Induction of c-Fos and ΔFosB immunoreactivity in rat brain by vagal nerve stimulation

Neuropsychopharmacology

Volumn 33, Issue 8, 2008, Pages 1884-1895

  Cunningham, J Thomas ^a   Mifflin, Steven W ^a   Gould, Georgianna G ^a   Frazer, Alan ^a  

^a University of Texas Health Science Center at San Antonio   (United States)

Author keywords

FosB; c Fos; Depression; Forced swim test; Vagal nerve stimulation

Indexed keywords

DESIPRAMINE; PROTEIN C FOS; TRANSCRIPTION FACTOR FOSB;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE MONITORING; BRAIN MAPPING; BRAIN REGION; BREATHING RATE; CONTROLLED STUDY; DRUG EFFECT; FORCED SWIMMING TEST; HEART RATE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; TELEMETRY; VAGUS NERVE STIMULATION;

ANIMALS; BLOOD PRESSURE; BRAIN CHEMISTRY; DEPRESSION; ELECTRIC STIMULATION; ELECTRODES, IMPLANTED; HEART RATE; IMMUNOHISTOCHEMISTRY; MALE; MOTOR ACTIVITY; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY MECHANICS; SWIMMING; TELEMETRY; VAGUS NERVE;

EID: 45149095307     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1301570     Document Type: Article

References (79)

