Oxytocin signaling in basolateral and central amygdala nuclei differentially regulates the acquisition, expression, and extinction of context-conditioned fear in rats

Learning and Memory

Volumn 22, Issue 5, 2015, Pages 247-257

  Campbell Smith, Emma J ^a   Holmes, Nathan M ^a   Lingawi, Nura W ^a   Panayi, Marios C ^a   Westbrook, R Frederick ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

OXYTOCIN; OXYTOCIN ANTAGONIST; OXYTOCIN RECEPTOR; OXYTOCIN, TRI-GLY-;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVERSIVE BEHAVIOR; BASOLATERAL AMYGDALA; CONTROLLED STUDY; FEAR; FREEZING; LEARNING; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; AMYGDALA; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; ASSOCIATION; CATALEPSY; CONDITIONED REFLEX; DRUG EFFECTS; ELECTRIC SHOCK; METABOLISM; PHYSIOLOGY; REINFORCEMENT;

AMYGDALA; ANIMALS; CONDITIONING, CLASSICAL; CUES; ELECTROSHOCK; EXTINCTION, PSYCHOLOGICAL; FEAR; FREEZING REACTION, CATALEPTIC; MALE; OXYTOCIN; RATS; RECEPTORS, OXYTOCIN; SIGNAL TRANSDUCTION;

EID: 84929616777     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.036962.114     Document Type: Article

References (45)

