Corticotropin-releasing hormone receptors in the medial prefrontal cortex regulate hypothalamic-pituitary-adrenal activity and anxiety-related behavior regardless of prior stress experience

Brain Research

Volumn 1186, Issue 1, 2007, Pages 212-223

  Jaferi, Azra ^a   Bhatnagar, Seema ^b,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

ACTH; Anxiety; Corticosterone; Corticotropin releasing hormone; Prefrontal cortex; Restraint

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR ANTAGONIST; CORTICOTROPIN RELEASING FACTOR RECEPTOR; DEXTRO PHENYL CORTICOTROPIN RELEASING HORMONE; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DRUG EFFECT; HABITUATION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LIMBIC CORTEX; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; STRESS;

ADAPTATION, PHYSIOLOGICAL; ADRENOCORTICOTROPIC HORMONE; ANIMALS; ANXIETY; ASSOCIATION LEARNING; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; HABITUATION, PSYCHOPHYSIOLOGIC; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; PITUITARY-ADRENAL SYSTEM; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; STRESS, PSYCHOLOGICAL;

ANIMALIA;

EID: 37649019314     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.07.100     Document Type: Article

References (100)

1. Adamec R.E., and McKay D. Amygdala kindling, anxiety, and corticotrophin releasing factor (CRF). Physiol. Behav. 54 3 (1993) 423-431
2. Akana S.F., Hanson E.S., Horsley C.J., Strack A.M., Bhatnagar S., Bradbury M.J., Milligan E.D., and Dallman M.F. Clamped corticosterone (B) reveals the effect of endogenous B on both facilitated responsivity to acute restraint and metabolic responses to chronic stress. Stress 1 1 (1996) 33-49
3. Akana S.F., Chu A., Soriano L., and Dallman M.F. Corticosterone exerts site-specific and state-dependent effects in prefrontal cortex and amygdala on regulation of adrenocorticotropic hormone, insulin and fat depots. J. Neuroendocrinol. 13 7 (2001) 627-637
4. Amat J., Baratta M.V., Paul E., Bland S.T., Watkins L.R., and Maier S.F. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat. Neurosci. 8 3 (2005) 365-371
5. Bagley, and Moghaddam. Temporal dynamics of glutamate efflux in the prefrontal cortex and in the hippocampus following repeated stress: effects of pretreatment with saline or diazepam. Neuroscience 77 1 (1997) 65-73
6. Bakshi V.P., Smith-Roe S., Newman S.M., Grigoriadis D.E., and Kalin N.H. Reduction of stress-induced behavior by antagonism of corticotropin-releasing hormone 2 (CRH2) receptors in lateral septum or CRH1 receptors in amygdala. J. Neurosci. 22 7 (2002) 2926-2935
7. Baldwin H.A., Rassnick S., Rivier J., Koob G.F., and Britton K.T. CRF antagonist reverses the "anxiogenic" response to ethanol withdrawal in the rat. Psychopharmacology (Berl.) 103 2 (1991) 227-232
8. Baldwin A.E., Sadeghian K., and Kelley A.E. Appetitive instrumental learning requires coincident activation of NMDA and dopamine D1 receptors within the medial prefrontal cortex. J. Neurosci. 22 3 (2002) 1063-1071
9. Bale T.L., and Vale W.W. CRF and CRF receptors: role in stress responsivity and other behaviors. Annu. Rev. Pharmacol. Toxicol. 44 (2004) 525-557
10. Bhatnagar S., and Dallman M.F. Neuroanatomical basis for facilitation of hypothalamic-pituitary-adrenal responses to a novel stressor after chronic stress. Neuroscience 84 4 (1998) 1025-1039
11. Bhatnagar S., and Meaney M.J. Hypothalamic-pituitary-adrenal function in chronic intermittently cold-stressed neonatally handled and non handled rats. J. Neuroendocrinol. 7 (1995) 97-108
