Orbitofrontal cortex inactivation impairs between- but not within-session Pavlovian extinction: An associative analysis

Neurobiology of Learning and Memory

Volumn 108, Issue , 2014, Pages 78-87

  Panayi, Marios C ^a   Killcross, Simon ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Extinction; Orbitofrontal cortex; Pavlovian; Prediction error

Indexed keywords

EXTINCTION; ORBITOFRONTAL CORTEX; PAVLOVIAN; PREDICTION ERROR;

ANIMALS; ASSOCIATION LEARNING; CONDITIONING, CLASSICAL; EXTINCTION, PSYCHOLOGICAL; GABA-A RECEPTOR AGONISTS; MALE; MEMORY; MUSCIMOL; PREFRONTAL CORTEX; RATS; RATS, LONG-EVANS;

EID: 84893764522     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2013.08.002     Document Type: Article

References (61)

1. Boulougouris V., Dalley J.W., Robbins T.W. Effects of orbitofrontal, infralimbic and prelimbic cortical lesions on serial spatial reversal learning in the rat. Behavioural Brain Research 2007, 179(2):219-228.
2. Boulougouris V., Robbins T.W. Pre-surgical training ameliorates orbitofrontal-mediated impairments in spatial reversal learning. Behavioural Brain Research 2009, 197(2):469-475.
3. Bouton M.E. Context, time, and memory retrieval in the interference paradigms of pavlovian learning. Psychological Bulletin 1993, 114(1):80-99.
4. Burke K.A., Takahashi Y.K., Correll J., Brown P.L., Schoenbaum G. Orbitofrontal inactivation impairs reversal of Pavlovian learning by interfering with 'disinhibition' of responding for previously unrewarded cues. European Journal of Neuroscience 2009, 30(10):1941-1946.
5. Butter, C. M. (1969). Perseveration in Extinction and in Discrimination Reversal Tasks Following Selective Frontal Ablations in Macaca Mulatta. Physiology & Behavior, 4(2), 163-&.
6. Chudasama Y., Robbins T.W. Dissociable contributions of the orbitofrontal and infralimbic cortex to pavlovian autoshaping and discrimination reversal learning: further evidence for the functional heterogeneity of the rodent frontal cortex. Journal of Neuroscience 2003, 23(25):8771-8780.
7. Dalley J.W., Laane K., Theobald D.E., Armstrong H.C., Corlett P.R., Chudasama Y., et al. Time-limited modulation of appetitive Pavlovian memory by D1 and NMDA receptors in the nucleus accumbens. Proceedings of the National Academy of Sciences of the USA 2005, 102(17):6189-6194.
8. Delamater A.R. Experimental extinction in Pavlovian conditioning: Behavioural and neuroscience perspectives. Quarterly Journal of Experimental Psychology Section B - Comparative and Physiological Psychology 2004, 57(2):97-132.
9. Delamater A.R. The role of the orbitofrontal cortex in sensory-specific encoding of associations in Pavlovian and instrumental conditioning. Linking affect to action: Critical contributions of the orbitofrontal cortex 2007, Vol. 1121:152-173. Blackwell Publishing, Oxford.
10. Delamater A.R. Issues in the extinction of specific stimulus-outcome associations in Pavlovian conditioning. Behaviour Processes 2012, 90(1):9-19.
11. Delamater A.R. On the nature of CS and US representations in Pavlovian learning. Learning & Behavior 2012, 40(1):1-23.
12. Delamater A.R., Campese V., Westbrook R.F. Renewal and spontaneous recovery, but not latent inhibition, are mediated by gamma-aminobutyric acid in appetitive conditioning. Journal of Experimental Psychology: Animal Behavior Processes 2009, 35(2):224-237.
13. Dickinson, A., & Dearing, M. F. (1979). Appetitive-aversive interactions and inhibitory processes. In A. Dickinson, R. A. Boakes (Eds.), Mechanisms of learning and Motivation: A memorial volume to Jerzy Konorski (pp. 203-232). Hillsdale, NJ: Erlbaum.
14. Gallagher M., McMahan R.W., Schoenbaum G. Orbitofrontal cortex and representation of incentive value in associative learning. Journal of Neuroscience 1999, 19(15):6610-6614.
15. Hall, G. (2002). Associative structures in Pavlovian and instrumental conditioning. In: C. R. Gallistel (Ed.), Stevens' handbook of experimental psychology, third ed., (vol. 3, pp. 1-45). New York: John Wiley & Sons.
16. Harris J.A., Carpenter J.S. Response rate and reinforcement rate in Pavlovian conditioning. Journal of Experimental Psychology: Animal Behavior Processes 2011, 37(4):375-384.
