Neuropeptide Y impairs retrieval of extinguished fear and modulates excitability of neurons in the infralimbic prefrontal cortex

Journal of Neuroscience

Volumn 36, Issue 4, 2016, Pages 1306-1315

  Vollmer, Lauren L ^a   Schmeltzer, Sarah ^a   Schurdak, Jennifer ^a   Ahlbrand, Rebecca ^a   Rush, Jennifer ^a   Dolgas, Charles M ^a   Baccei, Mark L ^a,b   Sah, Renu ^a,c  

^a UNIVERSITY OF CINCINNATI   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Extinction; Fear; Infralimbic; Neuropeptide Y; Prefrontal; Y1

Indexed keywords

NEUROPEPTIDE Y; ARGININE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CORTICOSTERONE; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 1; N2 DIPHENYLACETYL N (4 UREIDOMETHYLBENZYL)ARGININAMIDE; NEUROPEPTIDE Y RECEPTOR;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPRESSION; EXCITATION; FEAR; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INFRALIMBIC CORTEX; MALE; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; RAT; STRESS; WORKING MEMORY; ANALOGS AND DERIVATIVES; ANIMAL; CHEMICALLY INDUCED; CYTOLOGY; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; LEARNING DISORDER; METABOLISM; NERVE CELL; PREFRONTAL CORTEX; RECALL; REINFORCEMENT; SPRAGUE DAWLEY RAT; SYNAPTIC POTENTIAL;

ANIMALS; ARGININE; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CORTICOSTERONE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EXTINCTION, PSYCHOLOGICAL; FEAR; GLUTAMATE DECARBOXYLASE; LEARNING DISORDERS; MALE; MENTAL RECALL; NEURONS; NEUROPEPTIDE Y; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROPEPTIDE Y; SYNAPTIC POTENTIALS;

EID: 84956808434     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4955-13.2016     Document Type: Article

References (54)

