Context-dependent modulation of auditory processing by serotonin

Hearing Research

Volumn 279, Issue 1-2, 2011, Pages 74-84

  Hurley, L M ^a   Hall, I C ^b  

^a INDIANA UNIVERSITY   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SEROTONIN; SEROTONIN RECEPTOR;

ACOUSTIC NERVE FIBER; AGING; AROUSAL; AUDITORY RESPONSE; AUDITORY SYSTEM; AUTONOMIC INNERVATION; BEHAVIOR; COCHLEA INJURY; EVOKED AUDITORY RESPONSE; HEARING IMPAIRMENT; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SENSORY STIMULATION; SEROTONIN RELEASE; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM; SOCIAL INTERACTION; STIMULUS RESPONSE; STRESS; CONTEXT DEPENDENT MODULATION; HEARING; INNERVATION; POSTSYNAPTIC POTENTIAL; PROTEIN EXPRESSION; RAPHE NUCLEUS; REGULATORY MECHANISM; SEROTONERGIC PROJECTION; SOCIAL ASPECT;

EID: 84866528723     PISSN: 03785955     EISSN: 18785891     Source Type: Journal    
DOI: 10.1016/j.heares.2010.12.015     Document Type: Review

References (131)

1. Abrams J.K., Johnson P.L., Hollis J.H., Lowry C.A. Anatomic and functional topography of the dorsal raphe nucleus. Ann. N. Y Acad. Sci. 2004, 1018:46-57.
2. Adell A., Celada P., Abellan M.T., Artigas F. Origin and functional role of the extracellular serotonin in the midbrain raphe nuclei. Brain Res. Brain Res. Rev. 2002, 39:154-180.
3. Baldan Ramsey L.C., Sinha S.R., Hurley L.M. 5-HT1A and 5-HT1B receptors differentially modulate rate and timing of auditory responses in the mouse inferior colliculus. Eur. J. Neurosci. 2010, 32:368-379.
4. Barnes N.M., Sharp T. A review of central 5-HT receptors and their function. Neuropharmacology 1999, 38:1083-1152.
5. Basura G.J., Abbas A.I., O'Donohue H., Lauder J.M., Roth B.L., Walker P.D., Manis P.B. Ontogeny of serotonin and serotonin2A receptors in rat auditory cortex. Hear. Res. 2008, 244:45-50.
6. Beaudet A., Descarries L. The fine structure of central serotonin neurons. J. Physiol. (Paris) 1981, 77:193-203.
7. Bohorquez A., Hurley L.M. Activation of serotonin 3 receptors changes in vivo auditory responses in the mouse inferior colliculus. Hear. Res. 2009, 251:29-38.
8. Boutelle M.G., Zetterstrom T., Pei Q., Svensson L., Fillenz M. In vivo neurochemical effects of tail pinch. J. Neurosci. Methods 1990, 34:151-157.
9. Bunin M.A., Wightman R.M. Quantitative evaluation of 5-hydroxytryptamine (serotonin) neuronal release and uptake: an investigation of extrasynaptic transmission. J. Neurosci. 1998, 18:4854-4860.
10. Campbell M.J., Lewis D.A., Foote S.L., Morrison J.H. Distribution of choline acetyltransferase-, serotonin-, dopamine-beta-hydroxylase-, tyrosine hydroxylase-immunoreactive fibers in monkey primary auditory cortex. J. Comp. Neurol. 1987, 261:209-220.
11. Celada P., Artigas F. Monoamine oxidase inhibitors increase preferentially extracellular 5-hydroxytryptamine in the midbrain raphe nuclei. A brain microdialysis study in the awake rat. Naunyn Schmiedebergs Arch. Pharmacol. 1993, 347:583-590.
12. Chalmers D.T., Watson S.J. Comparative anatomical distribution of 5-HT1A receptor mRNA and 5-HT1A binding in rat brain-a combined in situ hybridisation/in vitro receptor autoradiographic study. Brain Res. 1991, 561:51-60.
13. Clement H.W., Kirsch M., Hasse C., Opper C., Gemsa D., Wesemann W. Effect of repeated immobilization on serotonin metabolism in different rat brain areas and on serum corticosterone. J. Neural Transm. 1998, 105:1155-1170.
14. Cransac H., Cottet-Emard J.M., Pequignot J.M., Peyrin L. Monoamines (noradrenaline, dopamine, serotonin) in the rat cochlear nuclei: endogenous levels and turnover. Hear. Res. 1995, 90:65-71.
15. Cransac H., Cottet-Emard J.M., Hellstrom S., Peyrin L. Specific sound-induced noradrenergic and serotonergic activation in central auditory structures. Hear. Res. 1998, 118:151-156.