1. Amir A, Amano T, Pare D. 2011. Physiological identification and infralimbic responsiveness of rat intercalated amygdala neurons. J Neurophysiol 105: 3054-3066.
2. Bale TL, Davis AM, Auger AP, Dorsa DM, McCarthy MM. 2001. CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior. J Neurosci 21: 2546-2552.
3. Bartz JA, Zaki J, Ochsner KN, Bolger N, Kolevzon A, Ludwig N, Lydon JE. 2010. Effects of oxytocin on recollections of maternal care and closeness. Proc Natl Acad Sci 107: 21371-21375.
4. Bartz JA, Zaki J, Bolger N, Ochsner KN. 2011. Social effects of oxytocin in humans: context and person matter. Trends Cogn Sci 15: 301-309.
5. Betz MA, Gabriel KR. 1978. Type IV errors and analysis of simple effects. J Educ Stat 3: 121-143.
6. Betz MA, Levin JR. 1982. Coherent analysis-of-variance hypothesis testing strategies: a general approach. J Educ Stat 7: 193-206.
7. Bird KD. 2004. Analysis of variance via confidence intervals. Sage Publications, London.
8. Carrive P, Lee J, Su A. 2000. Lidocaine blockade of amygdala output in fear-conditioned rats reduces Fos expression in the ventrolateral periaqueductal gray. Neuroscience 95: 1071-1080.
9. Ciocchi S, Herry C, Grenier F, Wolff SB, Letzkus JJ, Vlachos I, Ehrlich I, Sprengel R, Deisseroth K, Stadler MB, et al. 2010. Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468: 277-282.
10. Domes G, Heinrichs M, Gläscher J, Büchel C, Braus DF, Herpertz SC. 2007. Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol Psychiatry 62: 1187-1190.
11. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Lüthi A. 2009. Amygdala inhibitory circuits and the control of fear memory. Neuron 62: 757-771.
12. Fanselow MS. 1980. Conditioned and unconditional components of post-shock freezing. Pavlov J Biol Sci 15: 177-182.
13. Fanselow MS. 1986. Conditioned fear-induced opiate analgesia: a competing motivational state theory of stress analgesia. Ann N Y Acad Sci 467: 40-54.
14. Frank E, Landgraf R. 2008. The vasopressin system-from antidiuresis to psychopathology. Eur J Pharmacol 583: 226-242.
15. Gozzi A, Jain A, Giovannelli A, Bertollini C, Crestan V, Schwarz AJ, Tsetsenis T, Ragozzino D, Gross CT, Bifone A. 2010. A neural switch for active and passive fear. Neuron 67: 656-666.
16. HaubensakW, Kunwar PS, Cai H, Ciocchi S, Wall NR, Ponnusamy R, Biag J, DongHW, Deisseroth K, Callaway EM, et al. 2010. Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 468: 270-276.
17. Hays WL. 1963. Statistics for psychologists. Holt, Rinehart and Winston, New York.
18. Herry C, Ciocchi S, Senn V, Demmou L, Müller C, Lüthi A. 2008. Switching on and off fear by distinct neuronal circuits. Nature 454: 600-606.
19. Huber D, Veinante P, Stoop R. 2005. Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science 308: 245-248.
20. Huff NC, Wright-Hardesty KJ, Higgins EA, Matus-Amat P, Rudy JW. 2005. Context pre-exposure obscures amygdala modulation of contextual-fear conditioning. Learn Mem 12: 456-460.
21. Insel TR. 2010. The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65: 768-779.
22. Kiernan MJ, Westbrook RF. 1993. Effects of exposure to a to-be-shocked environment upon the rat's freezing response: Evidence for facilitation, latent inhibition and perceptual learning. Q J Exp Psychol B 46: 271-288.
23. Kirsch P, Esslinger C, Chen Q, Mier D, Lis S, Siddhanti S, Gruppe H, Mattay VS, Gallhofer B, Meyer-Lindenberg A. 2005. Oxytocin modulates neural circuitry for social cognition and fear in humans. J Neurosci 25: 11489-11493.
24. Knobloch HS, Charlet A, Hoffmann LC, Eliava M, Khrulev S, Cetin AH, Osten P, Schwarz MK, Seeburg PH, Stoop R, et al. 2012. Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73: 553-566.
25. Kremarik P, Freund-Mercier MJ, Stoeckel ME. 1993. Histoautoradiographic detection of oxytocin- and vasopressin-binding sites in the telencephalon of the rat. J Comp Neurol 333: 343-359.
26. Lahoud N, Maroun M. 2013. Oxytocinergic manipulations in corticolimbic circuit differentially affect fear acquisition and extinction. Psychoneuroendocrinology 38: 2184-2195.
27. LeDoux J. 2007. The amygdala. Curr Biol 17: R868-R874.
28. Lee HJ, Macbeth AH, Pagani JH, Young WS III. 2009. Oxytocin: the great facilitator of life. Prog Neurobiol 88: 127-151.
29. Lee S, Kim SJ, Kwon OB, Lee JH, Kim JH. 2013. Inhibitory networks of the amygdala for emotional memory. Front Neural Circuits 7: 129.
30. Likhtik E, Popa D, Apergis-Schoute J, Fidacaro GA, Paré D. 2008. Amygdala intercalated neurons are required for expression of fear extinction. Nature 454: 642-645.
31. McCarthy MM, McDonald CH, Brooks PJ, Goldman D. 1996. An anxiolytic action of oxytocin is enhanced by estrogen in the mouse. Physiol Behav 60: 1209-1215.
32. Muller J, Corodimas KP, Fridel Z, LeDoux JE. 1997. Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to an explicit conditioned stimulus and to contextual stimuli. Behav Neurosci 111: 683-691.
33. Neumann ID. 2008. Brain oxytocin: a key regulator of emotional and social behaviours in both females and males. J Neuroendocrinol 20: 858-865.
34. Neumann ID, Landgraf R. 2012. Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci 35: 649-659.
35. Pape HC, Pare D. 2010. Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 90: 419-463.
36. Paxinos G, Watson C. 1997. The rat brain in stereotaxic coordinates, 3rd ed. Academic Press, San Diego.
37. Penzo MA, Robert V, Li B. 2014. Fear conditioning potentiates synaptic transmission onto long-range projection neurons in the lateral subdivision of central amygdala. J Neurosci 34: 2432-2437.
38. Petrovic P, Kalisch R, Singer T, Dolan RJ. 2008. Oxytocin attenuates affective evaluations of conditioned faces and amygdala activity. J Neurosci 28: 6607-6615.
39. Sah P, Westbrook RF, Lüthi A. 2008. Fear conditioning and long-term potentiation in the amygdala: what really is the connection? Ann N Y Acad Sci 1129: 88-95.
40. Stoop R. 2012. Neuromodulation by oxytocin and vasopressin. Neuron 76: 142-159.
41. Terenzi MG, Ingram CD. 2005. Oxytocin-induced excitation of neurones in the rat central and medial amygdaloid nuclei. Neuroscience 134: 345-354.
42. Toth I, Neumann ID, Slattery DA. 2012. Central administration of oxytocin receptor ligands affects cued fear extinction in rats and mice in a timepoint-dependent manner. Psychopharmacology (Berl) 223: 149-158.
43. Viviani D, Charlet A, van den Burg E, Robinet C, Hurni N, Abatis M, Magara F, Stoop R. 2011. Oxytocin selectively gates fear responses through distinct outputs from the central amygdala. Science 333: 104-107.
44. Wilensky AE, Schafe GE, Kristensen MP, LeDoux JE. 2006. Rethinking the fear circuit: the central nucleus of the amygdala is required for the acquisition, consolidation, and expression of Pavlovian fear conditioning. J Neurosci 26: 12387-12396.
45. Zoicas I, Slattery DA, Neumann ID. 2014. Brain oxytocin in social fear conditioning and its extinction: involvement of the lateral septum. Neuropsychopharmacology 39: 3027-3035.