17. Hart G., Harris J.A., Westbrook R.F. Systemic or intra-amygdala infusion of the benzodiazepine, midazolam, impairs learning, but facilitates re-learning to inhibit fear responses in extinction. Learning & Memory 2010, 17(4):210-220.
18. Herry C., Ferraguti F., Singewald N., Letzkus J.J., Ehrlich I., Luthi A. Neuronal circuits of fear extinction. European Journal of Neuroscience 2010, 31(4):599-612.
19. Huston J.P., Silva M.A., Komorowski M., Schulz D., Topic B. Animal models of extinction-induced depression: Loss of reward and its consequences. Neuroscience and Biobehavioral Reviews 2013, 10.
20. Izquierdo A., Murray E.A. Opposing effects of amygdala and orbital prefrontal cortex lesions on the extinction of instrumental responding in macaque monkeys. European Journal of Neuroscience 2005, 22(9):2341-2346.
21. Kaplan G.B., Heinrichs S.C., Carey R.J. Treatment of addiction and anxiety using extinction approaches: neural mechanisms and their treatment implications. Pharmacology, Biochemistry and Behavior 2011, 97(3):619-625.
22. Laborda M.A., Miguez G., Polack C.W., Miller R.R. Animal models of psychopathology: Historical models and the pavlovian contribution. Terapia Psicologica 2012, 30(1):45-59.
23. Lantz E.A. Effect of number of trials, interstimulus interval, and dishabituation during CS habituation on subsequent conditioning in a CER paradigm. Animal Learning & Behavior 1973, 1(4):273-277.
24. LePelley M.E. The role of associative history in models of associative learning: A selective review and a hybrid model. Quarterly Journal of Experimental Psychology 2004, 57B:192-243.
25. Leung H.T., Westbrook R.F. Spontaneous recovery of extinguished fear responses deepens their extinction: a role for error-correction mechanisms. Journal of Experimental Psychology: Animal Behavior Processes 2008, 34(4):461-474.
26. Levy D.J., Glimcher P.W. The root of all value: a neural common currency for choice. Current Opinion in Neurobiology 2012, 22(6):1027-1038.
27. Li S.H., Westbrook R.F. Massed extinction trials produce better short-term but worse long-term loss of context conditioned fear responses than spaced trials. Journal of Experimental Psychology: Animal Behavior Processes 2008, 34(3):336-351.
28. Mackintosh N.J. A theory of attention: Variations in the associability of stimuli with reinforcement. Psychological Review 1975, 82(4):279-298.
29. Makkar S.R., Zhang S.Q., Cranney J. Behavioral and neural analysis of GABA in the acquisition, consolidation, reconsolidation, and extinction of fear memory. Neuropsychopharmacology 2010, 35(8):1625-1652.
30. McAlonan K., Brown V.J. Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behavioural Brain Research 2003, 146(1-2):97-103.
31. Ostlund S.B., Balleine B.W. Orbitofrontal cortex mediates outcome encoding in pavlovian but not instrumental conditioning. Journal of Neuroscience 2007, 27(18):4819-4825.
32. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, San Diego. 4th ed.
33. Pearce J.M., Hall G. A model for Pavlovian learning: Variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychological Review 1980, 87(6):532-552.
34. Pickens C.L., Saddoris M.P., Gallagher M., Holland P.C. Orbitofrontal lesions impair use of cue-outcome associations in a devaluation task. Behavioral Neuroscience 2005, 119(1):317-322.
35. Pickens C.L., Saddoris M.P., Setlow B., Gallagher M., Holland P.C., Schoenbaum G. Different roles for orbitofrontal cortex and basolateral amygdala in a reinforcer devaluation task. Journal of Neuroscience 2003, 23(35):11078-11084.
36. Quirk G.J., Russo G.K., Barron J.L., Lebron K. The role of ventromedial prefrontal cortex in the recovery of extinguished fear. Journal of Neuroscience 2000, 20(16):6225-6231.
37. Ramirez D.R., Savage L.M. Differential involvement of the basolateral amygdala, orbitofrontal cortex, and nucleus accumbens core in the acquisition and use of reward expectancies. Behavioral Neuroscience 2007, 121(5):896-906.
38. Reekie Y.L., Braesicke K., Man M.S., Roberts A.C. Uncoupling of behavioral and autonomic responses after lesions of the primate orbitofrontal cortex. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(28):9787-9792.