12. Bhatnagar S., Viau V., Chu A., Soriano L., Meijer O.C., and Dallman M.F. A cholecystokinin-mediated pathway to the paraventricular thalamus is recruited in chronically stressed rats and regulates hypothalamic-pituitary-adrenal function. J. Neurosci. 20 14 (2000) 5564-5573
13. Bhatnagar S., Huber R., Nowak N., and Trotter P. Lesions of the posterior paraventricular thalamus block habituation of hypothalamic-pituitary-adrenal responses to repeated restraint. J. Neuroendocrinol. 14 (2002) 403-410
14. Bhatnagar S., Huber R., Lazar E., Pych L., and Vining C. Chronic stress alters behavior in the conditioned defensive burying test: role of the posterior paraventricular thalamus. Pharmacol. Biochem. Behav. 76 2 (2003) 343-349
15. Birrell J.M., and Brown V.J. Medial frontal cortex mediates perceptual attentional set shifting in the rat. J. Neurosci. 20 11 (2000) 4320-4324
16. Bruuijnzeel A.W., Stam R., and Wiegant V.M. Effect of a benzodiazepine receptor agonist and corticotropin-releasing hormone receptor antagonists on long-term foot-shock-induced increase in defensive withdrawal behavior. Psychopharmacology (Berl.) 158 2 (2001) 132-139
17. Calvo N., and Volosin M. Glucocorticoid and mineralocorticoid receptors are involved in the facilitation of anxiety-like response induced by restraint. Neuroendocrinology 73 4 (2001) 261-271
18. Capriles N., Rodaros D., Sorge R.E., and Stewart J. A role for the prefrontal cortex in stress- and cocaine-induced reinstatement of cocaine seeking in rats. Psychopharmacology 168 1-2 (2003) 66-74
19. Chadda R., and Devaud L.L. Differential effects of mild repeated restraint stress on behaviors and GABA(A) receptors in male and female rats. Pharmacol. Biochem. Behav. 81 4 (2005) 854-863
20. Chalmers D.T., Lovenberg T.W., and De Souza E.B. Localization of novel corticotropin-releasing factor receptor (CRF2) mRNA expression to specific subcortical nuclei in rat brain: comparison with CRF1 receptor mRNA expression. J. Neurosci. 15 10 (1995) 6340-6350
21. Conde F., Maire-Lepoivre E., Audinat E., and Crepel F. Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents. J. Comp. Neurol. 352 4 (1995) 567-593
22. Crane J.W., Ebner K., and Day T.A. Medial prefrontal cortex suppression of the hypothalamic-pituitary-adrenal axis response to a physical stressor, systemic delivery of interleukin-1beta. Eur. J. Neurosci. 17 7 (2003) 1473-1481
23. Crawley J.N., Olschowka J.A., Diz D.I., and Jacobowitz D.M. Behavioral investigation of the coexistence of substance P, corticotropin releasing factor, and acetylcholinesterase in lateral dorsal tegmental neurons projecting to the medial frontal cortex of the rat. Peptides 6 5 (1985) 891-901
24. Cullinan W.E., Helmreich D.L., and Watson S.J. Fos expression in forebrain afferents to the hypothalamic paraventricular nucleus following swim stress. J. Comp. Neurol. 368 1 (1996) 88-99
25. Dalley J.W., Theobald D.E., Bouger P., Chudasama Y., Cardinal R.N., and Robbins T.W. Cortical cholinergic function and deficits in visual attentional performance in rats following 192 IgG-saporin-induced lesions of the medial prefrontal cortex. Cereb. Cortex 14 8 (2004) 922-932
26. Daniels W.M., Richter L., and Stein D.J. The effects of repeated intra-amygdala CRF injections on rat behavior and HPA axis function after stress. Metab. Brain Dis. 19 1-2 (2004) 15-23
27. Deak T., Nguyen K.T., Ehrlich A., Watkins L., Spencer R., Maier S., Licinio J., Wong M., Chrousos G., Webster E., and Gold P. The impact of the nonpeptide corticotropin releasing hormone antagonist antalarmin on behavioral and endocrine responses to stress. Endocrinology 140 (1999) 79-86
28. Diorio D., Viau V., and Meaney M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J. Neurosci. 13 9 (1993) 3839-3847
