Selective Control of Fear Expression by Optogenetic Manipulation of Infralimbic Cortex after Extinction

Neuropsychopharmacology

Volumn 41, Issue 5, 2016, Pages 1261-1273

  Kim, Hyung Su ^a,b   Cho, Hye Yeon ^a   Augustine, George J ^b,c,d   Han, Jin Hee ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Korea Institute of Science and Technology   (South Korea)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; SYNAPSIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EXPECTATION; FEAR; FEAR EXTINCTION; GENE EXPRESSION; INFRALIMBIC CORTEX; MALE; MOUSE; NERVE CELL; NONHUMAN; OPTOGENETICS; PHOTOINHIBITION; PHOTOSTIMULATION; PRIORITY JOURNAL; RECALL; ANIMAL; AUDITORY STIMULATION; C57BL MOUSE; CONDITIONED REFLEX; METABOLISM; PHYSIOLOGY; PREFRONTAL CORTEX; REINFORCEMENT;

ACOUSTIC STIMULATION; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CONDITIONING, CLASSICAL; EXTINCTION, PSYCHOLOGICAL; FEAR; MALE; MENTAL RECALL; MICE; MICE, INBRED C57BL; NEURONS; OPTOGENETICS; PREFRONTAL CORTEX;

EID: 84960911516     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2015.276     Document Type: Article

References (50)