1. Ansah T, Wage L, Shockley D (1996). Changes in locomotor activity, core temperature, and heart rate in response to repeated cocaine administration. Physiol Behav 59: 1261-1267.
2. 99mTc-HMPAO SPET brain images. Eur J Nucl Med Mol Imaging 30: 301-305.
3. Beck CH (1995). Acute treatment with antidepressant drugs selectively increases the expression of c-fos in the rat brain. J Psychiatry Neurosci 20: 25-32.
4. Castle M, Comoli E, Loewy AD (2005). Autonomic brainstem nuclei are linked to the hippocampus. Neuroscience 134: 657-669.
5. Chen J, Kelz MB, Hope BT, Nakabeppu Y, Nestler EJ (1997). Chronic Fos-related antigens: stable variants of deltaFosB induced in brain by chronic treatments. J Neurosci 17: 4933-4941.
6. Cole AJ, Abu-Shakra S, Saffen DW, Baraban JM, Worley PF (1990). Rapid rise in transcription factor mRNAs in rat brain after electroshock-induced seizures. J Neurochem 55: 1920-1927.
7. Cryan JF, Markou A, Lucki I (2002a). Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 23: 238-245.
8. Cryan JF, Page ME, Lucki I (2002b). Noradrenergic lesions differentially alter the antidepressant-like effects of reboxetine in a modified forced swim test. Eur J Pharmacol 436: 197-205.
9. Cryan JF, Page ME, Lucki I (2005b). Differential behavioral effects of the antidepressants reboxetine, fluoxetine, and moclobemide in a modified forced swim test following chronic treatment. Psychopharmacology (Berl) 182: 335-344.
10. Cryan JF, Valentino RJ, Lucki I (2005a). Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev 29: 547-569.
11. Cunningham JT, Grindstaff RJ, Grindstaff RR, Sullivan MJ (2002). Fos immunoreactivity in the diagonal band and the perinuclear zone of the supraoptic nucleus after hypertension and hypervolaemia in unanaesthetized rats. J Neuroendocrinol 14: 219-227.
12. Cunningham JT, Herrera-Rosales M, Martinez MA, Mifflin S (2007). Identification of active central nervous system sites in renal wrap hypertensive rats. Hypertension 49: 653-658.
13. Curran T, Morgan JI (1995). Fos: an immediate-early transcription factor in neurons. J Neurobiol 26: 403-412.
14. Curtis KS, Cunningham JT, Heesch CM (1999). Fos expression in brain stem nuclei of pregnant rats after hydralazine-induced hypotension. Am J Physiol 277(2 Part 2): R532-R540.
15. Dampney RA (1994). Functional organization of central pathways regulating the cardiovascular system. Physiol Rev 74: 323-364.
16. Dampney RA, Horiuchi J (2003). Functional organisation of central cardiovascular pathways: studies using c-fos gene expression. Prog Neurobiol 71: 359-384.
17. Dorr AE, Debonnel G (2006). Effect of vagus nerve stimulation on serotonergic and noradrenergic transmission. J Pharmacol Exp Ther 318: 890-898.
18. Dragunow M, Faull R (1989). The use of c-fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 29: 261-265.
19. Duncan GE, Knapp DJ, Johnson KB, Breese GR (1996). Functional classification of antidepressants based on antagonism of swim stress-induced fos-like immunoreactivity. J Pharmacol Exp Ther 277: 1076-1089.
20. Dziedzicka-Wasylewska M, Faron-Gorecka A, Kusmider M, Drozdowska E, Rogoz Z, Siwanowicz J et al (2006). Effect of antidepressant drugs in mice lacking the norepinephrine transporter. Neuropsychopharmacology 31: 2424-2432.
21. Foley JO, DuBois F (1937). Quantitative studies of the vagus nerve in the cat. I. The ratio of sensory motor studies. J Comp Neurol 67: 49-67.
22. Fraga IC, Fregoneze JB, Carvalho FL, Dantas KB, Azevedo CS, Pinho CB et al (2005). Acute fluoxetine administration differentially affects brain C-Fos expression in fasted and refed rats. Neuroscience 134: 327-334.
23. Gieroba ZJ, Blessing WW (1994). Fos-containing neurons in medulla and pons after unilateral stimulation of the afferent abdominal vagus in conscious rabbits. Neuroscience 59: 851-858.
24. Goldapple K, Segal Z, Garson C, Lau M, Bieling P, Kennedy S et al (2004). Modulation of cortical-limbic pathways in major depression: treatment-specific effects of cognitive behavior therapy. Arch Gen Psychiatry 61: 34-41.
25. Gottlieb HB, Ji LL, Jones H, Penny ML, Fleming T, Cunningham JT (2006). Differential effects of water and saline intake on water deprivation-induced c-Fos staining in the rat. Am J Physiol Regul Integr Comp Physiol 290: R1251-R1261.
26. Grindstaff RJ, Grindstaff RR, Sullivan MJ, Cunningham JT (2000). Role of the locus ceruleus in baroreceptor regulation of supraoptic vasopressin neurons in the rat. Am J Physiol Regul Integr Comp Physiol 279: R306-R319.
27. Groves DA, Bowman EM, Brown VJ (2005). Recordings from the rat locus coeruleus during acute vagal nerve stimulation in the anaesthetised rat. Neurosci Lett 379: 174-179.
28. Groves DA, Brown VJ (2005). Vagal nerve stimulation: a review of its applications and potential mechanisms that mediate its clinical effects. Neurosci Biobehav Rev 29: 493-500.
29. Guyenet PG (2006). The sympathetic control of blood pressure. Nat Rev Neurosci 7: 335-346.
