Postnatal changes in tryptophan hydroxylase and serotonin transporter immunoreactivity in multiple brainstem nuclei of the rat: Implications for a sensitive period

Journal of Comparative Neurology

Volumn 518, Issue 7, 2010, Pages 1082-1097

  Liu, Qiuli ^a   Wong Riley, Margaret T T ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

5 HT; Critical period; Development; Raph nuclei; Respiratory control network; Serotonin transporter

Indexed keywords

SEROTONIN TRANSPORTER; TRYPTOPHAN HYDROXYLASE;

AMBIGUUS NUCLEUS; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN STEM; CONTROLLED STUDY; FEMALE; GLOBUS PALLIDUS; MALE; NERVE CELL NETWORK; NEUROPIL; NONHUMAN; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAPHE MAGNUS NUCLEUS; RAPHE NUCLEUS; RAT;

ANIMALS; ANIMALS, NEWBORN; BRAIN STEM; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; TIME FACTORS; TRYPTOPHAN HYDROXYLASE;

EID: 77949415671     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22265     Document Type: Article

References (92)

1. Azmitia EC. 2001. Modern views on an ancient chemical: serotonin effects on cell proliferation, maturation, and apoptosis. Brain Res Bull 56:413-424.
2. Baker-Herman TL, Mitchell GS. 2002. Phrenic long-term facilitation requires spinal serotonin receptor activation and protein synthesis. J Neurosci 22:6239-6246.
3. Ballanyi K. 2004. Neuromodulation of the perinatal respiratory network. Curr Neuropharm 2:221-243.
4. Bieger D, Hopkins DA. 1987. Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: the nucleus ambiguus. J Comp Neurol 262:546-562.
5. Bonham AC. 1995. Neurotransmitters in the CNS control of breathing. Respir Physiol 101:219-230.
6. Braga VA, Antunes VR, Machado BH. 2006. Autonomic and respiratory responses to microinjection of L-glutamate into the commissural subnucleus of the NTS in the working heart-brainstem preparation of the rat. Brain Res 1093:150-160.
7. Brown P, Molliver ME. 2000. Dual serotonin (5-HT) projections to the nucleus accumbens core and shell: relation of the 5-HT transporter to amphetamine-induced neurotoxicity. J Neurosci 20:1952-1963.
8. Burman KJ, Ige AO, White JH, Marshall FH, Pangalos MN, Emson PC, Minson JB, Llewellyn-Smith IJ. 2003. GABAB receptor subunits, R1 and R2, in brainstem catecholamine and serotonin neurons. Brain Res 970:35-46.
9. Buznikov GA, Lambert HW, Lauder JM. 2001. Serotonin and serotonin-like substances as regulators of early embryogenesis and morphogenesis. Cell Tissue Res 305:177-186.
10. Chubakov AR, Gromova EA, Konovalov GV, Sarkisova EF, Chumasov EI. 1986. The effects of serotonin on the morphofunctional development of rat cerebral neocortex in tissue culture. Brain Res 369:285-297.
11. Cream C, Li A, Nattie E. 2002. The retrotrapezoid nucleus (RTN): local cytoarchitecture and afferent connections. Respir Physiol Neurobiol 130:121-137.
12. Ellenberger HH, Feldman JL. 1990. Brainstem connections of the rostral ventral respiratory group of the rat. Brain Res 513:35-42.
13. Feldman JL, Del Negro CA. 2006. Looking for inspiration: new perspectives on respiratory rhythm. Nat Rev Neurosci 7:232-242.
14. Feldman JL, Mitchell GS, Nattie EE. 2003. Breathing: rhythmicity, plasticity, chemosensitivity Annu Rev Neurosci 26:239-66.
15. Finley JCW, Katz DM. 1992. The central organization of carotid body afferent projection to the brainstem of the rat. Brain Res 572:108-116.
16. Fox K. 1992. A critical period for experience-dependent synaptic plasticity in rat barrel cortex. J Neurosci 12:1826-1838.
17. Fujita M, Shimada S, Maeno H, Nishimura T, Tohyama M. 1993. Cellular localization of serotonin transporter mRNA in the rat brain. Neurosci Lett 162:59-62.
18. Fuller DD, Zabka AG, Baker TL, Mitchell GS. 2001. Phrenic longterm facilitation requires 5-HT receptor activation during but not following episodic hypoxia. J Appl Physiol 90:2001-2006.
19. Gaytán SP, Calero F, Núñez-Abades PA, Morillo AM, Pásaro R. 1997. Pontomedullary efferent projections of the ventral respiratory neuronal subsets of the rat. Brain Res Bull 42:323-334.
