Inactivating the infralimbic but not prelimbic medial prefrontal cortex facilitates the extinction of appetitive Pavlovian conditioning in Long-Evans rats

Neurobiology of Learning and Memory

Volumn 118, Issue , 2015, Pages 198-208

  Mendoza, J ^a   Sanio, C ^a   Chaudhri, N ^a  

^a Center for Studies in Behavioural Neurobiology/FRQS Groupe de recherche en neurobiologie Tementale Department of Psychology Concordia University ^*  (Canada)

Author keywords

Inhibitory conditioning; Instrumental conditioning; Learning; Pavlovian conditioning; Prefrontal cortex; Sucrose

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; SUCROSE; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR STIMULATING AGENT; BACLOFEN; MUSCIMOL;

ANATOMICAL VARIATION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONDITIONING; CONTROLLED STUDY; INFRALIMBIC MEDIAL PREFRONTAL CORTEX; INSTRUMENTAL CONDITIONING; MALE; MEMORY CONSOLIDATION; NONHUMAN; PAVLOVIAN CONDITIONING; PREFRONTAL CORTEX; PRELIMBIC MEDIAL PREFRONTAL CORTEX; RAT; REINFORCEMENT; TASK PERFORMANCE; ANIMAL; APPETITE; CONDITIONED REFLEX; DRUG EFFECTS; LONG EVANS RAT; PHYSIOLOGY;

ANIMALS; APPETITIVE BEHAVIOR; BACLOFEN; CONDITIONING, CLASSICAL; CONDITIONING, OPERANT; EXTINCTION, PSYCHOLOGICAL; GABA-A RECEPTOR AGONISTS; GABA-B RECEPTOR AGONISTS; MALE; MUSCIMOL; PREFRONTAL CORTEX; RATS; RATS, LONG-EVANS;

EID: 84921368638     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2014.12.006     Document Type: Article

References (50)