30. Henry TR, Bakay RA, Pennell PB, Epstein CM, Votaw JR (2004). Brain blood-flow alterations induced by therapeutic vagus nerve stimulation in partial epilepsy: II. prolonged effects at high and low levels of stimulation. Epilepsia 45: 1064-1070.
31. Henry TR, Bakay RA, Votaw JR, Pennell PB, Epstein CM, Faber TL et al (1998). Brain blood flow alterations induced by therapeutic vagus nerve stimulation in partial epilepsy: I. Acute effects at high and low levels of stimulation. Epilepsia 39: 983-990.
32. Herdegen T, Leah JD (1998). Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res Brain Res Rev 28: 370-490.
33. Hope BT, Kelz MB, Duman RS, Nestler EJ (1994). Chronic electroconvulsive seizure (ECS) treatment results in expression of a long-lasting AP-1 complex in brain with altered composition and characteristics. J Neurosci 14: 4318-4328.
34. Howarth F, Jacobson M, Naseer O, Adeghate E (2005). Short- term effects of streptozotocin- induced diabetes on the electrocardiogram, physical activity and body temperature in rats. Exp Physiol 90: 229-237.
35. Howe BM, Bruno SB, Higgs KA, Stigers RL, Cunningham JT (2004). FosB expression in the central nervous system following isotonic volume expansion in unanesthetized rats. Exp Neurol 187: 190-198.
36. Ji LL, Fleming T, Penny ML, Toney GM, Cunningham JT (2005). Effects of water deprivation and rehydration on c-Fos and FosB staining in the rat supraoptic nucleus and lamina terminalis region. Am J Physiol Regul Integr Comp Physiol 288: R311-R321.
37. Kalia M, Sullivan JM (1982). Brainstem projections of sensory and motor components of the vagus nerve in the rat. J Comp Neurol 211: 248-265.
38. Kawashima K, Amano H, Fujimoto K, Suzuki T, Fujii T, Mochizuki S et al (1996). Effect of repeated administration of KT3-671, a nonpeptide AT1 receptor antagonist, on diurnal variation in blood pressure, heart rate, and locomotor acitivity in stroke-prone spontanesouly hypertensive rats as determined by radiotelemetry. J Cardiovasc Pharmacol 27: 411-416.
39. Kovacs KJ (1998). c-Fos as a transcription factor: a stressful (re)view from a functional map. Neurochem Int 33: 287-297.
40. Krahl SE, Clark KB, Smith DC, Browning RA (1998). Locus coeruleus lesions suppress the seizure-attenuating effects of vagus nerve stimulation. Epilepsia 39: 709-714.
41. Krahl SE, Senanayake SS, Pekary AE, Sattin A (2004). Vagus nerve stimulation (VNS) is effective in a rat model of antidepressant action. J Psychiatr Res 38: 237-240.
42. Kuipers SD, Trentani A, Westenbroek C, Bramham CR, Korf J, Kema IP et al (2006). Unique patterns of FOS, phospho-CREB and BrdU immunoreactivity in the female rat brain following chronic stress and citalopram treatment. Neuropharmacology 50: 428-440.
43. Lenox RH, Frazer A (2002). Mechanism of action of antidepressants and mood-stabilizers. In: Davis KL, Charney D, Coyle JT, Nemeroff C (eds). Neuropsychopharmacology, The Fifth Generation of Progress. Lippincott Williams & Wilkins: Philadelphia. pp 1139-1163.
44. Lucki I (1997). The forced swimming test as a model for core and component behavioral effects of antidepressant drugs. Behav Pharmacol 8: 523-532.
45. Mayberg HS, Brannan SK, Tekell JL, Silva JA, Mahurin RK, McGinnis S et al (2000). Regional metabolic effects of fluoxetine in major depression: serial changes and relationship to clinical response. Biol Psychiatry 48: 830-843.
46. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C et al (2005). Deep brain stimulation for treatment-resistant depression. Neuron 45: 651-660.
47. Meerlo P, Sgoifo A, Boer S, Koolhaas J (1999). Long-lasting consequences of a social conflict in rats: behavior during the interaction predicts subsequent changes in daily rhythms of heart rate, temperature, and activity. Behav Neurosci 113: 1283-1290.
48. Miyata S, Hamamura T, Lee Y, Miki M, Habara T, Oka T et al (2005). Contrasting Fos expression induced by acute reboxetine and fluoxetine in the rat forebrain: neuroanatomical substrates for the antidepressant effect. Psychopharmacology (Berl) 177: 289-295.
49. Miyata S, Tsujioka H, Itoh M, Matsunaga W, Kuramoto H, Kiyohara T (2001). Time course of Fos and Fras expression in the hypothalamic supraoptic neurons during chronic osmotic stimulation. Brain Res Mol Brain Res 90: 39-47.
50. Morelli M, Pinna A, Ruiu S, Del Zompo M (1999). Induction of Fos-like-immunoreactivity in the central extended amygdala by antidepressant drugs. Synapse 31: 1-4.
51. Morinobu S, Strausbaugh H, Terwilliger R, Duman RS (1997). Regulation of c-Fos and NGF1-A by antidepressant treatments. Synapse 25: 313-320.
52. Muigg P, Hoelzl U, Palfrader K, Neumann I, Wigger A, Landgraf R et al (2007). Altered brain activation pattern associated with drug-induced attenuation of enhanced depression-like behavior in rats bred for high anxiety. Biol Psychiatry 61: 782-796.
53. Naritoku DK, Terry WJ, Helfert RH (1995). Regional induction of fos immunoreactivity in the brain by anticonvulsant stimulation of the vagus nerve. Epilepsy Res 22: 53-62.