20. Gould E. 1999. Serotonin and hippocampal neurogenesis. Neuropsychopharmacology 21:46S-51S.
21. Gray PA, Rekling JC, Bocchiaro CM, Feldman JL. 1999. Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the pre-Bötzinger complex. Science 286: 1566-1568.
22. Guyenet PG, Stornetta RL, Bayliss DA, Mulkey DK. 2005. Retrotrapezoid nucleus: a litmus test for the identification of central chemoreceptors. Exp Physiol 90:247-253.
23. Guyenet PG, Stornetta RL, Bayliss DA. 2008. Retrotrapezoid nucleus and central chemoreception. J Physiol 586:2043-2048.
24. Haxhiu MA, Erokwu B, Bhardwaj V, Dreshaj IA. 1998. The role of the medullary raphé nuclei in regulation of cholinergic outflow to the airways. J Auton Nerv Syst 69:64-71.
25. Hilaire G, Duron B. 1999. Maturation of the mammalian respiratory system. Physiol Rev 79:325-360.
26. Hilaire G, Bou C, Monteau R. 1997. Serotonergic modulation of central respiratory activity in the neonatal mouse: an in vitro study. Eur J Pharmacol 329:115-120.
27. Hodges MR, Richerson GB. 2008. Contributions of 5-HT neurons to respiratory control: neuromodulatory and trophic effects. Respir Physiol Neurobiol 164:222-232.
28. Hodges MR, Wehner M, Aungst J, Smith JC, Richerson GB. 2009. Transgenic mice lacking serotonin neurons have severe apnea and high mortality during development. J Neurosci 29: 10341-10349.
29. Holstege G. 2009. The mesopontine rostromedial tegmental nucleus and the emotional motor system: role in basic survival behavior. J Comp Neurol 513:559-565.
30. Holtman JR Jr, Marion LJ, Speck DF. 1990. Origin of serotonincontaining projections to the ventral respiratory group in the rat. Neuroscience 37:541-552.
31. Horner RL. 2007. Respiratory motor activity: influence of neuromodulators and implications for sleep disordered breathing. Can J Physiol Pharmacol 85:155-165.
32. Horschitz S, Hummerich R, Schloss P. 2001. Structure, function and regulation of the 5-hydroxytryptamine (serotonin) transporter. Biochem Soc Trans 29:728-732.
33. Huang J, Pickel VM. 2002. Serotonin transporters (SERTs) within the rat nucleus of the solitary tract: subcellular distribution and relation to 5HT2A receptors. J Neurocytol 31:667-679.
34. Inazu M, Takeda H, Ikoshi H, Sugisawa M, Uchida Y, Matsumiya T. 2001. Pharmacological characterization and visualization of the glial serotonin transporter. Neurochem Int 39:39-49.
35. Ivgy-May N, Tamir H, Gershon MD. 1994. Synaptic properties of serotonergic growth cones in developing rat brain. J Neurosci 14:1011-1129.
36. Jacobs BL, Fornal CA. 1995. Serotonin and behavior. A general hypothesis. In: Bloom FE, Kupfer DJ, editors. Psychopharmacology: the fourth generation of progress. New York: Raven Press. p 461-469.
37. Janusonis S, Gluncic V, Rakic P. 2004. Early serotonergic projections to Cajal-Retzius cells: relevance for cortical development. J Neurosci 24:1652-1659.
38. Jordan D. 2001. Central nervous pathways and control of the airways. Respir Physiol 125:67-81.
39. Kinney HC. 2005. Abnormalities of the brainstem serotonergic system in the sudden infant death syndrome: a review. Pediatr Dev Pathol 8:507-524.
40. Kinney HC. 2009. Brainstem mechanisms underlying the sudden infant death syndrome: evidence from human pathologic studies. Dev Psychobiol 51:223-233.
41. Kish SJ, Tong J, Hornykiewicz O, Rajput A, Chang LJ, Guttman M, Furukawa Y. 2008. Preferential loss of serotonin markers in caudate vs. putamen in Parkinson's disease. Brain 131:120-131.
42. Lauder JM. 1990. Ontogeny of the serotonergic system in the rat: serotonin as a developmental signal. Ann N Y Acad Sci 600: 297-313.
43. Lebrand C, Gaspar P, Nicolas D, Hornung JP. 2006. Transitory uptake of serotonin in the developing sensory pathways of the common marmoset. J Comp Neurol 499:677-689.
44. 2 receptors. Curr Drug Targets 3:11-26.
45. Li A, Nattie E. 2008. Serotonin transporter knockout mice have a reduced ventilatory response to hypercapnia (predominantly in males) but not to hypoxia. J Physiol 586:2321-2329.
