Role of bed nucleus of the stria terminalis and amygdala AMPA receptors in the development and expression of context conditioning and sensitization of startle by prior shock

Brain Structure and Function

Volumn 219, Issue 6, 2014, Pages 1969-1982

  Davis, Michael ^a   Walker, David L ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AMPA; Amygdala; Anxiety; Bed nucleus of the stria terminalis; Fear; Hyperarousal; Sensitization; Startle

Indexed keywords

6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; AMPA RECEPTOR; 2,3-DIOXO-6-NITRO-7-SULFAMOYLBENZO(F)QUINOXALINE; QUINOXALINE DERIVATIVE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR COMMISSURE; ARTICLE; BASOLATERAL AMYGDALA; CAPSULA INTERNA; CONTROLLED STUDY; FEAR; FEAR CONDITIONING TEST; FOOTSHOCK; LOW FREQUENCY NOISE; MALE; NERVE CELL; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSITIZATION; SHOCK; STARTLE REFLEX; STRIA TERMINALIS; ANIMAL; ANTAGONISTS AND INHIBITORS; CONDITIONED REFLEX; DRUG EFFECTS; ELECTROSTIMULATION; PHYSIOLOGY; SEPTUM NUCLEUS; SPRAGUE DAWLEY RAT;

AMYGDALA; ANIMALS; CONDITIONING, CLASSICAL; ELECTRIC STIMULATION; FEAR; MALE; QUINOXALINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; REFLEX, STARTLE; SEPTAL NUCLEI;

EID: 84936127236     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-013-0616-5     Document Type: Article

References (86)