1. Adrian TE, Allen JM, Bloom SR, Ghatei MA, Rossor MN, Roberts GW, Crow TJ, Tatemoto K, Polak JM (1983) Neuropeptide Y distribution in human brain. Nature 306:584-586. CrossRef Medline
2. Alho H, Ferrarese C, Vicini S, Vaccarino F (1988) Subsets of GABAergic neurons in dissociated cell cultures of neonatal rat cerebral cortex show co-localization with specific modulator peptides. Brain Res 467:193-204. Medline
3. Allen YS, Adrian TE, Allen JM, Tatemoto K, Crow TJ, Bloom SR, Polak JM (1983) Neuropeptide Y distribution in rat brain. Science 221:877-879. CrossRef Medline
4. Bacci A, Huguenard JR, Prince DA (2002) Differential modulation of synaptic transmission by neuropeptide Y in rat neocortical neurons. Proc Natl Acad Sci U S A 99:17125-17130. CrossRef Medline
5. Burgos-Robles A, Vidal-Gonzalez I, Santini E, Quirk GJ (2007) Consolidation of fearextinctionrequiresNMDAreceptor-dependentburstingintheventromedial prefrontal cortex. Neuron 53:871-880. CrossRef Medline
6. Butts KA, Weinberg J, Young AH, Phillips AG (2011) Glucocorticoid receptors in the prefrontal cortex regulate stress-evoked dopamine efflux and aspects of executive function. Proc Natl Acad SciU S A108:18459-18464. CrossRef Medline
7. Caetano MS, Jin LE, Harenberg L, Stachenfeld KL, Arnsten AF, Laubach M (2012) Noradrenergic control of error perseveration in medial prefrontal cortex. Front Integr Neurosci 6:125. CrossRef Medline
8. Cohen H, Liu T, Kozlovsky N, Kaplan Z, Zohar J, Mathé AA (2012) The neuropeptide Y (NPY)-ergic system is associated with behavioral resilence to stress exposure in an animal model of post-traumatic stress disorder. Neuropsychopharmacology 37:350-363. CrossRef Medline
9. Colmers WF, Bleakman D (1994) Effects of neuropeptide Y on the electrical properties of neurons. Trends Neurosci 17:373-379. CrossRef Medline
10. Do-Monte FH, Manzano-Nieves G, Quiñones-Laracuente K, Ramos-Medina L, Quirk GJ (2015) Revisiting the role of the infralimbic cortex in fear extinction with optogenetics. J Neurosci 35:3607-3615. CrossRef Medline
11. Dumont Y, Fournier A, St-Pierre S, Quirion R (1996) Autoradiographic distribution of [ 125I]Leu31, Pro34]PYY and [ 125I]PYY3-36 binding sites in the rat brain evaluated with two newly developed Y1 and Y2 receptor radioligands. Synapse 22:139-158. CrossRef Medline
12. Eaton K, Sallee FR, Sah R (2007) Relevance of neuropeptide Y (NPY) in psychiatry. Curr Top Med Chem 7:1645-1659. CrossRef Medline
13. Eriksdotter-Nilsson M, Meister B, Hökfelt T, Elde R, Fahrenkrug J, Frey P, Oertel W, Rehfeld JF, Terenius L, Olson L (1987) Glutamic acid decarboxylase-and peptide-immunoreactive neurons in cortex cerebri following development in isolation: evidence of homotypic and disturbed patterns in intraocular grafts. Synapse 1:539-551. CrossRef Medline
14. Fendt M, Bürki H, Imobersteg S, Lingenhöhl K, McAllister KH, Orain D, Uzunov DP, Chaperon F (2009) Fear reducing effects of inta-amygdala neuropeptide Y infusion in animal model of conditioned fear: an NPY Y1 receptor independent effect. Psychopharmacology 206:291-301. CrossRef Medline
15. Figueiredo HF, Dolgas CM, Herman JP (2002) Stress activation of cortex and hippocampus is modulated by sex and stage of estrus. Endocrinology 143:2534-2540. CrossRef Medline
16. Floresco SB, Seamans JK, Phillips AG (1997) Selective roles for hippocampal, prefrontal cortical and ventral striatal circuits in radial-arm maze tasks with or without a delay. J Neurosci 17:1880-1890. Medline
17. Giesbrecht CJ, Mackay JP, Silveira HB, Urban JH, Colmers WF (2010) Countervailing modulation of Ih by neuropeptide Y and corticotrophinreleasing factor in basolateral amygdala as a possible mechanism for their effects on stress-related behaviors. J Neurosci 30:16970-16982. CrossRef Medline