54. Nemeroff CB, Mayberg HS, Krahl SE, McNamara J, Frazer A, Henry TR et al (2006). VNS therapy in treatment-resistant depression: clinical evidence and putative neurobiological mechanisms. Neuropsychopharmacology 31: 1345-1355.
55. Nestler EJ (2004). Molecular mechanisms of drug addiction. Neuropharmacology 47(Suppl 1): 24-32.
56. Nobler MS, Oquendo MA, Kegeles LS, Malone KM, Campbell CC, Sackeim HA et al (2001). Decreased regional brain metabolism after ect. Am J Psychiatry 158: 305-308.
57. Norgren R (1978). Projections from the nucleus of the solitary tract in the rat. Neuroscience 3: 207-218.
58. Osharina V, Bagaev V, Wallois F, Larnicol N (2006). Autonomic response and Fos expression in the NTS following intermittent vagal stimulation: Importance of pulse frequency. Auton Neurosci: Basic Clin 126-127: 72-80.
59. Page ME, Detke MJ, Dalvi A, Kirby LG, Lucki I (1999). Serotonergic mediation of the effects of fluoxetine, but not desipramine, in the rat forced swimming test. Psychopharmacology (Berl) 147: 162-167.
60. Paxinos G, Watson C (1986). The Rat Brain in Stereotaxic Coordinates. Academic Press: New York.
61. Porsolt RD, Le Pichon M, Jalfre M (1977). Depression: a new animal model sensitive to antidepressant treatments. Nature 266: 730-732.
62. Roosevelt RW, Smith DC, Clough RW, Jensen RA, Browning RA (2006). Increased extracellular concentrations of norepinephrine in cortex and hippocampus following vagus nerve stimulation in the rat. Brain Res 1119: 124-132.
63. Rush AJ, Marangell LB, Sackeim HA, George MS, Brannan SK, Davis SM et al (2005a). Vagus nerve stimulation for treatment-resistant depression: a randomized, controlled acute phase trial. Biol Psychiatry 58: 347-354.
64. Rush AJ, Sackeim HA, Marangell LB, George MS, Brannan SK, Davis SM et al (2005b). Effects of 12 months of vagus nerve stimulation in treatment-resistant depression: a naturalistic study. Biol Psychiatry 58: 355-363.
65. Rutherfurd SD, Widdop RE, Sannajust F, Louis WJ, Gundlach AL (1992). Expression of c-fos and NGFI-A messenger RNA in the medulla oblongata of the anaesthetized rat following stimulation of vagal and cardiovascular afferents. Brain Res Mol Brain Res 13: 301-312.
66. Sackeim HA, Brannan SK, John Rush A, George MS, Marangell LB, Allen J (2007). Durability of antidepressant response to vagus nerve stimulation (VNSTM). Int J Neuropsychopharmacol (originally published online by Cambridge University Press, 9 February 2007, http://journals.cambridge.org/ 193378).
67. Saper CB (1995). Central autonomic system. In: Paxinos G (ed). The Rat Nervous System. Academic Press: San Diego, CA. pp 107-135.
68. Senba E, Ueyama T (1997). Stress-induced expression of immediate early genes in the brain and peripheral organs of the rat. Neurosci Res 29: 183-207.
69. Slattery DA, Morrow JA, Hudson AL, Hill DR, Nutt DJ, Henry B (2005). Comparison of alterations in c-fos and Egr-1 (zif268) expression throughout the rat brain following acute administration of different classes of antidepressant compounds. Neuropsychopharmacology 30: 1278-1287.
70. Sumner BE, Cruise LA, Slattery DA, Hill DR, Shahid M, Henry B (2004). Testing the validity of c-fos expression profiling to aid the therapeutic classification of psychoactive drugs. Psychopharmacology (Berl) 171: 306-321.
71. Takayama K, Suzuki T, Miura M (1994). The comparison of effects of various anesthetics on expression of Fos protein in the rat brain. Neurosci Lett 176: 59-62.
72. Ter Horst GJ, de Boer P, Luiten PG, van Willigen JD (1989). Ascending projections from the solitary tract nucleus to the hypothalamus. A Phaseolus vulgaris lectin tracing study in the rat. Neuroscience 31: 785-797.
73. Thomsen C, Helboe L (2003). Regional pattern of binding and c-Fos induction by (R)- and (S)-citalopram in rat brain. Neuroreport 14: 2411-2414.
74. Torres G, Horowitz JM, Laflamme N, Rivest S (1998). Fluoxetine induces the transcription of genes encoding c-fos, corticotropin-releasing factor and its type 1 receptor in rat brain. Neuroscience 87: 463-477.
75. Winston SM, Hayward MD, Nestler EJ, Duman RS (1990). Chronic electroconvulsive seizures down-regulate expression of the immediate-early genes c-fos and c-jun in rat cerebral cortex. J Neurochem 54: 1920-1925.
76. Woodbury DM, Woodbury JW (1990). Effects of vagal stimulation on experimentally induced seizures in rats. Epilepsia 31(Suppl 2): S7-S19.
77. Xu F, Gainetdinov RR, Wetsel WC, Jones SR, Bohn LM, Miller GW et al (2000). Mice lacking the norepinephrine transporter are supersensitive to psychostimulants. Nat Neurosci 3: 465-471.
78. Yousfi-Malki M, Puizillout JJ (1994). Induction of Fos-like protein in neurons of the medulla oblongata after electrical stimulation of the vagus nerve in anesthetized rabbit. Brain Res 635: 317-322.
79. Zhang W, Wang Z, Zhang W (2004). Characterizing blood pressure, heart rate, physical activity, circadian rhythm and their response to nos inhibitor and substrate in chf rats with telemetry. Vasc Dis Prev 1: 159-166.