Dorsolateral prefrontal cortex drives mesolimbic dopaminergic regions to initiate motivated behavior

Journal of Neuroscience

Volumn 31, Issue 28, 2011, Pages 10340-10346

  Ballard, Ian C ^a   Murty, Vishnu P ^a,b   McKell Carter, R ^a,b   Macinnes, Jeffrey J ^a   Huettel, Scott A ^a   Alison Adcock, R ^a,b  

^a DUKE UNIVERSITY   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICIPATION; ARTICLE; ASSOCIATION; BEHAVIOR; CEREBELLUM; CORPUS STRIATUM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; INSULA; MESENCEPHALON; MESOLIMBIC DOPAMINERGIC SYSTEM; MOTIVATION; NUCLEUS ACCUMBENS; POSTERIOR PARIETAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; REACTION TIME; REWARD; VENTRAL TEGMENTUM;

ADULT; BRAIN MAPPING; DOPAMINE; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MOTIVATION; NEURAL PATHWAYS; NEURONS; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; REWARD; VENTRAL TEGMENTAL AREA;

EID: 79960401659     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0895-11.2011     Document Type: Article

References (70)

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. Alcaro A, Huber R, Panksepp J (2007) Behavioral functions of the mesolimbic dopaminergic system: an affective neuroethological perspective. Brain Res Rev 56:283-321.
3. Amiaz R, Levy D, Vainiger D, Grunhaus L, Zangen A (2009) Repeated highfrequency transcranial magnetic stimulation over the dorsolateral prefrontal cortex reduces cigarette craving and consumption. Addiction 104:653-660.
4. Bakshi VP, Kelley AE (1991) Dopaminergic regulation of feeding behavior. 1. Differential effects of haloperidol microinfusion into 3 striatal subregions. Psychobiology 19:223-232.
5. Beckstead RM, Domesick VB, Nauta WJ (1979) Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res 175:191-217.
6. Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28:309-369.
7. Boettiger CA, Mitchell JM, Tavares VC, Robertson M, Joslyn G, D'Esposito M, Fields HL (2007) Immediate reward bias in humans: fronto-parietal networks and a role for the catechol-O-methyltransferase 158 Val/Val genotype. J Neurosci 27:14383-14391.
8. Breiter HC, Gollub RL, Weisskoff RM, Kennedy DN, Makris N, Berke JD, Goodman JM, Kantor HL, Gastfriend DR, Riorden JP, Mathew RT, Rosen BR, Hyman SE (1997) Acute effects of cocaine on human brain activity and emotion. Neuron 19:591-611.
9. Bromberg-Martin ES, Matsumoto M, Hikosaka O (2010) Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68:815-834.
10. Camus M, Halelamien N, Plassmann H, Shimojo S, O'Doherty J, Camerer C, Rangel A (2009) Repetitive transcranial magnetic stimulation over the right dorsolateral prefrontal cortex decreases valuations during food choices. Eur J Neurosci 30:1980-1988.
11. Carter RM, Macinnes JJ, Huettel SA, Adcock RA (2009) Activation in the VTA and nucleus accumbens increases in anticipation of both gains and losses. Front Behav Neurosci 3:21.
12. Crone EA, Wendelken C, Donohue SE, Bunge SA (2006) Neural evidence for dissociable components of task-switching. Cereb Cortex 16:475-486.
13. Doll BB, Jacobs WJ, Sanfey AG, Frank MJ (2009) Instructional control of reinforcement learning: a behavioral and neurocomputational investigation. Brain Res 1299:74-94.
14. Dove A, Pollmann S, Schubert T, Wiggins CJ, von Cramon DY (2000) Prefrontal cortex activation in task switching: an event-related fMRI study. Brain Res Cogn Brain Res 9:103-109.
15. Durstewitz D, Seamans JK, Sejnowski TJ (2000) Neurocomputational models of working memory. Nat Neurosci 3 [Suppl]:1184-1191.
16. Fields HL, Hjelmstad GO, Margolis EB, Nicola SM (2007) Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu Rev Neurosci 30:289-316.
17. Fiorillo CD, Tobler PN, Schultz W (2003) Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299:1898-1902.