39. Rescorla, R. A. (1979). Conditioned inhibition and extinction. In A. Dickinson, R. A. Boakes (Eds.), Mechanisms of learning and Motivation: A memorial volume to Jerzy Konorski (pp. 83-110). Hillsdale, NJ: Erlbaum.
40. Rescorla R.A. Spontaneous recovery. Learning & Memory 2004, 11(5):501-509.
41. Rescorla R.A., Cunningham C.L. The erasure of reinstated fear. Animal Learning & Behavior 1977, 5(4):386-394.
42. Rescorla R.A., Cunningham C.L. Recovery of the US representation over time during extinction. Learning and Motivation 1978, 9:373-391.
43. Rescorla R.A., Wagner A.R. A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. Classical conditioning II: Current theory and research 1972, 64-99. Appleton-Century-Crofts, New York. A.H. Black, W.F. Prokasy (Eds.).
44. Rhodes S.E., Killcross S. Lesions of rat infralimbic cortex enhance recovery and reinstatement of an appetitive Pavlovian response. Learning & Memory 2004, 11(5):611-616.
45. Rhodes S.E.V., Killcross A.S. Lesions of rat infralimbic cortex enhance renewal of extinguished appetitive Pavlovian responding. European Journal of Neuroscience 2007, 25(8):2498-2503.
46. Riceberg J.S., Shapiro M.L. Reward stability determines the contribution of orbitofrontal cortex to adaptive behavior. Journal of Neuroscience 2012, 32(46):16402-16409.
47. 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. Reward and Decision Making in Corticobasal Ganglia Networks 2007, 1104:21-34.
48. Roesch M.R., Calu D.J., Esber G.R., Schoenbaum G. All that glitters dissociating attention and outcome expectancy from prediction errors signals. Journal of Neurophysiology 2010, 104(2):587-595.
49. Rudebeck P.H., Murray E.A. Amygdala and orbitofrontal cortex lesions differentially influence choices during object reversal learning. Journal of Neuroscience 2008, 28(33):8338-8343.
50. Sah P., Westbrook R.F. Behavioural neuroscience. The circuit of fear. Nature 2008, 454(7204):589-590.
51. Schiller D., Weiner I. Lesions to the basolateral amygdala and the orbitofrontal cortex but not to the medial prefrontal cortex produce an abnormally persistent latent inhibition in rats. Neuroscience 2004, 128(1):15-25.
52. Schoenbaum G., Setlow B., Nugent S.L., Saddoris M.P., Gallagher M. Lesions of orbitofrontal cortex and basolateral amygdala complex disrupt acquisition of odor-guided discriminations and reversals. Learning & Memory 2003, 10(2):129-140.
53. Schoenbaum G., Takahashi Y., Liu T., McDannald M.A. Does the orbitofrontal cortex signal value?. Annals of the New York Academy of Sciences 2011, 1239(1):87-99.
54. Steinberg E.E., Keiflin R., Boivin J.R., Witten I.B., Deisseroth K., Janak P.H. A causal link between prediction errors, dopamine neurons and learning. Nature Neuroscience 2013, 16(7):966-973.
55. Sutton R.S., Barto A.G. Reinforcement learning: An introduction 1998, MIT Press, Cambridge, MA.
56. Takahashi Y.K., Roesch M.R., Stainaker T.A., Haney R.Z., Caiu D.J., Taylor A., et al. The orbitofrontal cortex and ventral tegmental area are necessary for learning from unexpected outcomes. Neuron 2009, 62(2):269-280.
57. Takahashi Y.K., Roesch M.R., Wilson R.C., Toreson K., O'Donnell P., Niv Y., et al. Expectancy-related changes in firing of dopamine neurons depend on orbitofrontal cortex. Nature Neuroscience 2011, 14(12):1590-1597.
58. van Duuren E., Lankelma J., Pennartz C.M. Population coding of reward magnitude in the orbitofrontal cortex of the rat. Journal of Neuroscience 2008, 28(34):8590-8603.
59. van Wingerden M., Vinck M., Lankelma J., Pennartz C.M. Theta-band phase locking of orbitofrontal neurons during reward expectancy. Journal of Neuroscience 2010, 30(20):7078-7087.
60. Wagner A.R., Brandon S.E. Evolution of a structured connectionist model of Pavlovian conditioning (ÆSOP). Contemporary learning theories: Pavliocian conditioning and the status of tradional learning theories 1989, Erlbaum, Hillsdale, NJ. S.B. Klein, R.R. Mowrer (Eds.).
61. Wagner A.R. SOP: A model of automatic memory processing in animal behavior. Information processing in animals: Memory mechanisms 1981, 5-47. Erlbaum, Hillsdale, NJ. N.E. Spear, R.R. Miller (Eds.).