16. Cransac H., Peyrin L., Cottet-Emard J.M., Farhat F., Pequignot J.M., Reber A. Aging effects on monoamines in rat medial vestibular and cochlear nuclei. Hear. Res. 1996, 100:150-156.
17. Cuccurazzu B., Halberstadt A.L. Projections from the vestibular nuclei and nucleus prepositus hypoglossi to dorsal raphe nucleus in rats. Neurosci. Lett. 2008, 439:70-74.
18. Dahlin A., Xia L., Kong W., Hevner R., Wang J. Expression and immunolocalization of the plasma membrane monoamine transporter in the brain. Neuroscience 2007, 146:1193-1211.
19. DeFelipe J., Hendry S.H., Hashikawa T., Jones E.G. Synaptic relationships of serotonin-immunoreactive terminal baskets on GABA neurons in the cat auditory cortex. Cereb. Cortex 1991, 1:117-133.
20. Ebert U., Ostwald J. Serotonin modulates auditory information processing in the cochlear nucleus of the rat. Neurosci. Lett. 1992, 145:51-54.
21. Edagawa Y., Saito H., Abe K. Endogenous serotonin contributes to a developmental decrease in long-term potentiation in the rat visual cortex. J. Neurosci. 2001, 21:1532-1537.
22. Edwards D.H., Yeh S.R., Musolf B.E., Antonsen B.L., Krasne F.B. Metamodulation of the crayfish escape circuit. Brain Behav. Evol. 2002, 60:360-369.
23. Faingold C.L., Gehlbach G., Caspary G.M. Functional pharmacology of inferior colliculus neurons. Neurobiology of Hearing: The Central Auditory System 1991, 223-251. Raven, New York. R.A. Altschuler (Ed.).
24. Fitzgerald K.K., Sanes D.H. Serotonergic modulation of synapses in the developing gerbil lateral superior olive. J. Neurophysiol. 1999, 81:2743-2752.
25. Fitzpatrick D., Diamond I.T., Raczkowski D. Cholinergic and monoaminergic innervation of the cat's thalamus: comparison of the lateral geniculate nucleus with other principal sensory nuclei. J. Comp. Neurol. 1989, 288:647-675.
26. Gasser P.J., Orchinik M., Raju I., Lowry C.A. Distribution of organic cation transporter 3, a corticosterone-sensitive monoamine transporter, in the rat brain. J. Comp. Neurol. 2009, 512:529-555.
27. Gil-Loyzaga P., Bartolome M.V., Vicente-Torres M.A. Serotonergic innervation of the organ of Corti of the cat cochlea. Neuroreport 1997, 8:3519-3522.
28. Grahn R.E., Will M.J., Hammack S.E., Maswood S., McQueen M.B., Watkins L.R., Maier S.F. Activation of serotonin-immunoreactive cells in the dorsal raphe nucleus in rats exposed to an uncontrollable stressor. Brain Res. 1999, 826:35-43.
29. Gu Q. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 2002, 111:815-835.
30. Hall I.C., Rebec G.V., Hurley L.M. Serotonin in the inferior colliculus fluctuates with behavioral state and environmental stimuli. J. Exp. Biol. 2010, 213:1009-1017.
31. Hall, I.C., Sell, G.L., Hurley, L.M., 2011. Social regulation of serotonin in the auditory midbrain. Behav. Neurosci., in press.
32. Hannon J., Hoyer D. Molecular biology of 5-HT receptors. Behav. Brain Res. 2008, 195:198-213.
33. Harris-Warrick R.M., Johnson B.R. Checks and balances in neuromodulation. Front. Behav. Neurosci. 2010, 4.
34. Hayley S., Borowski T., Merali Z., Anisman H. Central monoamine activity in genetically distinct strains of mice following a psychogenic stressor: effects of predator exposure. Brain Res. 2001, 892:293-300.
35. Hegerl U., Gallinat J., Juckel G. Event-related potentials. Do they reflect central serotonergic neurotransmission and do they predict clinical response to serotonin agonists?. J. Affect. Disord. 2001, 62:93-100.
36. Heym J., Steinfels G.F., Jacobs B.L. Activity of serotonin-containing neurons in the nucleus raphe pallidus of freely moving cats. Brain Res. 1982, 251:259-276.
37. Holt A.G., Asako M., Lomax C.A., MacDonald J.W., Tong L., Lomax M.I., Altschuler R.A. Deafness-related plasticity in the inferior colliculus: gene expression profiling following removal of peripheral activity. J. Neurochem. 2005, 93:1069-1086.