29. Dong H.W., Petrovich G.D., and Swanson L.W. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res. Rev. 38 (2001) 192-246
30. Dunn A.J., and File S.E. Corticotropin-releasing factor has an anxiogenic action in the social interaction test. Horm. Behav. 21 2 (1987) 193-202
31. Edwards A.V., and Jones C.T. Autonomic control of adrenal function. J. Anat. 183 Pt 2 (1993) 291-307
32. Engeland W.C. Functional innervation of the adrenal cortex by the splanchnic nerve. Horm. Metab. Res. 30 6-7 (1998) 311-314
33. Erb S., and Stewart J. A role for the bed nucleus of the stria terminalis, but not the amygdala, in the effects of corticotropin-releasing factor on stress-induced reinstatement of cocaine seeking. J. Neurosci. 19 20 (2001) RC35
34. Erb S., Salmaso N., Rodaros D., and Stewart J. A role for the CRF-containing pathway from central nucleus of the amygdala to bed nucleus of the stria terminalis in the stress-induced reinstatement of cocaine seeking in rats. Psychopharmacology 158 4 (2001) 360-365
35. Espejo E.F. Selective dopamine depletion within the medial prefrontal cortex induces anxiogenic-like effects in rats placed on the elevated plus maze. Brain Res. 762 1-2 (1997) 281-284
36. Figueiredo H.F., Bruestle A., Bodie B., Dolgas C.M., and Herman J.P. The medial prefrontal cortex differentially regulates stress-induced c-fos expression in the forebrain depending on type of stressor. Eur. J. Neurosci. 18 8 (2003) 2357-2364
37. Finlay J.M., Jedema H.P., Rabinovic A.D., Mana M.J., Zigmond M.J., and Sved A.F. Impact of corticotropin-releasing hormone on extracellular norepinephrine in prefrontal cortex after chronic cold stress. J. Neurochem. 69 (1997) 144-150
38. Fuchs E., and Flugge G. Modulation of binding sites for corticotropin-releasing hormone by chronic psychosocial stress. Psychoneuroendocrinology 20 1 (1995) 33-51
39. Funk D., Li Z., Shaham Y., and Le A.D. Effect of blockade of corticotropin-releasing factor receptors in the median raphe nucleus on stress-induced c-fos mRNA in the rat brain. Neuroscience 122 1 (2003) 1-4
40. Garcia A., Marti O., Valles A., Dal-Zotto S., and Armario A. Recovery of the hypothalamic-pituitary-adrenal response to stress. Effect of stress intensity, stress duration and previous stress exposure. Neuroendocrinology 72 2 (2000) 114-125
41. Gonzalez L.E., Rujano M., Tucci S., Paredes D., Silva E., Alba G., and Hernandez L. Medial prefrontal transection enhances social interaction. I: Behavioral studies. Brain Res. 887 1 (2000) 7-15
42. Gregus A., Wintink A.J., Davis A.C., and Kalynchuk L.E. Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behav. Brain Res. 156 1 (2005) 105-114
43. Habib K.E., Weld K.P., Rice K.C., Pushkas J., Champoux M., Listwak S., Webster E.L., Atkinson A.J., Schulkin J., Contoreggi C., Chrousos G.P., McCann S.M., Suomi S.J., Higley J.D., and Gold P.W. Oral administration of a corticotropin-releasing hormone receptor antagonist significantly attenuates behavioral, neuroendocrine, and autonomic responses to stress in primates. Proc. Natl. Acad. Sci. 97 11 (2000) 6079-6084
44. Hammack S.E., Richey K.J., Schmid M.J., LoPresti M.L., Watkins L.R., and Maier S.F. The role of corticotropin-releasing hormone in the dorsal raphe nucleus in mediating the behavioral consequences of uncontrollable stress. J. Neurosci. 22 3 (2002) 1020-1026
45. Heidbreder C.A., and Groenewegen H.J. The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci. Biobehav. Rev. 27 6 (2003) 555-579
46. Heinrichs S., Lapsansky J., Lovenberg T., DeSouza E., and Chalmers D. Corticotropin releasing factor CRF-1 but not CRF-2 receptors mediate anxiogenic-like behavior. Regul. Pept. 71 (1997) 15-21
