Multifaceted contributions by different regions of the orbitofrontal and medial prefrontal cortex to probabilistic reversal learning

Journal of Neuroscience

Volumn 36, Issue 6, 2016, Pages 1996-2006

  Dalton, Gemma L ^a   Wang, Nena Y ^a   Phillips, Anthony G ^a   Floresco, Stan B ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Orbitofrontal cortex; Prelimbic cortex; Probabilistic; Reversal learning

Indexed keywords

BACLOFEN; MUSCIMOL; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; CONTROLLED STUDY; EXPERIMENTAL BEHAVIORAL TEST; INFRALIMBIC CORTEX; LATENT PERIOD; LEARNING; MALE; MEDIAL PREFRONTAL CORTEX; NEGATIVE FEEDBACK; NEUROPHYSIOLOGY; NONHUMAN; ORBITAL CORTEX; POSITIVE FEEDBACK; PRIORITY JOURNAL; RAT; REINFORCEMENT; ADAPTIVE BEHAVIOR; ANIMAL; DISCRIMINATION LEARNING; DRUG EFFECTS; FRONTAL LOBE; INSTRUMENTAL CONDITIONING; LIMBIC SYSTEM; LONG EVANS RAT; PHYSIOLOGY; PREFRONTAL CORTEX; PSYCHOMOTOR PERFORMANCE; REWARD; UNCERTAINTY;

ANIMALS; BACLOFEN; CONDITIONING, OPERANT; DISCRIMINATION LEARNING; FEEDBACK, PSYCHOLOGICAL; FRONTAL LOBE; GABA AGONISTS; LIMBIC SYSTEM; MALE; MUSCIMOL; PREFRONTAL CORTEX; PSYCHOMOTOR PERFORMANCE; RATS; RATS, LONG-EVANS; REVERSAL LEARNING; REWARD; UNCERTAINTY;

EID: 84958819035     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3366-15.2016     Document Type: Article

References (60)