1. Bossert J.M., Stern A.L., Theberge F.R., Cifani C., Koya E., Hope B.T., Shaham Y. Ventral medial prefrontal cortex neuronal ensembles mediate context-induced relapse to heroin. Nature Neuroscience 2011, 14:420-422.
2. Bouton M.E., Westbrook R.F., Corcoran K.A., Maren S. Contextual and temporal modulation of extinction: Behavioral and biological mechanisms. Biological Psychiatry 2006, 60:352-360.
3. Burgos-Robles A., Vidal-Gonzalez I., Quirk G.J. Sustained conditioned responses in prelimbic prefrontal neurons are correlated with fear expression and extinction failure. The Journal of Neuroscience. The Official Journal of the Society for Neuroscience 2009, 29:8474-8482.
4. Chang C.H., Maren S. Strain difference in the effect of infralimbic cortex lesions on fear extinction in rats. Behavioral Neuroscience 2010, 124:391-397.
5. Chaudhri N., Sahuque L.L., Janak P.H. Context-induced relapse of conditioned behavioral responding to ethanol cues in rats. Biological Psychiatry 2008, 64:203-210.
6. Chaudhri N., Woods C.A., Sahuque L.L., Gill T.M., Janak P.H. Unilateral inactivation of the basolateral amygdala attenuates context-induced renewal of Pavlovian-conditioned alcohol-seeking. The European Journal of Neuroscience 2013, 38:2751-2761.
7. Chudasama Y., Passetti F., Rhodes S.E., Lopian D., Desai A., Robbins T.W. Dissociable aspects of performance on the 5-choice serial reaction time task following lesions of the dorsal anterior cingulate, infralimbic and orbitofrontal cortex in the rat: Differential effects on selectivity, impulsivity and compulsivity. Behavioural Brain Research 2003, 146:105-119.
8. Corcoran K.A., Quirk G.J. Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. The Journal of neuroscience. The official journal of the Society for Neuroscience 2007, 27:840-844.
9. Garcia R., Chang C.H., Maren S. Electrolytic lesions of the medial prefrontal cortex do not interfere with long-term memory of extinction of conditioned fear. Learning & Memory 2006, 13:14-17.
10. Gass J.T., Trantham-Davidson H., Kassab A.S., Glen W.B., Olive M.F., Chandler L.J. Enhancement of extinction learning attenuates ethanol-seeking behavior and alters plasticity in the prefrontal cortex. The Journal of Neuroscience. The Official Journal of the Society for Neuroscience 2014, 34:7562-7574.
11. Ghazizadeh A., Ambroggi F., Odean N., Fields H.L. Prefrontal cortex mediates extinction of responding by two distinct neural mechanisms in accumbens shell. The Journal of Neuroscience. The Official Journal of the Society for Neuroscience 2012, 32:726-737.
12. Groblewski P.A., Cunningham C.L. Repeated microinjections into the medial prefrontal cortex (mPFC) impair extinction of conditioned place preference in mice. Behavioural Brain Research 2012, 230:299-303.
13. Groblewski P.A., Ryabinin A.E., Cunningham C.L. Activation and role of the medial prefrontal cortex (mPFC) in extinction of ethanol-induced associative learning in mice. Neurobiology of Learning and Memory 2012, 97:37-46.
14. Kalivas P.W., Volkow N.D. The neural basis of addiction: A pathology of motivation and choice. The American Journal of Psychiatry 2005, 162:1403-1413.
15. LaLumiere R.T., Niehoff K.E., Kalivas P.W. The infralimbic cortex regulates the consolidation of extinction after cocaine self-administration. Learning & Memory 2010, 17:168-175.
16. LaLumiere R.T., Smith K.C., Kalivas P.W. Neural circuit competition in cocaine-seeking: roles of the infralimbic cortex and nucleus accumbens shell. The European Journal of Neuroscience 2012, 35:614-622.
17. Laurent V., Westbrook R.F. Inactivation of the infralimbic but not the prelimbic cortex impairs consolidation and retrieval of fear extinction. Learning & Memory 2009, 16:520-529.
18. Marchant N.J., Furlong T.M., McNally G.P. Medial dorsal hypothalamus mediates the inhibition of reward seeking after extinction. The Journal of Neuroscience. The Official Journal of the Society for Neuroscience 2010, 30:14102-14115.
19. Maren S., Chang C.H. Recent fear is resistant to extinction. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:18020-18025.
20. Martin J.H. Autoradiographic estimation of the extent of reversible inactivation produced by microinjection of lidocaine and muscimol in the rat. Neuroscience Letters 1991, 127:160-164.
21. Martin J.H., Ghez C. Pharmacological inactivation in the analysis of the central control of movement. Journal of Neuroscience Methods 1999, 86:145-159.
22. Milad M.R., Quirk G.J. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 2002, 420:70-74.
23. Milad M.R., Vidal-Gonzalez I., Quirk G.J. Electrical stimulation of medial prefrontal cortex reduces conditioned fear in a temporally specific manner. Behavioral Neuroscience 2004, 118:389-394.
24. Morgan M.A., Romanski L.M., LeDoux J.E. Extinction of emotional learning: Contribution of medial prefrontal cortex. Neuroscience Letters 1993, 163:109-113.