1. Adamec RE, Burton P, Shallow T, Budgell J (1999) Unilateral block of NMDA receptors in the amygdala prevents predator stress-induced lasting increases in anxiety-like behavior and unconditioned startle–effective hemisphere depends on the behavior. Physiol Behav 65(4–5):739–751
2. Alheid GF, Heimer L (1988) New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27(1):1–39
3. Alheid G, De Olmos JS, Beltramino CA (1995) Amygdala and extended amygdala. In: Paxinos G (ed) The rat nervous system. Academic Press, New York, pp 495–578
4. Arluison M, Brochier G, Vankova M, Leviel V, Villalobos J, Tramu G (1994) Demonstration of peptidergic afferents to the bed nucleus of the stria terminalis using local injections of colchicine. A combined immunohistochemical and retrograde tracing study. Brain Res Bull 34:319–337
5. Brownstein M, Saavedra MM, Palkovits M (1974) Norepinephrine and dopamine in the limbic system of the rat. Brain Res 79:431–436
6. Bruijnzeel AW, Stam R, Wiegant VM (2001) LY354740 attenuates the expression of long-term behavioral sensitization induced by a single session of footshocks. Eur J Pharmacol 426:77–80
7. Christianson JP, Jennings JH, Ragole T, Flyer JG, Benison AM, Barth DS, Watkins LR, Maier SF (2011) Safety signals mitigate the consequences of uncontrollable stress via a circuit involving the sensory insular cortex and bed nucleus of the stria terminalis. Biol Psychiatry 70(5):458–464. doi:10.1016/j.biopsych.2011.04.004
8. Ciccocioppo R, Fedeli A, Economidou D, Policani F, Weiss F, Massi M (2003) The bed nucleus is a neuroanatomical substrate for the anorectic effect of corticotropin-releasing factor and for its reversal by nociceptin/orphanin FQ. J Neurosci 23(28):9445–9451
9. Davis M, Walker DL, Miles L, Grillon C (2010) Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 35(1):105–135. doi:10.1038/npp.2009.109
10. de Olmos JS, Heimer L (1999) The concepts of the ventral striatopallidal system and extended amygdala. Ann N Y Acad Sci 877:1–32
11. Deyama S, Katayama T, Ohno A, Nakagawa T, Kaneko S, Yamaguchi T, Yoshioka M, Minami M (2008) Activation of the ß-adrenoceptor-protein kinase A signaling pathway within the ventral bed nucleus of the stria terminalis mediates the negative affective component of pain in rats. J Neurosci 28(31):7728–7736.
12. Deyama S, Katayama T, Kondoh N, Nakagawa T, Kaneko S, Yamaguchi T, Yoshioka M, Minami M (2009) Role of enhanced noradrenergic transmission within the ventral bed nucleus of the stria terminalis in visceral pain-induced aversion in rats. Behav Brain Res 197(2):279–283. doi:10.1016/j.bbr.2008.08.024
13. Dong HW, Petrovich GD, Swanson LW (2001) Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res Brain Res Rev 38(1–2):192–246
14. Fanselow M, LeDoux J (1999) Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 23:229–232
15. Fendt M, Siegl S, Steiniger-Brach B (2005) Noradrenaline transmission within the ventral bed nucleus of the stria terminalis is critical for fear behavior induced by trimethylthiazoline, a component of fox odor. J Neurosci 25(25):5998–6004
16. Gale GD, Anagnostaras SG, Godsil BP, Mitchell S, Nozawa T, Sage JR, Wiltgen B, Fanselow MS (2004) Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. J Neurosci 24(15):3810–3815
17. Garrick T, Morrow N, Shalev AY, Eth S (2001) Stress-induced enhancement of auditory startle: an animal model of posttraumatic stress disorder. Psychiatry 64(4):346–354
18. Gewirtz JC, McNish KA, Davis M (1998) Lesions of the bed nucleus of the stria terminalis block sensitization of the acoustic startle reflex produced by repeated stress, but not fear-potentiated startle. Prog Neuropsychopharmacol Biol Psychiatry 22:625–648
19. Goldstein G, van Kammen W, Shelly C, Miller DJ, van Kammen DP (1987) Survivors of imprisonment in the Pacific theater during World War II. Am J Psychiatry 144(9):1210–1213
20. Golub Y, Mauch CP, Dahlhoff M, Wotjak CT (2009) Consequences of extinction training on associative and non-associative fear in a mouse model of Posttraumatic Stress Disorder (PTSD). Behav Brain Res 205(2):544–549. doi:10.1016/j.bbr.2009.08.019
21. Gray TS, Magnuson DJ (1992) Peptide immunoreactive neurons in the amygdala and the bed nucleus of the stria terminalis project to the midbrain central gray in the rat. Peptides 13(3):451–460
22. Greenberg BD, Gabriels LA, Malone DA Jr, Rezai AR, Friehs GM, Okun MS, Shapira NA, Foote KD, Cosyns PR, Kubu CS, Malloy PF, Salloway SP, Giftakis JE, Rise MT, Machado AG, Baker KB, Stypulkowski PH, Goodman WK, Rasmussen SA, Nuttin BJ (2010) Deep brain stimulation of the ventral internal capsule/ventral striatum for obsessive-compulsive disorder: worldwide experience. Mol Psychiatry 15(1):64–79. doi:10.1038/mp.2008.55