1. Amano T, Unal CT, Pare D (2010). Synaptic correlates of fear extinction in the amygdala. Nat Neurosci 13: 489-494.
2. Benson DL, Isackson PJ, Gall CM, Jones EG (1992). Contrasting patterns in the localization of glutamic acid decarboxylase and Ca2+/calmodulin protein kinase gene expression in the rat central nervous system. Neuroscience 46: 825-849.
3. Chang CH, Berke JD, Maren S (2010). Single-unit activity in the medial prefrontal cortex during immediate and delayed extinction of fear in rats. PLoS ONE 5: e11971.
4. Cho JH, Deisseroth K, Bolshakov VY (2013). Synaptic encoding of fear extinction in mPFC-amygdala circuits. Neuron 80: 1491-1507.
5. Do-Monte FH, Manzano-Nieves G, Quinones-Laracuente K, Ramos-Medina L, Quirk GJ (2015). Revisiting the role of infralimbic cortex in fear extinction with optogenetics. J Neurosci 35: 3607-3615.
6. Fanselow MS, Gale GD (2003). The amygdala, fear, and memory. Ann NY Acad Sci 985: 125-134.
7. Farinelli M, Deschaux O, Hugues S, Thevenet A, Garcia R (2006). Hippocampal train stimulation modulates recall of fear extinction independently of prefrontal cortex synaptic plasticity and lesions. Learn Mem 13: 329-334.
8. Franklin KBJ, Paxinos G (2008). The Mouse Brain in Stereotaxic Coordinates3rd ednAcademic Press (Elsevier): New York.
9. Garcia R, Chang CH, Maren S (2006). Electrolytic lesions of the medial prefrontal cortex do not interfere with long-term memory of extinction of conditioned fear. Learn Mem 13: 14-17.
10. Gewirtz JC, Falls WA, Davis M (1997). Normal conditioned inhibition and extinction of freezing and fear-potentiated startle following electrolytic lesions of medial prefrontal cortex in rats. Behav Neurosci 111: 712-726.
11. Goshen I, Brodsky M, Prakash R, Wallace J, Gradinaru V, Ramakrishnan C et al (2011). Dynamics of retrieval strategies for remote memories. Cell 147: 678-689.
12. Herry C, Ferraguti F, Singewald N, Letzkus JJ, Ehrlich I, Luthi A (2010). Neuronal circuits of fear extinction. Eur J Neurosci 31: 599-612.
13. Herry C, Vouimba RM, Garcia R (1999). Plasticity in the mediodorsal thalamo-prefrontal cortical transmission in behaving mice. J Neurophysiol 82: 2827-2832.
14. Hoover WB, Vertes RP (2007). Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 212: 149-179.
15. Hugues S, Chessel A, Lena I, Marsault R, Garcia R (2006). Prefrontal infusion of PD098059 immediately after fear extinction training blocks extinction-associated prefrontal synaptic plasticity and decreases prefrontal ERK2 phosphorylation. Synapse 60: 280-287.
16. Kapp BS, Frysinger RC, Gallagher M, Haselton JR (1979). Amygdala central nucleus lesions: effect on heart rate conditioning in the rabbit. Physiol Behav 23: 1109-1117.
17. Knapska E, Maren S (2009). Reciprocal patterns of c-Fos expression in the medial prefrontal cortex and amygdala after extinction and renewal of conditioned fear. Learn Mem 16: 486-493.
18. Kwon JT, Nakajima R, Kim HS, Jeong Y, Augustine GJ, Han JH (2014). Optogenetic activation of presynaptic inputs in lateral amygdala forms associative fear memory. Learn Mem 21: 627-633.
19. LaLumiere RT, Niehoff KE, Kalivas PW (2010). The infralimbic cortex regulates the consolidation of extinction after cocaine selfadministration. Learn Mem 17: 168-175.
20. Laurent V, Westbrook RF (2009). Inactivation of the infralimbic but not the prelimbic cortex impairs consolidation and retrieval of fear extinction. Learn Mem 16: 520-529.
21. Lebron K, Milad MR, Quirk GJ (2004). Delayed recall of fear extinction in rats with lesions of ventral medial prefrontal cortex. Learn Mem 11: 544-548.
22. LeDoux JE (2000). Emotion circuits in the brain. Annu Rev Neurosci 23: 155-184.
23. Lee AT, Vogt D, Rubenstein JL, Sohal VS (2014). A class of GABAergic neurons in the prefrontal cortex sends long-range projections to the nucleus accumbens and elicits acute avoidance behavior. J Neurosci 34: 11519-11525.
24. Milad MR, Quirk GJ (2002). Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420: 70-74.
25. Milad MR, Quirk GJ (2012). Fear extinction as a model for translational neuroscience: ten years of progress. Annu Rev Psychol 63: 129-151.
26. Milad MR, Rauch SL, Pitman RK, Quirk GJ (2006). Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol Psychol 73: 61-71.
27. Milad MR, Vidal-Gonzalez I, Quirk GJ (2004). Electrical stimulation of medial prefrontal cortex reduces conditioned fear in a temporally specific manner. Behav Neurosci 118: 389-394.
28. Milad MR, Wright CI, Orr SP, Pitman RK, Quirk GJ, Rauch SL (2007). Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol Psychiatry 62: 446-454.
29. Morgan MA, LeDoux JE (1995). Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behav Neurosci 109: 681-688.
30. Morgan MA, Romanski LM, LeDoux JE (1993). Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci Lett 163: 109-113.
31. Morgan MA, Schulkin J, LeDoux JE (2003). Ventral medial prefrontal cortex and emotional perseveration: the memory for prior extinction training. Behav Brain Res 146: 121-130.
32. Myers KM, Davis M (2007). Mechanisms of fear extinction. Mol Psychiatry 12: 120-150.
33. Pavlov I (1927). Conditioned Reflexes. Oxford University Press: Oxford, UK.
34. Peters J, Kalivas PW, Quirk GJ (2009). Extinction circuits for fear and addiction overlap in prefrontal cortex. Learn Mem 16: 279-288.
35. Phelps EA, Delgado MR, Nearing KI, LeDoux JE (2004). Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43: 897-905.
36. Quirk GJ, Garcia R, Gonzalez-Lima F (2006). Prefrontal mechanisms in extinction of conditioned fear. Biol Psychiatry 60: 337-343.
37. Quirk GJ, Mueller D (2008). Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33: 56-72.
38. Quirk GJ, Russo GK, Barron JL, Lebron K (2000). The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J Neurosci 20: 6225-6231.
39. Rosenkranz JA, Moore H, Grace AA (2003). The prefrontal cortex regulates lateral amygdala neuronal plasticity and responses to previously conditioned stimuli. J Neurosci 23: 11054-11064.
40. Santini E, Quirk GJ, Porter JT (2008). Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. J Neurosci 28: 4028-4036.
41. Senn V, Wolff SB, Herry C, Grenier F, Ehrlich I, Grundemann J et al (2014). Long-range connectivity defines behavioral specificity of amygdala neurons. Neuron 81: 428-437.
42. Sierra-Mercado D, Corcoran KA, Lebron-Milad K, Quirk GJ (2006). Inactivation of ventromedial prefrontal cortex reduces expression of conditioned fear and impairs subsequent recall of extinction. Eur J Neurosci 24: 1751-1758.
43. Sierra-Mercado D, Padilla-Coreano N, Quirk GJ (2011). Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36: 529-538.
44. Sotres-Bayon F, Bush DE, LeDoux JE (2004). Emotional perseveration: an update on prefrontal-amygdala interactions in fear extinction. Learn Mem 11: 525-535.
45. Sotres-Bayon F, Quirk GJ (2010). Prefrontal control of fear: more than just extinction. Curr Opin Neurobiol 20: 231-235.
46. Thompson BM, Baratta MV, Biedenkapp JC, Rudy JW, Watkins LR, Maier SF (2010). Activation of the infralimbic cortex in a fear context enhances extinction learning. Learn Mem 17: 591-599.
47. Trouche S, Sasaki JM, Tu T, Reijmers LG (2013). Fear extinction causes target-specific remodeling of perisomatic inhibitory synapses. Neuron 80: 1054-1065.
48. Van den Oever MC, Rotaru DC, Heinsbroek JA, Gouwenberg Y, Deisseroth K, Stuber GD et al (2013). Ventromedial prefrontal cortex pyramidal cells have a temporal dynamic role in recall and extinction of cocaine-associated memory. J Neurosci 33: 18225-18233.
49. Vidal-Gonzalez I, Vidal-Gonzalez B, Rauch SL, Quirk GJ (2006). Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 13: 728-733.
50. Willcocks AL, McNally GP (2013). The role of medial prefrontal cortex in extinction and reinstatement of alcohol-seeking in rats. Eur J Neurosci 37: 259-268.