18. Gutman AR, Yang Y, Ressler KJ, Davis M (2008) The role of Neuropeptide Y in the expression and extinction of fear-potentiated startle. J Neurosci 28:12682-12690. CrossRef Medline
19. Heilig M, Widerlöv E (1995) Neurobiology and clinical aspects of neuropeptide Y. Crit Rev Neurobiol 9:115-136. Medline
20. Inslicht SS, Metzler TJ, Garcia NM, Pineles SL, Milad MR, Orr SP, Marmar CR, Neylan TC (2013) Sex differences in fear conditioning in posttraumatic stress disorder. J Psychiatr Res 47:64-71. CrossRef Medline
21. Jovanovic T, Norrholm SD, Blanding NQ, Davis M, Duncan E, Bradley B, Ressler KJ (2010) Impaired fear inhibition is a biomarker of PTSD but not depression. Depress Anxiety 27:244-251. CrossRef Medline
22. Lach G, de Lima TC (2013) Role of NPY Y1 receptor on acquisition, consolidation, and extinction on contextual fear conditioning: dissociation between anxiety, locomotion and non-emotional memory. Neurobiol Learn Mem 103:26-33. CrossRef Medline
23. McGuire J, Herman JP, Horn PS, Sallee FR, Sah R (2010) Enhanced fear recall and emotional arousal in rats recovering from chronic variable stress. Physiol Behav 101:474-482. CrossRef Medline
24. McGuire JL, Larke LE, Sallee FR, Herman JP, Sah R (2011) Differential regulation of neuropeptide Y in the amygdala and prefrontal cortex during recovery from chronic variable stress. Front Behav Neurosci 5:54. CrossRef Medline
25. McKlveen JM, Myers B, Flak JN, Bundzikova J, Solomon MB, Seroogy KB, Herman JP (2013) Role of prefrontal cortex glucocorticoid receptors in stress and emotion. Biol Psychiatry 74:672-679. CrossRef Medline
26. McNally RJ (2006) Cognitive abnormalities in post-traumatic stress disorder. Trends Cog Sci 10:271-277. CrossRef Medline
27. McQuiston AR, Colmers WF (1996) Neuropeptide Y2 receptors inhibit the frequency of spontaneous but not miniature EPSCs in CA3 pyramidal cells of rat hippocampus. J Neurophysiol 76:3159-3168. Medline
28. Milad MR, Quirk GJ (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420:70-74. CrossRef Medline
29. Milad MR, Pitman RK, Ellis CB, Gold AL, Shin LM, Lasko NB, Zeidan MA, Handwerger K, Orr SP, Rauch SL (2009) Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry 66:1075-1082. CrossRef Medline
30. Molosh AI, Sajdyk TJ, Truitt WA, Zhu W, Oxford GS, Shekhar A (2013) NPY Y(1) receptors differentially modulate GABA(A) and NMDA receptors via divergent signal-transduction pathways to reduce excitability of amygdala neurons. Neuropsychopharmacology 38:1352-1364. CrossRef Medline
31. Parsons RG, Ressler KJ (2013) Implications of memory modulation for post-traumatic stress and fear disorders. Nat Neurosci 16:146-153. CrossRef Medline
32. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. San Diego: Academic.
33. Quirk GJ, Mueller D (2008) Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33:56-72. CrossRef Medline
34. Radley JJ, Arias CM, Sawchenko PE (2006) Regional differentiation of the medial prefrontal cortex in regulating adaptive responses to acute emotional stress. J Neurosci 26:12967-12976. CrossRef Medline
35. Rostkowski AB, Teppen TL, Peterson DA, Urban JH (2009) Cell-specific expression of neuropeptide Y Y1 receptor immunoreactivity in the rat basolateral amygdala. J Comp Neurol 517:166-176. CrossRef Medline
36. Sah R, Geracioti TD (2013) Neuropeptide Y and posttraumatic stress disorder. Mol Psychiatry 18:646-655. CrossRef Medline
37. Sah R, Ekhator NN, Strawn JR, Sallee FR, Baker DG, Horn PS, Geracioti TD Jr (2009) Low cerebrospinal fluid neuropeptide Y concentrations in posttraumatic stress disorder. Biol Psychiatry 66:705-707. CrossRef Medline
38. Sah R, Ekhator N, Jefferson-Wilson L, Horn P, Geracioti T Jr (2014) Cerebrospinal fluid neuropeptide Y in combat veterans with and without posttraumatic stress disorder. Psychoneuroendocrinology 40:277-283. CrossRef Medline