46. Liu Q, Wong-Riley MTT. 2002. Postnatal expression of neurotransmitters, receptors, and cytochrome oxidase in the rat pre-Bötzinger complex. J Appl Physiol 92:923-934.
47. Liu Q, Wong-Riley MTT. 2003. Postnatal changes in cytochrome oxidase expressions in brainstem nuclei of rats: implications for sensitive periods. J Appl Physiol 95:2285-2291.
48. Liu Q, Wong-Riley MTT. 2005. Postnatal developmental expressions of neurotransmitters and receptors in various brainstem nuclei of rats. J Appl Physiol 98:1442-1457.
49. Liu Q, Wong-Riley MT. 2008. Postnatal changes in the expression of serotonin 2A receptors in various brainstem nuclei of the rat. J Appl Physiol 104:1801-1808.
50. Liu Q, Lowry TF, Wong-Riley MT. 2006. Postnatal changes in ventilation during normoxia and acute hypoxia in the rat: implication for a sensitive period. J Physiol 577:957-970.
51. Liu Q, Fehring C, Lowry TF, Wong-Riley MT. 2009. Postnatal development of metabolic rate during normoxia and acute hypoxia in rats: implication for a sensitive period. J Appl Physiol 106:1212-1222.
52. Loewy AD, McKellar S. 1980. The neuroanatomical basis of central cardiovascular control. Fed Proc 39:2495-2503.
53. Lovick TA. 1987. Cardiovascular control from neurons in the ventrolateral medulla. In: Taylor EW, editor. The neurobiology of the cardiorespiratory system. Manchester: Manchester University Press. p 199-208.
54. Millhorn DE, Eldridge FL, Waldrop TG. 1980. Prolonged stimulation of respiration by endogenous central serotonin. Respir Physiol 42:171-188.
55. Moon RY, Horne RS, Hauck FR. 2007. Sudden infant death syndrome. Lancet 370:1578-1587.
56. Mulkey DK, Stornetta RL, Weston MC, Simmons JR, Parker A, Bayliss DA, Guyenet PG. 2004. Respiratory control by ventral surface chemoreceptor neurons in rats. Nat Neurosci 7:1360-1369.
57. Mulkey DK, Rosin DL, West G, Takakura AC, Moreira TS, Bayliss DA, Guyenet PG. 2007. Serotonergic neurons activate chemosensitive retrotrapezoid nucleus neurons by a pHindependent mechanism. J. Neurosci 27:14128-14138.
58. Narita N, Narita M, Takashima S, Nakayama M, Nagai T, Okado N. 2001. Serotonin transporter gene variation is a risk factor for sudden infant death syndrome in the Japanese population. Pediatrics 107:690-692.
59. Nielsen K, Brask D, Knudsen GM, Aznar S. 2006. Immunodetection of the serotonin transporter protein is a more valid marker for serotonergic fibers than serotonin. Synapse 59: 270-276.
60. Onimaru H, Homma I. 2003. A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J Neurosci 23:1478-1486.
61. Panigrahy A, Filiano J, Sleeper LA, Mandell F, Valdes-Dapena M, Krous HF, Rava LA, Foley E, White WF, Kinney HC. 2000. Decreased serotonergic receptor binding in rhombic lipderived regions of the medulla oblongata in the sudden infant death syndrome. J Neuropathol Exp Neurol 59:377-384.
62. Park DH, Snyder DW, Joh TH. 1986. Postnatal developmental changes of tryptophan hydroxylase activity in serotonergic cell bodies and terminals of rat brain. Brain Res 378:183-185.
63. Paterson DS, Trachtenberg FL, Thompson EG, Belliveau RA, Beggs AH, Darnall R, Chadwick AE, Krous HF, Kinney HC. 2006. Multiple serotonergic brainstem abnormalities in sudden infant death syndrome. JAMA 296:2124-2132.
64. Paton JF, Rogers WT, Schwaber JS. 1991. Tonically rhythmic neurons within a cardiorespiratory region of the nucleus tractus solitarii of the rat. J Neurophysiol 66:824-838.
65. Pavone LM, Tafuri S, Mastellone V, Morte RD, Lombardi P, Avallone L, Maharajan V, Staiano N, Scala G. 2007. Expression of the serotonin transporter (SERT) in the choroid plexuses from buffalo brain. Anat Rec 290:1492-1499.
66. Peña F, Ramirez JM. 2002. Endogenous activation of serotonin-2A receptors is required for respiratory rhythm generation in vitro. J Neurosci 22:11055-11064.
67. Penatti EM, Berniker AV, Kereshi B, Cafaro C, Kelly ML, Niblock MM, Gao HG, Kinney HC, Li A, Nattie EE. 2006. Ventilatory response to hypercapnia and hypoxia after extensive lesion of medullary serotonergic neurons in newborn conscious piglets. J Appl Physiol 101:1177-1188.