38. Holmstrom L.A., Eeuwes L.B., Roberts P.D., Portfors C.V. Efficient encoding of vocalizations in the auditory midbrain. J. Neurosci. 2010, 30:802-819.
39. Holy T.E., Guo Z. Ultrasonic songs of male mice. PLoS Biol. 2005, 3:e386.
40. Hoyer D., Hannon J.P., Martin G.R. Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol. Biochem. Behav. 2002, 71:533-554.
41. Hurley L.M. Different serotonin receptor agonists have distinct effects on sound-evoked responses in inferior colliculus. J. Neurophysiol. 2006, 96:2177-2188.
42. Hurley L.M. Activation of the serotonin 1A receptor alters the temporal characteristics of auditory responses in the inferior colliculus. Brain Res. 2007, 1181:21-29.
43. Hurley L.M., Park T., Brand A., Grothe B. In vivo neuromodulation of LSO neurons 2003, ARO Abstr #1247.
44. Hurley L.M., Pollak G.D. Serotonin differentially modulates responses to tones and frequency-modulated sweeps in the inferior colliculus. J. Neurosci. 1999, 19:8071-8082.
45. Hurley L.M., Pollak G.D. Serotonin effects on frequency tuning of inferior colliculus neurons. J. Neurophysiol. 2001, 85:828-842.
46. Hurley L.M., Thompson A.M. Serotonergic innervation of the auditory brainstem of the Mexican free-tailed bat, Tadarida brasiliensis. J. Comp. Neurol. 2001, 435:78-88.
47. Hurley L.M., Pollak G.D. Serotonin shifts first-spike latencies of inferior colliculus neurons. J. Neurosci. 2005, 25:7876-7886.
48. Hurley L.M., Pollak G.D. Serotonin modulates responses to species-specific vocalizations in the inferior colliculus. J. Comp. Physiol. A Neuroethol Sens Neural Behav. Physiol. 2005, 191:535-546.
49. Hurley L.M., Devilbiss D.M., Waterhouse B.D. A matter of focus: monoaminergic modulation of stimulus coding in mammalian sensory networks. Curr. Opin. Neurobiol. 2004, 14:488-495.
50. Hurley L.M., Tracy J.A., Bohorquez A. Serotonin 1B receptor modulates frequency response curves and spectral integration in the inferior colliculus by reducing GABAergic inhibition. J. Neurophysiol. 2008, 100:1656-1667.
51. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiol. Rev. 1992, 72:165-229.
52. Jacobs B.L., Fornal C.A. Activity of serotonergic neurons in behaving animals. Neuropsychopharmacology 1999, 21:9S-15S.
53. Ji W., Suga N. Serotonergic modulation of plasticity of the auditory cortex elicited by fear conditioning. J. Neurosci. 2007, 27:4910-4918.
54. Johnson R.G., Stevens K.E., Rose G.M. 5-Hydroxytryptamine2 receptors modulate auditory filtering in the rat. J. Pharmacol. Exp. Ther. 1998, 285:643-650.
55. Kaiser A., Covey E. 5-HT innervation of the auditory pathway in birds and bats. Acoustical Signal Processing in the Central Auditory System 1997, 71-78. Plenum, New York. J.L. Syka (Ed.).
56. Katz P.S. Neuromodulation intrinsic to the central pattern generator for escape swimming in Tritonia. Ann. N. Y. Acad. Sci. 1998, 860:181-188.
57. Kawano H., Decker K., Reuss S. Is there a direct retina-raphe-suprachiasmatic nucleus pathway in the rat?. Neurosci. Lett. 1996, 212:143-146.
58. Kiehn O., Harris-Warrick R.M. Serotonergic stretch receptors induce plateau properties in a crustacean motor neuron by a dual-conductance mechanism. J. Neurophysiol. 1992, 68:485-495.
59. Kim D.O., Yang X.M., Ye Y. A subpopulation of dorsal raphe nucleus neurons retrogradely labeled with cholera toxin-B injected into the inner ear. Exp. Brain Res. 2003, 153:514-521.
60. Klepper A., Herbert H. Distribution and origin of noradrenergic and serotonergic fibers in the cochlear nucleus and inferior colliculus of the rat. Brain Res. 1991, 557:190-201.
61. Klug A., Bauer E.E., Hanson J.T., Hurley L., Meitzen J., Pollak G.D. Response selectivity for species-specific calls in the inferior colliculus of Mexican free-tailed bats is generated by inhibition. J. Neurophysiol. 2002, 88:1941-1954.