47. Herman J.P., Prewitt C.M., and Cullinan W.E. Neuronal circuit regulation of the hypothalamo-pituitary-adrenocortical stress axis. Crit. Rev. Neurobiol. 10 3-4 (1996) 371-394
48. Hurley K.M., Herbert H., Moga M.M., and Saper C.B. Efferent projections of the infralimbic cortex of the rat. J. Comp. Neurol. 308 2 (1991) 249-276
49. Jaferi A., and Bhatnagar S. Corticosterone can act at the posterior paraventricular thalamus to inhibit hypothalamic-pituitary-adrenal activity in animals that habituate to repeated stress. Endocrinology 147 10 (2006) 4917-4930
50. Jaferi A., Nowak N., and Bhatnagar S. Negative feedback functions in chronically stressed rats: role of posterior paraventricular thalamus. Physiol. Behav. 78 (2003) 365-373
51. Kim K.S., and Han P.L. Optimization of chronic stress paradigms using anxiety- and depression-like behavioral parameters. J. Neurosci. Res. 83 3 (2006) 497-507
52. Korte S.M., and De Boer S.F. A robust animal model of state anxiety: fear-potentiated behaviour in the elevated plus-maze. Eur. J. Pharmacol. 463 1-3 (2003) 163-175
53. Lacroix L., Spinelli S., Heidbreder C.A., and Feldon J. Differential role of the medial and lateral prefrontal cortices in fear and anxiety. Behav. Neurosci. 114 6 (2000) 1119-1130
54. Landgraf R. Neuropeptides and anxiety-related behavior. Endocr. J. 48 5 (2001) 517-533
55. Le A.D., Harding S., Juzytsch W., Fletcher P.J., and Shaham Y. The role of corticotropin-releasing factor in the median raphe nucleus in relapse to alcohol. J. Neurosci. 22 18 (2002) 7844-7849
56. Li H.Y., and Sawchenko P.E. Hypothalamic effector neurons and extended circuitries activated in "neurogenic" stress: a comparison of footshock effects exerted acutely, chronically, and in animals with controlled glucocorticoid levels. J. Comp. Neurol. 6;393 2 (1998) 244-266
57. Makino S., Schulkin J., Smith M.A., Pacak K., Palkovits M., and Gold P.W. Regulation of corticotropin-releasing hormone receptor messenger ribonucleic acid in the rat brain and pituitary by glucocorticoids and stress. Endocrinology 136 10 (1995) 4517-4525
58. Martijena I.D., Calvo N., Volosin M., and Molina V.A. Prior exposure to a brief restraint session facilitates the occurrence of fear in response to a conflict situation: behavioral and neurochemical correlates. Brain Res. 752 1-2 (1997) 136-142
59. Martins A.P., Marras R.A., and Guimaraes F.S. Anxiogenic effect of corticotropin-releasing hormone in the dorsal periaqueductal grey. NeuroReport 8 16 (1997) 3601-3604
60. McElroy J.F., Ward K.A., Zeller K.L., Jones K.W., Gilligan P.J., He L., and Lelas S. The CRF(1) receptor antagonist DMP696 produces anxiolytic effects and inhibits the stress-induced hypothalamic-pituitary-adrenal axis activation without sedation or ataxia in rats. Psychopharmacology (Berl.) 165 1 (2002) 86-92
61. Melia K.R., Ryabinin A.E., Schroeder R., Bloom F.E., and Wilson M.C. Induction and habituation of immediate early gene expression in rat brain by acute and repeated restraint stress. J. Neurosci. 14 10 (1994) 5929-5938
62. Mendonca F.H., and Guimaraes F.S. Intra-hippocampal administration of cycloheximide attenuates the restraint-induced exploratory deficit of an elevated plus maze. Behav. Brain Res. 91 1-2 (1998) 207-211
63. Morency M.A., Stewart R.J., and Beninger R.J. Circling behavior following unilateral microinjections of cocaine into the medial prefrontal cortex: dopaminergic or local anesthetic effect?. J. Neurosci. 7 3 (1987) 812-818
64. Morgan M.A., and LeDoux J.E. Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behav. Neurosci. 109 4 (1995) 681-688