1. Bari A, Theobald DE, Caprioli D, Mar AC, Aidoo-Micah A, Dalley JW, Robbins TW (2010) Serotonin modulates sensitivity to reward and negative feedback in a probabilistic reversal learning task in rats. Neuropsychopharmacology 35:1290-1301. CrossRef Medline
2. Berlin HA, Rolls ET, Kischka U (2004) Impulsivity, time perception, emotion and reinforcement sensitivity in patients with orbitofrontal cortex lesions. Brain 127:1108-1126. CrossRef Medline
3. Birrell JM, Brown VJ (2000) Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20:4320-4324. Medline
4. Boulougouris V, Robbins TW (2009) Pre-surgical training ameliorates orbitofrontal-mediated impairments in spatial reversal learning. Behav Brain Res 197:469-475. CrossRef Medline
5. Boulougouris V, Dalley JW, Robbins TW (2007) Effects of orbitofrontal, infralimbic and prelimbic cortical lesions on serial spatial reversal learning in the rat. Behav Brain Res 179:219-228. CrossRef Medline
6. Chase HW, Clark L, Sahakian BJ, Bullmore ET, Robbins TW (2008) Dissociable roles of prefrontal subregions in self-ordered working memory performance. Neuropsychologia 46:2650-2661. CrossRef Medline
7. Chau BK, Sallet J, Papageorgiou GK, Noonan MP, Bell AH, Walton ME, Rushworth MF (2015) Contrasting roles for orbitofrontal cortex and amygdala in credit assignment and learning in macaques. Neuron 87: 1106-1118. CrossRef Medline
8. Cools R, Clark L, Owen AM, Robbins TW (2002) Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging. J Neurosci 22:4563-4567. Medline
9. Dalton GL, Phillips AG, Floresco SB (2014) Preferential involvement by nucleus accumbens shell in mediating probabilistic learning and reversal shifts. J Neurosci 34:4618-4626. CrossRef Medline
10. Dias R, Robbins TW, Roberts AC (1996) Primate analogue of the Wisconsin card sorting test: effects of excitotoxic lesions of the prefrontal cortex in the marmoset. Behav Neurosci 110:872-886. CrossRef Medline
11. Durstewitz D, Vittoz NM, Floresco SB, Seamans JK (2010) Abrupt transitions between prefrontal neural ensemble states accompany behavioral transitions during rule learning. Neuron 66:438-448. CrossRef Medline
12. Elliott R, Dolan RJ, Frith CD (2000) Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. Cereb Cortex 10:308-317. CrossRef Medline
13. Fellows LK, Farah MJ (2003) Ventromedial frontal cortex mediates affective shifting in humans: evidence from a reversal learning paradigm. Brain 126:1830-1837. CrossRef Medline
14. Flagel SB, Clark JJ, Robinson TE, Mayo L, Czuj A, Willuhn I, Akers CA, Clinton SM, Phillips PE, Akil H (2011) A selective role for dopamine in stimulus-reward learning. Nature 469:53-57. CrossRef Medline
15. Floresco SB, Block AE, Tse MT (2008) Inactivation of the medial prefrontal cortex of the rat impairs strategy set-shifting, but not reversal learning, using a novel, automated procedure. Behav Brain Res 190:85-96. CrossRef Medline
16. Ghods-Sharifi S, Haluk DM, Floresco SB (2008) Differential effects of inactivation of the orbitofrontal cortex on strategy set-shifting and reversal learning. Neurobiol Learn Mem 89:567-573. CrossRef Medline
17. Gläscher J, Hampton AN, O’Doherty JP (2009) Determining a role for ventromedial prefrontal cortex in encoding action-based value signals during reward-related decision making. Cereb Cortex 19:483-495. CrossRef Medline
18. Gläscher J, Adolphs R, Damasio H, Bechara A, Rudrauf D, Calamia M, Paul LK, Tranel D (2012) Lesion mapping of cognitive control and valuebased decision making in the prefrontal cortex. Proc Natl Acad Sci U S A 109:14681-14686. CrossRef Medline
19. Gourley SL, Lee AS, Howell JL, Pittenger C, Taylor JR (2010) Dissociable regulation of instrumental action within mouse prefrontal cortex. Eur J Neurosci 32:1726-1734. CrossRef Medline
20. Hoover WB, Vertes RP (2007) Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 212:149-179. CrossRef Medline
21. Hoover WB, Vertes RP (2011) Projections of the medial orbital and ventral orbital cortex in the rat. J Comp Neurol 519:3766-3801. CrossRef Medline
22. Hornak J, O’Doherty J, Bramham J, Rolls ET, Morris RG, Bullock PR, Polkey CE (2004) Reward-related reversal learning after surgical excisions in orbito-frontal or dorsolateral prefrontal cortex in humans. J Cogn Neurosci 16:463-478. CrossRef Medline
23. Jo YS, Mizumori SJ (2015) Prefrontal regulation of neuronal activity in the ventral tegmental area. Cereb Cortex. Advance online publication. Retrieved September 22, 2015. CrossRef Medline
24. Kable JW, Glimcher PW (2009) The neurobiology of decision: consensus and controversy. Neuron 63:733-745. CrossRef Medline
25. Levens SM, Larsen JT, Bruss J, Tranel D, Bechara A, Mellers BA (2014) What might have been? The role of the ventromedial prefrontal cortex and lateral orbitofrontal cortex in counterfactual emotions and choice. Neuropsychologia 54:77-86. CrossRef Medline
26. Mainen ZF, Kepecs A (2009) Neural representation of behavioral outcomes in the orbitofrontal cortex. Curr Opin Neurobiol 19:84-91. CrossRef Medline
27. McAlonan K, Brown VJ (2003) Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behav Brain Res 146: 97-103. CrossRef Medline
28. Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167-202. CrossRef Medline
29. Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD (2000) The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: a latent variable analysis. Cogn Psychol 41:49-100. CrossRef Medline
30. Noonan MP, Kolling N, Walton ME, Rushworth MF (2012) Re-evaluating the role of the orbitofrontal cortex in reward and reinforcement. Eur J Neurosci 35:997-1010. CrossRef Medline