23. Grillon C, Cordova J, Levine LR, Morgan CA 3rd (2003) Anxiolytic effects of a novel group II metabotropic glutamate receptor agonist (LY354740) in the fear-potentiated startle paradigm in humans. Psychopharmacology 168(4):446–454
24. Grueter BA, Winder DG (2005) Group II and III metabotropic glutamate receptors suppress excitatory synaptic transmission in the dorsolateral bed nucleus of the stria terminalis. Neuropsychopharmacology 30(7):1302–1311
25. Hammack SE, Cheung J, Rhodes KM, Schutz KC, Falls WA, Braas KM, May V (2009) Chronic stress increases pituitary adenylate cyclase-activating peptide (PACAP) and brain-derived neurotrophic factor (BDNF) mRNA expression in the bed nucleus of the stria terminalis (BNST): roles for PACAP in anxiety-like behavior. Psychoneuroendocrinology 34(6):833–843. doi:10.1016/j.psyneuen.2008.12.013
26. Hammack SE, Roman CW, Lezak KR, Kocho-Shellenberg M, Grimmig B, Falls WA, Braas K, May V (2010) Roles for pituitary adenylate cyclase-activating peptide (PACAP) expression and signaling in the bed nucleus of the stria terminalis (BNST) in mediating the behavioral consequences of chronic stress. J Mol Neurosci 42(3):327–340. doi:10.1007/s12031-010-9364-7
27. Hazra R, Guo JD, Dabrowska J, Rainnie DG (2012) Differential distribution of serotonin receptor subtypes in BNST(ALG) neurons: modulation by unpredictable shock stress. Neuroscience 225:9–21. doi:10.1016/j.neuroscience.2012.08.014
28. Helton DR, Tizzano JP, Monn JA, Schoepp DD, Kallman MJ (1998) Anxiolytic and side-effect profile of LY354740: a potent, highly selective, orally active agonist for group II metabotropic glutamate receptors. J Pharmacol Exp Ther 284(2):651–660
29. Hott SC, Gomes FV, Fabri DR, Reis DG, Crestani CC, Correa FM, Resstel LB (2012) Both alpha1- and beta1-adrenoceptors in the bed nucleus of the stria terminalis are involved in the expression of conditioned contextual fear. Br J Pharmacol 167(1):207–221. doi:10.1111/j.1476-5381.2012.01985.x
30. Hughes KC, Shin LM (2011) Functional neuroimaging studies of post-traumatic stress disorder. Expert Rev Neurother 11(2):275–285. doi:10.1586/ern.10.198
31. Ju G, Swanson LW, Simerly RB (1989) Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat: II. Chemoarchitecture. J Comp Neurol 280(4):603–621
32. Kamprath K, Wotjak CT (2004) Nonassociative learning processes determine expression and extinction of conditioned fear in mice. Learn Mem 11:770–786
33. Kilts C, Anderson C (1986) The simultaneous quantification of dopamine, norepinephrine and epinephrine in micropunched rat brain nuclei by on-line trace enrichment HPLC with electro-chemical detection distribution of catecholamines in the limbic system. Neurochem Int 9:437–455
34. Kim M, Davis M (1993) Lack of a temporal gradient of retrograde amnesia in rats with amygdala lesions assessed with the fear-potentiated startle paradigm. Behav Neurosci 107:1088–1092
35. Koenigs M, Huey ED, Raymont V, Cheon B, Solomon J, Wassermann EM, Grafman J (2008) Focal brain damage protects against post-traumatic stress disorder in combat veterans. Nat Neurosci 11(2):232–237. doi:10.1038/nn2032
36. Kumar R (1970) Incubation of fear: experiments of the “Kamin Effect” in rats. J Comp Physiol Psychol 70(2):258–263
37. Leaton RN (1981) Habituation of startle response, lick suppression, and exploratory behavior in rats with hippocampal lesions. J Comp Physiol Psychol 95(5):813–826
38. Lebow M, Neufeld-Cohen A, Kuperman Y, Tsoory M, Gil S, Chen A (2012) Susceptibility to PTSD-like behavior is mediated by corticotropin-releasing factor receptor type 2 levels in the bed nucleus of the stria terminalis. J Neurosci 32(20):6906–6916. doi:10.1523/JNEUROSCI.4012-11.2012
39. Lee Y, Davis M (1997) Role of the hippocampus, bed nucleus of the stria terminalis and amygdala in the excitatory effect of corticotropin releasing hormone on the acoustic startle reflex. J Neurosci 17:6434–6446
40. Lee Y, Walker D, Davis M (1996) Lack of a temporal gradient of retrograde amnesia following NMDA-induced lesions of the basolateral amygdala assessed with the fear-potentiated startle paradigm. Behav Neurosci 110(4):836–839
41. Lee Y, Fitz S, Johnson PL, Shekhar A (2008) Repeated stimulation of CRF receptors in the BNST of rats selectively induces social but not panic-like anxiety. Neuropsychopharmacology 33:2586–2594
42. Luyten L, van Kuyck K, Vansteenwegen D, Nuttin B (2011) Electrolytic lesions of the bed nucleus of the stria terminalis disrupt freezing and startle potentiation in a conditioned context. Behav Brain Res 222(2):357–362. doi:10.1016/j.bbr.2011.03.066