18. Frankle WG, Laruelle M, Haber SN (2006) Prefrontal cortical projections to the midbrain in primates: evidence for a sparse connection. Neuropsychopharmacology 31:1627-1636.
19. Friston KJ, Mechelli A, Turner R, Price CJ (2000) Nonlinear responses in fMRI: the Balloon model, Volterra kernels, and other hemodynamics. Neuroimage 12:466-477.
20. Friston KJ, Harrison L, Penny W (2003) Dynamic causal modelling. Neuroimage 19:1273-1302.
21. Gao M, Liu CL, Yang S, Jin GZ, Bunney BS, Shi WX (2007) Functional coupling between the prefrontal cortex and dopamine neurons in the ventral tegmental area. J Neurosci 27:5414-5421.
22. Gao WJ, Goldman-Rakic PS (2003) Selective modulation of excitatory and inhibitory microcircuits by dopamine. Proc Natl Acad Sci U S A 100:2836-2841.
23. Gariano RF, Groves PM (1988) Burst firing induced in midbrain dopamine neurons by stimulation of the medial prefrontal and anterior cingulated cortices. Brain Res 462:194-198.
24. Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870-878.
25. Goldman-Rakic PS (1998) The cortical dopamine system: role in memory and cognition. Adv Pharmacol 42:707-711.
26. Goto Y, Grace AA (2005) Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat Neurosci 8:805-812.
27. Grace AA, Floresco SB, Goto Y, Lodge DJ (2007) Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci 30:220-227.
28. Haber SN, Knutson B (2010) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35:4-26.
29. Hare TA, Camerer CF, Rangel A (2009) Self-control in decision-making involves modulation of the vmPFC valuation system. Science 324:646-648.
30. Hazy TE, Frank MJ, O'Reilly RC (2006) Banishing the homunculus: making working memory work. Neuroscience 139:105-118.
31. Ikemoto S, Panksepp J (1999) The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev 31:6-41.
32. Kimberg DY, Aguirre GK, D'Esposito M (2000) Modulation task-related neural activity in task-switching: an fMRI study. Brain Res Cogn Brain Res 10:189-196.
33. Knutson B, Adams CM, Fong GW, Hommer D (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 21: RC159(1-5).
34. Ko JH, Monchi O, Ptito A, Bloomfield P, Houle S, Stafella AP (2008) Theta burst stimulation-induced inhibition of dorsolateral prefrontal cortex reveals hemispheric asymmetry in striatal dopamine release during set shifting task: a TMS- [(11)C]raclopride PET study. Eur J Neurosci 28:2147-2155.
35. Levy R, Goldman-Rakic PS (2000) Segregation of working memory functions within the dorsolateral prefrontal cortex. Exp Brain Res 133:23-32.
36. Li J, Delgado MR, Phelps EA (2011) How instructed knowledge modulates the neural systems of reward learning. Proc Natl Acad Sci USA 108:55-60.
37. Ljungberg T, Apicella P, Schultz W (1992) Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 67:145-163.
38. MacDonald AW 3rd, Cohen JD, Stenger VA, Carter CS (2000) Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 288:1835-1838.
39. McClure SM, Laibson DI, Loewenstein G, Cohen JD (2004) Separate neural systems value immediate and delayed monetary rewards. Science 306: 503-507.
40. McClure SM, Ericson KM, Laibson DI, Loewenstein G, Cohen JD (2007) Time discounting for primary rewards. J Neurosci 27:5796-5804.
41. Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167-202.
42. Owen AM, McMillan KM, Laird AR, Bullmore E (2005) N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp 25:46-59.
43. Parkinson JA, Dalley JW, Cardinal RN, Bamford A, Fehnert B, Lachenal G, Rudarakanchana N, Halkerston KM, Robbins TW, Everitt BJ (2002) Nucleus accumbens dopamine depletion impairs both acquisition and performance of appetitive pavlovian approach behaviour: implications for mesoaccumbens dopamine function. Behav Brain Res 137:149-163.