31. O’Doherty J, Kringelbach ML, Rolls ET, Hornak J, Andrews C (2001) Abstract reward and punishment representations in the human orbitofrontal cortex. Nat Neurosci 4:95-102. CrossRef Medline
32. O’Doherty J, Critchley H, Deichmann R, Dolan RJ (2003) Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices. J Neurosci 23:7931-7939. Medline
33. Ongür D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10:206-219. CrossRef Medline
34. Orsini CA, Moorman DE, Young JW, Setlow B, Floresco SB (2015) Neural mechanisms regulating different forms of risk-related decision-making: insights from animal models. Neurosci Biobehav Rev 58:147-167. CrossRef Medline
35. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates, Ed 5. San Diego: Elsevier Academic. PreussTM (1995) Do rats have prefrontal cortex? The Rose-Woolsey-Akert program reconsidered. J Cogn Neurosci 7:1-24. CrossRef Medline
36. Ragozzino ME, Wilcox C, Raso M, Kesner RP (1999) Involvement of rodent prefrontal cortex subregions in strategy switching. Behav Neurosci 113: 32-41. CrossRef Medline
37. Remijnse PL, Nielen MM, Uylings HB, Veltman DJ (2005) Neural correlates of a reversal learning task with an affectively neutral baseline: an eventrelated f MRI study. Neuroimage 26:609-618. CrossRef Medline
38. Rogers RD, Owen AM, Middleton HC, Williams EJ, Pickard JD, Sahakian BJ, Robbins TW (1999) Choosing between small, likely rewards and large, unlikely rewards activates inferior and orbital prefrontal cortex. J Neurosci 19:9029-9038. Medline
39. Roiser JP, Cannon DM, Gandhi SK, Taylor Tavares J, Erickson K, Wood S, Klaver JM, Clark L, Zarate CA Jr, Sahakian BJ, Drevets WC (2009) Hot and cold cognition in unmedicated depressed subjects with bipolar disorder. Bipolar Disord 11:178-189. CrossRef Medline
40. Rudebeck PH, Murray EA (2008) Amygdala and orbitofrontal cortex lesions differentially influence choices during object reversal learning. J Neurosci 28:8338-8343. CrossRef Medline
41. Rushworth MF, Buckley MJ, Behrens TE, Walton ME, Bannerman DM (2007) Functional organization of the medial frontal cortex. Curr Opin Neurobiol 17:220-227. CrossRef Medline
42. Schilman EA, Uylings HB, Galis-de Graaf Y, Joel D, Groenewegen HJ (2008) The orbital cortex in rats topographically projects to central parts of the caudate-putamen complex. Neurosci Lett 432:40-45. CrossRef Medline
43. Schoenbaum G, Nugent SL, Saddoris MP, Setlow B (2002) Orbitofrontal lesions in rats impair reversal but not acquisition of go, no-go odor discriminations. Neuroreport 13:885-890. CrossRef Medline
44. Sesack SR, Deutch AY, Roth RH, Bunney BS (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290:213-242. CrossRef Medline
45. Stalnaker TA, Cooch NK, Schoenbaum G (2015) What the orbitofrontal cortex does not do. Nat Neurosci 18:620-627. CrossRef Medline
46. St Onge JR, Floresco SB (2010) Prefrontal cortical contribution to riskbased decision making. Cereb Cortex 20:1816-1828. CrossRef Medline
47. St Onge JR, Stopper CM, Zahm DS, Floresco SB (2012) Separate prefrontalsubcortical circuits mediate different components of risk-based decision making. J Neurosci 32:2886-2899. CrossRef Medline
48. Stopper CM, Green EB, Floresco SB (2014) Selective involvement by the medial orbitofrontal cortex in biasing risky, but not impulsive, choice. Cereb Cortex 24:154-162. CrossRef Medline
49. Sul JH, Kim H, Huh N, Lee D, Jung MW (2010) Distinct roles of rodent orbitofrontal and medial prefrontal cortex in decision making. Neuron 66:449-460. CrossRef Medline
50. Taylor Tavares JV, Clark L, Furey ML, Williams GB, Sahakian BJ, Drevets WC (2008) Neural basis of abnormal response to negative feedback in unmedicated mood disorders. Neuroimage 42:1118-1126. CrossRef Medline
51. Tsuchida A, Doll BB, Fellows LK (2010) Beyond reversal: a critical role for human orbitofrontal cortex in flexible learning from probabilistic feedback. J Neurosci 30:16868-16875. CrossRef Medline
52. Uylings HB, Groenewegen HJ, Kolb B (2003) Do rats have a prefrontal cortex? Behav Brain Res 146:3-17. CrossRef Medline
53. van Duuren E, van der Plasse G, van der Blom R, Joosten RN, Mulder AB, Pennartz CM, Feenstra MG (2007) Pharmacological manipulation of neuronal ensemble activity by reverse microdialysis in freely moving rats: a comparative study of the effects of tetrodotoxin, lidocaine, and muscimol. J Pharmacol Exp Ther 323:61-69. CrossRef Medline
54. van Duuren E, van der Plasse G, Lankelma J, Joosten RN, Feenstra MG, Pennartz CM (2009) Single-cell and population coding of expected reward probability in the orbitofrontal cortex of the rat. J Neurosci 29: 8965-8976. CrossRef Medline
55. Walton ME, Behrens TE, Buckley MJ, Rudebeck PH, Rushworth MF (2010) Separable learning systems in the macaque brain and the role of orbitofrontal cortex in contingent learning. Neuron 65:927-939. CrossRef Medline
56. Waltz JA, Gold JM (2007) Probabilistic reversal learning impairments in schizophrenia: further evidence of orbitofrontal dysfunction. Schizophr Res 93:296-303. CrossRef Medline
57. Whitton AE, Treadway MT, Pizzagalli DA (2015) Reward processing dysfunction in major depression, bipolar disorder and schizophrenia. Curr Opin Psychiatry 28:7-12. CrossRef Medline
58. Williams ZM, Bush G, Rauch SL, Cosgrove GR, Eskandar EN (2004) Human anterior cingulate neurons and the integration of monetary reward with motor responses. Nat Neurosci 7:1370-1375. CrossRef Medline
59. Wise SP (2008) Forward frontal fields: phylogeny and fundamental function. Trends Neurosci 31:599-608. CrossRef Medline
60. Young JJ, Shapiro ML (2009) Double dissociation and hierarchical organization of strategy switches and reversals in the rat PFC. Behav Neurosci 123:1028-1035. CrossRef Medline