68. Pickel VM, Chan J. 1999. Ultrastructural localization of the serotonin transporter in limbic and motor compartments of the nucleus accumbens. J Neurosci 19:7356-7366.
69. Rekling, JC, Feldman JL. 1998. Pre-Bötzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu Rev Physiol 60:385-405.
70. Ribas-Salgueiro JL, Gaytán SP, Ribas J, Pásaro R. 2005. Characterization of efferent projections of chemosensitive neurons in the caudal parapyramidal area of the rat brain. Brain Res Bull 66:235-248.
71. Richerson GB. 2004. Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat Rev Neurosci 5:449-461.
72. Richerson GB, Wang W, Hodges MR, Dohle CI, Diez-Sampedro A. 2005. Homing in on the specific phenotype(s) of central respiratory chemoreceptors. Exp Physiol 90:259-269.
73. Rind HB, Russo AF, Whittemore SR. 2000. Developmental regulation of tryptophan hydroxylase messenger RNA expression and enzyme activity in the raphé and its target fields. Neuroscience 101:665-677.
74. Robinson N. 1968. Histochemistry of rat brainstem monoamine oxidase during maturation. J Neurochem 15:1151-1158.
75. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R. 2003. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805-809.
76. Schroeter S, Levy AI, Blakely RD. 1997. Polarized expression of the antidepressant-sensitive serotonin transporter in epinephrine-synthesizing chromaffin cells of the rat adrenal gland. Mol Cell Neurosci 9:170-184.
77. Smith JC, Morrison DE, Ellenberger HH, Otto MR, Feldman JL. 1989. Brainstem projections to the major respiratory neuron populations in the medulla of the cat. J Comp Neurol 281:69-96.
78. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL. 1991. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254:726-729.
79. Smith JC, Butera RJ, Koshiya N, Negro CD, Wilson CG, Johnson SM. 2000. Respiratory rhythm generation in neonatal and adult mammals: the hybrid pacemaker-network model. Respir Physiol 122:131-147.
80. Strüder HK, Weicker H. 2001. Physiology and pathophysiology of the serotonergic system and its implications on mental and physical performance. Part II. Int J Sports Med 22:482-497.
81. Suzuki M, Nishina M, Nakamura S, Maruyama K. 2004. Benzodiazepine- sensitive GABAA receptors in the commissural subnucleus of the NTS are involved in the carotid chemoreceptor reflex in rats. Auton Neurosci 110:108-113.
82. Taylor NC, Li A, Nattie EE. 2005. Medullary serotonergic neurons modulate the ventilatory response to hypercapnia but not hypoxia in conscious rats. J Physiol 566:543-557.
83. Tryba AK, Pena F, Ramirez JM. 2006. Gasping activity in vitro: a rhythm dependent on 5-HT2A receptors. J Neurosci 26:2623-2634.
84. Van Bockstaele EJ, Pieribone VA, Aston-Jones G. 2004. Diverse afferents onverge on the nucleus paragigantocellularis in the rat ventrolateral medulla: Retrograde and anterograde tracing studies. J Comp Neurol 290:561-584.
85. Varoqui H, Erickson JD. 1997. Vesicular neurotransmitter transporters. Potential sites for the regulation of synaptic function. Mol Neurobiol 15:165-191.
86. Vitalis T, Cases O, Passemard S, Callebert J, Parnavelas JG. 2007. Embryonic depletion of serotonin affects cortical development. Eur J Neurosci 26:331-344.
87. Whitaker-Azmitia PM, Druse M, Walker P, Lauder JM. 1996. Serotonin as a developmental signal. Behav Brain Res 73:19-29.
88. Wong-Riley MTT, Liu Q. 2005. Neurochemical development of brainstem nuclei involved in the control of respiration. Respir Physiol Neurobiol 149:83-98.
89. Wong-Riley MT, Liu Q. 2008. Neurochemical and physiological correlates of a critical period of respiratory development in the rat. Respir Physiol Neurobiol 164:28-37.
90. Zagon A. 1993. Innervation of serotonergic medullary raphé neurons from cells of the rostral ventrolateral medulla in rats. Neuroscience 55:849-867.
91. Zec N, Kinney HC. 2001. Anatomic relationships of the human nucleus paragigantocellularis lateralis: a DiI labeling study. Auton Neurosci 89:110-124.
92. Zifa E, Fillion G. 1992. 5-Hydroxytryptamine receptors. Pharmacol Rev 44:401-458.