44. Paspalas CD, Goldman-Rakic PS (2004) Microdomains for dopamine volume neurotransmission in primate prefrontal cortex. J Neurosci 24:5292-5300.
45. Penny WD, Stephan KE, Daunizeau J, Rosa MJ, Friston KJ, Schofield TM, Leff AP (2010) Comparing families of dynamic causal models. PLoS Comput Biol 6:e1000709.
46. Pogarell O, Koch W, Popperl G, Tatsch K, Jakob F, Zwanzger P, Mulert C, Rupprecht R, Moller HJ, Hegerl U, Padberg F (2006) Striatal dopamine release after prefrontal repetitive transcranial magnetic stimulation in major depression: preliminary results of a dynamic [123I] IBZM SPECT study. J Psychiatr Res 40:307-314.
47. Ridderinkhof KR, van den Wildenberg WP, Segalowitz SJ, Carter CS (2004) Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain Cogn 56:129-140.
48. Roitman MF, Wheeler RA, Wightman RM, Carelli RM (2008) Real-time chemical responses in the nucleus accumbens differentiate rewarding and aversive stimuli. Nat Neurosci 11:1376-1377.
49. Rushworth MF, Passingham RE, Nobre AC (2002) Components of switching intentional set. J Cogn Neurosci 14:1139-1150.
50. Sakai K (2008) Task set and prefrontal cortex. Annu Rev Neurosci 31: 219-245.
51. Salamone JD, Correa M, Farrar A, Mingote SM (2007) Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology (Berl) 191:461-482.
52. Savine AC, Beck SM, Edwards BG, Chiew KS, Braver TS (2010) Enhancement of cognitive control by approach and avoidance motivational states. Cogn Emot 24:338-356.
53. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1-27.
54. Seamans JK, Yang CR (2004) The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74:1-58.
55. Sesack SR, Carr DB (2002) Selective prefrontal cortex inputs to dopamine cells: implications for schizophrenia. Physiol Behav 77:513-517.
56. Sesack SR, Pickel VM (1992) Prefrontal cortical differents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J Comp Neurol 320:145-160.
57. Smith SM (2002) Fast robust automated brain extraction. HumBrain Mapp 17:143-155.
58. Staudinger MR, Erk S, Abler B, Walter H (2009) Cognitive reappraisal modulates expected value and prediction error encoding in the ventral striatum. Neuroimage 47:713-721.
59. Stephan KE, Weiskopf N, Drysdale PM, Robinson PA, Friston KJ (2007) Comparing hemodynamic models with DCM. Neuroimage 38:387-401.
60. Stephan KE, Penny WD, Daunizeau J, Moran RJ, Friston KJ (2009) Bayesian model selection for group studies. Neuroimage 46:1004-1017.
61. Stephan KE, Penny WD, Moran RJ, den Ouden HE, Daunizeau J, Friston KJ (2010) Ten simple rules for dynamic causal modeling. Neuroimage 49: 3099-3109.
62. Svensson TH, Tung CS (1989) Local cooling of pre-frontal cortex induces pacemaker-like firing of dopamine neurons in rat ventral tegmental area in vivo. Acta Physiol Scand 136:135-136.
63. Wager TD, Smith EE (2003) Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci 3:255-274.
64. Wagner AD, Maril A, Bjork RA, Schacter DL (2001) Prefrontal contributions to executive control: fMRI evidence for functional distinctions within lateral prefrontal cortex. Neuroimage 14:1337-1347.
65. Wallis JD, Miller EK (2003) Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur J Neurosci 18:2069-2081.
66. Wang M, Vijayraghavan S, Goldman-Rakic PS (2004) SelectiveD2 receptor actions on the functional circuitry of working memory. Science 303:853-856.
67. Watanabe M, Sakagami M (2007) Integration of cognitive and motivational context information in the primate prefrontal cortex. Cereb Cortex 17:i101-i109.
68. Williams GV, Goldman-Rakic PS (1995) Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature 376:572-575.
69. Williams SM, Goldman-Rakic PS (1998) Widespread origin of the primate mesofrontal dopamine system. Cereb Cortex 8:321-345.
70. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483-494.