65. Paxinos G, Watson C., 1997. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press, Harcourt Brace.
66. Pellow S., and File S.E. Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol. Biochem. Behav. 24 3 (1986) 525-529
67. Pellow S., Chopin P., File S., and Briley M. Validation of open:closed arm entries in an elevated plus maze as a measure of anxiety in the rat. J. Neurosci. Methods 14 (1985) 149-167
68. Perrot-Sinal T.S., Gregus A., Boudreau D., and Kalynchuk L.E. Sex and repeated restraint stress interact to affect cat odor-induced defensive behavior in adult rats. Brain Res. 1027 1-2 (2004) 161-172
69. Pinto A., Jankowski M., and Sesack S.R. Projections from the paraventricular nucleus of the thalamus to the rat prefrontal cortex and nucleus accumbens shell: ultrastructural characteristics and spatial relationships with dopamine afferents. J. Comp. Neurol. 459 2 (2003) 142-155
70. Quirk G.J., and Gehlert D.R. Inhibition of the amygdala: key to pathological states?. Ann. N. Y. Acad. Sci. 985 (2003) 263-272
71. Radulovic J., Sydow S., and Spiess J. Characterization of native corticotropin-releasing factor receptor type 1 (CRFR1) in the rat and mouse central nervous system. J. Neurosci. Res. 54 4 (1998) 507-521
72. Ragozzino M.E. The contribution of cholinergic and dopaminergic afferents in the rat prefrontal cortex to learning, memory and attention. Psychobiology 28 (2000) 238-247
73. Rangel A., Gonzalez L.E., Villarroel V., and Hernandez L. Anxiolysis followed by anxiogenesis relates to coping and corticosterone after medial prefrontal cortical damage in rats. Brain Res. 992 (2003) 96-103
74. Ridderinkhof K.R., Ullsperger M., Crone E.A., and Nieuwenhuis S. The role of the medial frontal cortex in cognitive control. Science 306 5695 (2004) 443-447
75. Rivier C.L., Grigoriasdis D.E., and Rivier J.E. Role of corticotropin-releasing factor receptors type 1 and 2 in modulating the rat adrenocorticotropin response to stressors. Endocrinology 144 6 (2003) 2396-2403
76. Roland B.L., and Sawchenko P.E. Local origins of some GABAergic projections to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J. Comp. Neurol. 332 1 (1993) 123-143
77. Roozendaal B., McReynolds J.R., and McGaugh J.L. The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment. J. Neurosci. 24 6 (2004) 1385-1392
78. Sarter M., and Markowitsch H.J. Convergence of basolateral amygdaloid and mediodorsal thalamic projections in different areas of the frontal cortex in the rat. Brain Res. Bull. 10 5 (1983) 607-622
79. Sahuque L.L., Kullberg E.F., Mcgeehan A.J., Kinder J.R., Hicks M.P., Blanton M.G., Janak P.H., and Olive M.F. 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 (Berl.) 186 1 (2006) 122-132
80. Sauvage M., and Steckler T. Detection of corticotropin-releasing hormone receptor 1 immunoreactivity in cholinergic, dopaminergic and noradrenergic neurons of the murine basal forebrain and brainstem nuclei-potential implication for arousal and attention. Neuroscience 104 3 (2001) 643-652
81. Shah A.A., and Treit D. Excitotoxic lesions of the medial PFC attenuate fear responses in the EPM, social interaction and shock probe burying tests. Brain Res. 969 (2003) 183-194
82. Shah A.A., and Treit D. Infusions of midazolam into the medial prefrontal cortex produce anxiolytic effects in the elevated plus-maze and shock-probe burying tests. Brain Res. 996 1 (2004) 31-40