43. Mahan AL, Ressler KJ (2012) Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci 35(1):24–35. doi:10.1016/j.tins.2011.06.007
44. Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897–931. doi:10.1146/annurev.neuro.24.1.897
45. Maren S, Aharonov G, Fanselow MS (1996) Retrograde abolition of conditional fear after excitotoxic lesions in the basolateral amygdala of rats: absence of a temporal gradient. Behav Neurosci 110(4):718–726
46. Marlin NA, Miller RR (1981) Associations to contextual stimuli as a determinant of long-term habituation. J Exp Psychol Anim Behav Process 7(4):313–333
47. Marshall GN, Schell TL, Glynn SM, Shetty V (2006) The role of hyperarousal in the manifestation of posttraumatic psychological distress following injury. J Abnorm Psychol 115(3):624–628. doi:10.1037/0021-843X.115.3.624
48. Morilak DA, Cecchi M, Khoshbouei H (2003) Interactions of norepinephrine and galanin in the central amygdala and lateral bed nucleus of the stria terminalis modulate the behavioral response to acute stress. Life Sci 73(6):715–726
49. Muly EC, Mania I, Guo JD, Rainnie DG (2007) Group II metabotropic glutamate receptors in anxiety circuitry: correspondence of physiological response and subcellular distribution. J Comp Neurol 505(6):682–700
50. Pamplona FA, Henes K, Micale V, Mauch CP, Takahashi RN, Wotjak CT (2011) Prolonged fear incubation leads to generalized avoidance behavior in mice. J Psychiatr Res 45(3):354–360. doi:10.1016/j.jpsychires.2010.06.015
51. Pego JM, Morgado P, Pinto LG, Cerqueira JJ, Almeida OF, Sousa N (2008) Dissociation of the morphological correlates of stress-induced anxiety and fear. Eur J Neurosci 27(6):1503–1516
52. Pickens CL, Golden SA, Adams-Deutsch T, Nair SG, Shaham Y (2009) Long-lasting incubation of conditioned fear in rats. Biol Psychiatry 65(10):881–886. doi:10.1016/j.biopsych.2008.12.010
53. Pitman RK, Orr SP, Shalev AY (1993) Once bitten, twice shy: beyond the conditioning model of PTSD. Biol Psychiatry 33(3):145–146
54. Poulos AM, Ponnusamy R, Dong HW, Fanselow MS (2010) Compensation in the neural circuitry of fear conditioning awakens learning circuits in the bed nuclei of the stria terminalis. Proc Natl Acad Sci USA 107(33):14881–14886. doi:10.1073/pnas.1005754107
55. Rauch SL, Shin LM, Phelps EA (2006) Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research–past, present, and future. Biol Psychiatry 60(4):376–382. doi:10.1016/j.biopsych.2006.06.004
56. Resstel LB, Alves FH, Reis DG, Crestani CC, Correa FM, Guimaraes FS (2008) Anxiolytic-like effects induced by acute reversible inactivation of the bed nucleus of stria terminalis. Neuroscience 154:869–876
57. Riccio DC, Ackil J, Burch-Vernon A (1992) Forgetting of stimulus attributes: methodological implications for assessing associative phenomena. Psychol Bull 112(3):433–445
58. Sahuque LL, Kullberg EF, McGeehan AJ, Kinder JR, Hicks MP, Blanton MG, Janak PH, Olive MF (2006) Anxiogenic and aversive effects of corticotropin-releasing factor (CRF) in the bed nucleus of the stria terminalis in the rat: role of CRF receptor subtypes. Psychopharmacology 186:122–132
59. Santibanez M, Gysling K, Forray MI (2006) Desipramine prevents the sustained increase in corticotropin-releasing hormone-like immunoreactivity induced by repeated immobilization stress in the rat central extended amygdala. J Neurosci Res 84(6):1270–1281
60. Sauerhofer E, Pamplona FA, Bedenk B, Moll GH, Dawirs RR, von Horsten S, Wotjak CT, Golub Y (2012) Generalization of contextual fear depends on associative rather than non-associative memory components. Behav Brain Res 233(2):483–493. doi:10.1016/j.bbr.2012.05.016
61. Schell TL, Marshall GN, Jaycox LH (2004) All symptoms are not created equal: the prominent role of hyperarousal in the natural course of posttraumatic psychological distress. J Abnorm Psychol 113(2):189–197
62. Schoepp DD, Wright RA, Levine LR, Gaydos B, Potter WZ (2003) LY354740, an mGlu2/3 receptor agonist as a novel approach to treat anxiety/stress. Stress 6(3):189–197
63. Schreurs BG, Smith-Bell CA, Burhans LB (2011) Incubation of conditioning-specific reflex modification: implications for Post Traumatic Stress Disorder. J Psychiatr Res 45(11):1535–1541. doi:10.1016/j.jpsychires.2011.07.003
64. Schweimer J, Fendt M, Schnitzler HU (2005) Effects of clonidine injections into the bed nucleus of the stria terminalis on fear and anxiety behavior in rats. Eur J Pharmacol 507(1–3):117–124