39. Sajdyk TJ, Johnson PL, Leitermann R, Fitz SD, Dietrich A, Morin M, Gehlert DR, Urban JH, Shekhar A (2008) Neuropeptide Y in the amygdala induces long term resilience to stress-induced reductions in social responses but not hypothalamic-adrenal-pituitary axis activity or hyperthermia. J Neurosci 28:893-903. CrossRef Medline
40. Serova LI, TiLlinger A, Alaluf LG, Laukova M, Keegan K, Sabban EL (2013) Single intranasal neuropeptide Y infusion attenuates development of PTSD-like symptoms to traumatic stress in rats. Neuroscience 236:298-312. CrossRef Medline
41. 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. CrossRef Medline
42. Sommer WH, Lidstrom J, Sun H, Passer D, Eskay R, Parker SC, et al, (2010) Human NPY promoter variation rs16147:T˃C as a moderator of prefrontal NPY gene expression and negative effect. Hum Mutation 31: E1594-E1608. CrossRef Medline
43. Sotres-Bayon F, Bush DE, LeDoux JE (2004) Emotional perseveration: an update on prefrontal-amygdala interactions in fear extinction. Learn Mem 11:525-535. CrossRef Medline
44. Sotres-Bayon F, Diaz-Mataix L, Bush DE, LeDoux JE (2009) Dissociable roles for the ventromedial prefrontal cortex and amygdala in fear extinction: NR2B contribution. Cereb Cortex 19:474-482. CrossRef Medline
45. Spencer SJ, Buller KM, Day TA (2005) Medial prefrontal cortex control of the paraventricular hypothalamic nucleus response to psychological stress: possible role of the bed nucleus of the stria terminalis. J Comp Neurol 481:363-376. CrossRef Medline
46. Sun QQ, Baraban SC, Prince DA, Huguenard JR (2003) Target-specific neuropeptide Y-ergic synaptic inhibition and its network consequences within the mammalian thalamus. J Neurosci 23:9639-9649. Medline
47. Tu B, Timofeeva O, Jiao Y, Nadler JV (2005) Spontaneous release of neuropeptide Y tonically inhibits recurrent mossy fiber synaptic transmission in epileptic brain. J Neurosci 25:1718-1729. CrossRef Medline
48. Verma D, Tasan RO, Herzog H, Sperk G (2012) NPY controls fear conditioning and fear extinction by combined action on Y1 and Y2 receptors. Br. J Pharmacol 166:1461-1473. CrossRef Medline
49. Verma D, Wood J, Lach G, Mietzsch M, Weger S, Heilbronn R, Herzog H, Bonaventure P, Sperk G, Tasan RO (2015) NPY Y2 receptors in the central amygdala reduce cued but not contextual fear. Neuropharmacology 99:665-674. CrossRef Medline
50. Vythilingam M, Gill JM, Luckenbaugh DA, Gold PW, Collin C, Bonne O, Plumb K, Polignano E, West K, Charney D (2010) Low early morning plasma cortisol in posttraumatic stress disorder is associated with comorbid depression but not with enhanced glucocorticoid feedback inhibition. Psychoneuroendocrinology 35:442-450. CrossRef Medline
51. Wu G, Feder A, Wegener G, Bailey C, Saxena S, Charney D, Mathé AA (2011) Central functions of neuropeptide Y in mood and anxiety disorders. Expert Opin Ther Targets 15:1317-1331. CrossRef Medline
52. Wulsin AC, Herman JP, Solomon MB (2010) Mifepristone decreases depression-like behavior and modulates neuroendocrine and central hypothalamic-pituitary-adrenocortical axis responsiveness to stress. Psychoneuroendocriology 35:1100-1112. CrossRef Medline
53. Zhang H, Sakharkar AJ, Shi G, Ugale R, Prakash A, Pandey SC (2010) Neuropeptide Y signaling in the central nucleus of the amygdala regulates alcohol-drinking and anxiety-like behaviors of alcohol-preferring rats. Alcohol Clin Exp Res 34:451-461. CrossRef Medline
54. Zhou Z, Zhu G, Hariri AR, Enoch MA, Scott D, Sinha R, Virkkunen M, Mash DC, Lipsky RH, Hu XZ, Hodgkinson CA, Xu K, Buzas B, Yuan Q, Shen PH, Ferrell RE, Manuck SB, Brown SM, Hauger RL, Stohler CS, Zubieta JK, Goldman D (2008) Genetic variation in human NPY expression affects stress response and emotion. Nature 452:997-1001. CrossRef Medline