83. Shah A.A., Sjovold T., and Treit D. Inactivation of the medial prefrontal cortex with the GABAA receptor agonist muscimol increases open-arm activity in the elevated plus-maze and attenuates shock-probe burying in rats. Brain Res. 1028 1 (2004) 112-115
84. Smagin G.N., Harris R.B., and Ryan D.H. Corticotropin-releasing factor receptor antagonist infused into the locus coeruleus attenuates immobilization stress-induced defensive withdrawal in rats. Neurosci. Lett. 220 3 (1996) 167-170
85. Spencer S.J., Buller K.M., and Day T.A. 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 4 (2005) 363-376
86. Sullivan R.M., and Gratton A. Lateralized effects of mPFC lesions on neuroendocrine and autonomic stress responses in rats. J. Neurosci. 19 7 (1999) 2834-2840
87. Sullivan R.M., and Gratton A. Prefrontal cortical regulation of hypothalamic-pituitary-adrenal function in the rat and implications for psychopathology: side matters. Psychoneuroendocrinology 27 (2002) 99-114
88. Swanson L.W., and Sawchenko P.E. Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu. Rev. Neurosci. 6 (1983) 269-324
89. Swanson L.W., Sawchenko P.E., Rivier J., and Vale W.W. Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36 3 (1983) 165-186
90. Takahashi L.K., Kalin N.H., Vanden Burgt J.A., and Sherman J.E. Corticotropin-releasing factor modulates defensive-withdrawal and exploratory behavior in rats. Behav. Neurosci. 103 3 (1989) 648-654
91. Terreberry R.R., and Neafsey E.J. The rat medial frontal cortex projects directly to autonomic regions of the brainstem. Brain Res. Bull. 19 6 (1987) 639-649
92. Thorsell A., Carlsson K., Ekman R., and Heilig M. Behavioral and endocrine adaptation, and up-regulation of NPY expression in rat amygdala following repeated restraint stress. NeuroReport 10 14 (1999) 3003-3007
93. Tzschentke T.M., and Schmidt W.J. Differential effects of discrete subarea-specific lesions of the rat medial prefrontal cortex on amphetamine- and cocaine-induced behavioural sensitization. Cereb. Cortex 10 5 (2000) 488-498
94. Vahl T.P., Ulrich-Lai Y.M., Ostrander M.M., Dolgas C.M., Elfers E.E., Seeley R.J., D-Alessio D.A., and Herman J.P. Comparative analysis of ACTH and corticosterone sampling methods in rats. Am. J. Physiol., Endocrinol Metabol. Gastrointest. Physiol. 289 5 (2005) E823-E828
95. Van Bockstaele E.J., Colago E.E., and Pickel V.M. Enkephalin terminals form inhibitory-type synapses on neurons in the rat nucleus locus coeruleus that project to the medial prefrontal cortex. Neuroscience 71 2 (1996) 429-442
96. Van Pett K., Viau V., Bittencourt J., Chan R., Li H., Arias C., Prins G., Perrin M., Vale W., and Sawchenko P. Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J. Comp. Neurol. 428 (2000) 191-212
97. Vertes R.P. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51 1 (2004) 32-58
98. Viau V., and Sawchenko P.E. Hypophysiotropic neurons of the paraventricular nucleus respond in spatially, temporally, and phenotypically differentiated manners to acute vs. repeated restraint stress: rapid publication. J. Comp. Neurol. 445 4 (2002) 293-307
99. Wall P.M., and Messier C. U-69,593 microinjection in the infralimbic cortex reduces anxiety and enhances spontaneous alternation memory in mice. Brain Res. 856 1-2 (2000) 259-280
100. Wiersma A., Konsman J.P., Knollema S., Bohus B., and Koolhaas J.M. Differential effects of CRH infusion into the central nucleus of the amygdala in the Roman high-avoidance and low-avoidance rats. Psychoneuroendocrinology 23 3 (1998) 261-274