25. Murphy E.R., Dalley J.W., Robbins T.W. Local glutamate receptor antagonism in the rat prefrontal cortex disrupts response inhibition in a visuospatial attentional task. Psychopharmacology (Berl) 2005, 179:99-107.
26. Parent M.B., McGaugh J.L. Posttraining infusion of lidocaine into the amygdala basolateral complex impairs retention of inhibitory avoidance training. Brain Research 1994, 661:97-103.
27. Pavlov I.P. Conditioned reflexes 1927, Oxford University Press, Oxford, UK.
28. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1997, Academic Press. 3rd ed.
29. Peters J., De Vries T.J. D-cycloserine administered directly to infralimbic medial prefrontal cortex enhances extinction memory in sucrose-seeking animals. Neuroscience 2013, 230:24-30.
30. Peters J., Kalivas P.W., Quirk G.J. Extinction circuits for fear and addiction overlap in prefrontal cortex. Learning & Memory 2009, 16:279-288.
31. Peters J., LaLumiere R.T., Kalivas P.W. Infralimbic prefrontal cortex is responsible for inhibiting cocaine seeking in extinguished rats. The Journal of Neuroscience. The Official Journal of the Society for Neuroscience 2008, 28:6046-6053.
32. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 2008, 33:56-72.
33. Quirk G.J., Russo G.K., Barron J.L., Lebron K. The role of ventromedial prefrontal cortex in the recovery of extinguished fear. The Journal of Neuroscience. The Official Journal of the Society for Neuroscience 2000, 20:6225-6231.
34. Rhodes S.E., Killcross S. Lesions of rat infralimbic cortex enhance recovery and reinstatement of an appetitive Pavlovian response. Learning & memory 2004, 11:611-616.
35. Rhodes S.E., Killcross S. Lesions of rat infralimbic cortex enhance renewal of extinguished appetitive Pavlovian responding. The European journal of neuroscience 2007, 25:2498-2503.
36. Rocha A., Kalivas P.W. Role of the prefrontal cortex and nucleus accumbens in reinstating methamphetamine seeking. The European Journal of Neuroscience 2010, 31:903-909.
37. Rogers J.L., Ghee S., See R.E. The neural circuitry underlying reinstatement of heroin-seeking behavior in an animal model of relapse. Neuroscience 2008, 151:579-588.
38. Santini E., Quirk G.J., Porter J.T. Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. The Journal of Neuroscience. The Official Journal of the Society for Neuroscience 2008, 28:4028-4036.
39. Sierra-Mercado D., Corcoran K.A., Lebron-Milad K., Quirk G.J. Inactivation of the ventromedial prefrontal cortex reduces expression of conditioned fear and impairs subsequent recall of extinction. The European Journal of Neuroscience 2006, 24:1751-1758.
40. Sierra-Mercado D., Padilla-Coreano N., Quirk G.J. Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 2011, 36:529-538.
41. Skinner B.F. The behavior of organisms 1938, Appleton-Century, New York.
42. Sun N., Chi N., Lauzon N., Bishop S., Tan H., Laviolette S.R. Acquisition, extinction, and recall of opiate reward memory are signaled by dynamic neuronal activity patterns in the prefrontal cortex. Cerebral Cortex 2011, 21:2665-2680.
43. Tsutsui-Kimura I., Ohmura Y., Izumi T., Kumamoto H., Yamaguchi T., Yoshida T., Yoshioka M. Milnacipran enhances the control of impulsive action by activating D(1)-like receptors in the infralimbic cortex. Psychopharmacology (Berl) 2013, 225:495-504.
44. van Duuren E., van der Plasse G., van der Blom R., Joosten R.N., Mulder A.B., Pennartz C.M., Feenstra M.G. Pharmacological manipulation of neuronal ensemble activity by reverse microdialysis in freely moving rats: A comparative study of the effects of tetrodotoxin, lidocaine, and muscimol. The Journal of Pharmacology and Experimental Therapeutics 2007, 323:61-69.
45. Vidal-Gonzalez I., Vidal-Gonzalez B., Rauch S.L., Quirk G.J. Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learning & Memory 2006, 13:728-733.
46. Walker D.L., Davis M. The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction. Pharmacology, Biochemistry, and Behavior 2002, 71:379-392.
47. Walker D.L., Ressler K.J., Lu K.T., Davis M. Facilitation of conditioned fear extinction by systemic administration or intra-amygdala infusions of D-cycloserine as assessed with fear-potentiated startle in rats. The Journal of Neuroscience. The Official Journal of the Society for Neuroscience 2002, 22:2343-2351.
48. Willcocks A.L., McNally G.P. The role of medial prefrontal cortex in extinction and reinstatement of alcohol-seeking in rats. The European Journal of Neuroscience 2013, 37:259-268.
49. Yun I.A., Nicola S.M., Fields H.L. Contrasting effects of dopamine and glutamate receptor antagonist injection in the nucleus accumbens suggest a neural mechanism underlying cue-evoked goal-directed behavior. The European Journal of Neuroscience 2004, 20:249-263.
50. Zavala A.R., Weber S.M., Rice H.J., Alleweireldt A.T., Neisewander J.L. Role of the prelimbic subregion of the medial prefrontal cortex in acquisition, extinction, and reinstatement of cocaine-conditioned place preference. Brain Research 2003, 990:157-164.