007) Endoscopic eye tracking system for fMRI. J Neurosci Methods 160:10-15.
35. Knutson B, Adams CM, Fong GW, Hommer D (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 21:RC159.
36. Knutson B, Taylor J, Kaufman M, Peterson R, Glover G (2005) Distributed neural representation of expected value. J Neurosci 25:4806-4812.
37. Liu TT (2004) Efficiency, power, and entropy in event-related fMRI with multiple trial types, part II: design of experiments. Neuroimage 21:401-413.
38. Maunsell JH (2004) Neuronal representations of cognitive state: reward or attention? Trends Cogn Sci 8:261-265.
39. McGuire JT, Botvinick MM (2010) Prefrontal cortex, cognitive control, and the registration of decision costs. Proc Natl Acad Sci U S A 107: 7922-7926.
40. Mohanty A, Gitelman DR, Small DM, Mesulam MM (2008) The spatial attention network interacts with limbic and monoaminergic systems to modulate motivation-induced attention shifts. Cereb Cortex 18: 2604-2613.
41. Moore H, West AR, Grace AA (1999) The regulation of forebrain dopamine transmission: relevance to the pathophysiology and psychopathology of schizophrenia. Biol Psychiatry 46:40-55.
42. Nieoullon A (2002) Dopamine and the regulation of cognition and attention. Prog Neurobiol 67:53-83.
43. Pessiglione M, Seymour B, Flandin G, Dolan RJ, Frith CD (2006) Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442:1042-1045.
44. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci U S A 98:676-682.
45. Redgrave P, Prescott TJ, Gurney K (1999) Is the short-latency dopamine response too short to signal reward error? Trends Neurosci 22:146-151.
46. Robbins TW (2005) Chemistry of the mind: neurochemical modulation of prefrontal cortical function. J Comp Neurol 493:140-146.
47. Robbins TW, Arnsten AF (2009) The neuropsychopharmacology of frontoexecutive function: monoaminergic modulation. Annu Rev Neurosci 32:267-287.
48. Robbins TW, Everitt BJ (2007) A role for mesencephalic dopamine in activation: commentary on Berridge (2006). Psychopharmacology (Berl) 191:433-437.
49. Salamone JD (2009) Dopamine, effort, and decision making: theoretical comment on Bardgett et al. (2009). Behav Neurosci 123:463-467.
50. Salamone JD, Correa M, Mingote SM, Weber SM (2005) Beyond the reward hypothesis: alternative functions of nucleus accumbens dopamine. Curr Opin Pharmacol 5:34-41.
51. Schoenbaum G, Roesch MR, Stalnaker TA, Takahashi YK (2009) A new perspective on the role of the orbitofrontal cortex in adaptive behaviour. Nat Rev Neurosci 10:885-892.
52. Schott BH, Minuzzi L, Krebs RM, Elmenhorst D, Lang M, Winz OH, Seidenbecher CI, Coenen HH, Heinze HJ, Zilles K, Düzel E, Bauer A (2008) Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release. J Neurosci 28:14311-14319.
53. Schultz W (2007) Multiple dopamine functions at different time courses. Annu Rev Neurosci 30:259-288.
54. Seamans JK, Yang CR (2004) The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74:1-58.
55. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349-2356.
56. Servan-Schreiber D, Printz H, Cohen JD (1990) A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior. Science 249:892-895.
57. Servan-Schreiber D, Carter CS, Bruno RM, Cohen JD (1998) Dopamine and the mechanisms of cognition, part II: D-amphetamine effects in human subjects performing a selective attention task. Biol Psychiatry 43:723-729.
58. Tomasi D, Volkow ND, Wang R, Telang F, Wang GJ, Chang L, Ernst T, Fowler JS (2009) Dopamine transporters in striatum correlate with deactivation in the default mode network during visuospatial attention. PLoS One 4:e6102.
59. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483-494.
60. Wittmann BC, Schott BH, Guderian S, Frey JU, Heinze HJ, Düzel E (2005) Reward-related FMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation. Neuron 45:459-467.
61. Yamaguchi S, Kobayashi S (1998) Contributions of the dopaminergic system to voluntary and automatic orienting of visuospatial attention. J Neurosci 18:1869-1878.
62. Zink CF, Pagnoni G, Martin ME, Dhamala M, Berns GS (2003) Human striatal response to salient non rewarding stimuli. J Neurosci 23:8092-8097.
63. Zink CF, Pagnoni G, Martin-Skurski ME, Chappelow JC, Berns GS (2004) Human striatal responses to monetary reward depend on saliency. Neuron 42:509-517.