65. Servatius RJ, Ottenweller JE, Natelson BH (1995) Delayed startle sensitization distinguishes rats exposed to one or three stress sessions: further evidence toward an animal model of PTSD. Biol Psychiatry 38(8):539–546. doi:10.1016/0006-3223(94)00369-E
66. Shalev AY, Ragel-Fuchs Y, Pitman RK (1992) Conditioned fear and psychological trauma. Biol Psychiatry 31(9):863–865
67. Shalev AY, Peri T, Brandes D, Freedman S, Orr SP, Pitman RK (2000) Auditory startle response in trauma survivors with posttraumatic stress disorder: a prospective study. Am J Psychiatry 157(2):255–261
68. Shimada S, Inagaki S, Kubota Y, Kito S, Funaki H, Takagi H (1989a) Light and electron microscopic studies of calcitonin gene-related peptide-like immunoreactive terminals in the central nucleus of the amygdala and the bed nucleus of the stria terminalis of the rat. Exp Brain Res 77(1):217–220
69. Shimada S, Inagaki S, Kubota Y, Ogawa N, Shibasaki T, Takagi H (1989b) Coexistence of peptides (corticotropin releasing factor/neurotensin and substance P/somatostatin) in the bed nucleus of the stria terminalis and central amygdaloid nucleus of the rat. Neuroscience 30(2):377–383
70. Siegmund A, Wotjak CT (2007) Hyperarousal does not depend on trauma-related contextual memory in an animal model of Posttraumatic Stress Disorder. Physiol Behav 90(1):103–107. doi:10.1016/j.physbeh.2006.08.032
71. Sink KS, Walker DL, Yang Y, Davis M (2011) Calcitonin gene-related peptide in the bed nucleus of the stria terminalis produces an anxiety-like pattern of behavior and increases neural activation in anxiety-related structures. J Neurosci 31(5):1802–1810. doi:10.1523/JNEUROSCI.5274-10.2011
72. Sink KS, Chung A, Ressler KJ, Davis M, Walker DL (2013) Anxiogenic effects of CGRP within the BNST may be mediated by CRF acting at BNST CRFR1 receptors. Behav Brain Res 243:286–293. doi:10.1016/j.bbr.2013.01.024
73. Stam R (2007a) PTSD and stress sensitisation: a tale of brain and body Part 1: human studies. Neurosci Biobehav Rev 31(4):530–557
74. Stam R (2007b) PTSD and stress sensitisation: a tale of brain and body Part 2: animal models. Neurosci Biobehav Rev 31(4):558–584
75. Sullivan GM, Apergis J, Bush DE, Johnson LR, Hou M, Ledoux JE (2004) Lesions in the bed nucleus of the stria terminalis disrupt corticosterone and freezing responses elicited by a contextual but not by a specific cue-conditioned fear stimulus. Neuroscience 128(1):7–14
76. Vyas A, Bernal S, Chattarji S (2003) Effects of chronic stress on dendritic arborization in the central and extended amygdala. Brain Res 965(1–2):290–294
77. Walker DL, Davis M (1997) Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in light-enhanced versus fear-potentiated startle. J Neurosci 17:9375–9383
78. Walker DL, Davis M (2002) Quantifying fear potentiated startle using absolute versus percent increase scoring methods: implications for the neurocircuitry of fear and anxiety. Psychopharmacology 164:318–328
79. Walker DL, Davis M (2005) BNST mediation of long-lasting stress-induced sensitization of the acoustic startle response. Program# 70.8. Neuroscience 2005 Abstracts. Washington, DC: Society for Neuroscience. Online
80. Walker DL, Rattiner LM, Davis M (2002) Group II metabotropic glutamate receptors within the amygdala regulate fear as assessed with potentiated startle in rats. Behav Neurosci 116(6):1075–1083
81. Walker DL, Paschall GY, Davis M (2005) Glutamate receptor antagonist infusions into the basolateral and medial amygdala reveal differential contributions to olfactory vs. context fear conditioning and expression. Learn Mem 12(2):120–129. doi:10.1101/lm.87105
82. Walker DL, Miles LA, Davis M (2009) Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxiety-like versus phasic fear-like responses. Prog Neuropsychopharmacol Biol Psychiatry 33(8):1291–1308
83. Walter A, Mai JK, Lanta L, Gorcs T (1991) Differential distribution of immunohistochemical markers in the bed nucleus of the stria terminalis in the human brain. J Chem Neuroanat 4(4):281–298
84. Woodhams PL, Roberts GW, Polak JM, Crow TJ (1983) Distribution of neuropeptides in the limbic system of the rat: the bed nucleus of the stria terminalis, septum and preoptic area. Neuroscience 8(4):677–703
85. Zhao Z, Davis M (2004) Fear-potentiated startle in rats is mediated by neurons in the deep layers of the superior colliculus/deep mesencephalic nucleus of the rostral midbrain through the glutamate non-NMDA receptors. J Neurosci 24:10326–10334
86. Zimmerman JM, Maren S (2011) The bed nucleus of the stria terminalis is required for the expression of contextual but not auditory freezing in rats with basolateral amygdala lesions. Neurobiol Learn Mem 95(2):199–205. doi:10.1016/j.nlm.2010.11.002