62. Knudsen D.P., Gentner T.Q. Mechanisms of song perception in oscine birds. Brain Lang 2010.
63. Kosofsky B.E., Molliver M.E. The serotoninergic innervation of cerebral cortex: different classes of axon terminals arise from dorsal and median raphe nuclei. Synapse 1987, 1:153-168.
64. Kranz G.S., Kasper S., Lanzenberger R. Reward and the serotonergic system. Neurosci 2010, 166:1023-1035.
65. Lavoie B., Parent A. Serotoninergic innervation of the thalamus in the primate: an immunohistochemical study. J. Comp. Neurol. 1991, 312:1-18.
66. Le Moal M., Olds M.E. Peripheral auditory input to the midbrain limbic area and related structures. Brain Res. 1979, 167:1-17.
67. Lee H.S., Kim M.A., Valentino R.J., Waterhouse B.D. Glutamatergic afferent projections to the dorsal raphe nucleus of the rat. Brain Res. 2003, 963:57-71.
68. Lewis D.A., Campbell M.J., Foote S.L., Morrison J.H. The monoaminergic innervation of primate neocortex. Hum. Neurobiol. 1986, 5:181-188.
69. Liu J., Li X., Wang L., Dong Y., Han H., Liu G. Effects of salicylate on serotoninergic activities in rat inferior colliculus and auditory cortex. Hear. Res. 2003, 175:45-53.
70. Liu S., Bubar M.J., Lanfranco M.F., Hillman G.R., Cunningham K.A. Serotonin2C receptor localization in GABA neurons of the rat medial prefrontal cortex: implications for understanding the neurobiology of addiction. Neuroscience 2007, 146:1677-1688.
71. Luo X., Persico A.M., Lauder J.M. Serotonergic regulation of somatosensory cortical development: lessons from genetic mouse models. Dev. Neurosci. 2003, 25:173-183.
72. Manunta Y., Edeline J.M. Effects of noradrenaline on frequency tuning of rat auditory cortex neurons. Eur. J. Neurosci. 1997, 9:833-847.
73. Manunta Y., Edeline J.M. Noradrenergic induction of selective plasticity in the frequency tuning of auditory cortex neurons. J. Neurophysiol. 2004, 92:1445-1463.
74. Marriage J., Barnes N.M. Is central hyperacusis a symptom of 5-hydroxytryptamine (5-HT) dysfunction?. J. Laryngol. Otol. 1995, 109:915-921.
75. Mas M., Fumero B., Fernandez-Vera J.R., Gonzalez-Mora J.L. Neurochemical correlates of sexual exhaustion and recovery as assessed by in vivo microdialysis. Brain Res. 1995, 675:13-19.
76. McCormick D.A., Pape H.C. Noradrenergic and serotonergic modulation of a hyperpolarization-activated cation current in thalamic relay neurones. J. Physiol. 1990, 431:319-342.
77. Melo L.L., Brandão M.L. Role of 5-HT1A and 5-HT2 receptors in the aversion induced by electrical stimulation of inferior colliculus. Pharmacol. Biochem. Behav. 1995, 51:317-321.
78. Mendlin A., Martin F.J., Rueter L.E., Jacobs B.L. Neuronal release of serotonin in the cerebellum of behaving rats: an in vivo microdialysis study. J. Neurochem. 1996, 67:617-622.
79. Mesce K.A. Metamodulation of the biogenic amines: second-order modulation by steroid hormones and amine cocktails. Brain Behav. Evol. 2002, 60:339-349.
80. Miko I.J., Sanes D.H. Transient gain adjustment in the inferior colliculus is serotonin- and calcium-dependent. Hear. Res. 2009, 251:39-50.
81. Mitsushima D., Yamada K., Takase K., Funabashi T., Kimura F. Sex differences in the basolateral amygdala: the extracellular levels of serotonin and dopamine, and their responses to restraint stress in rats. Eur. J. Neurosci. 2006, 24:3245-3254.
82. Mizutani H., Hori T., Takahashi T. 5-HT1B receptor-mediated presynaptic inhibition at the calyx of Held of immature rats. Eur. J. Neurosci. 2006, 24:1946-1954.
83. Monckton J.E., McCormick D.A. Neuromodulatory role of serotonin in the ferret thalamus. J. Neurophysiol. 2002, 87:2124-2136.
84. Müller C.P., De Souza Silva M.A., Huston J.P. Double dissociating effects of sensory stimulation and cocaine on serotonin activity in the occipital and temporal cortices. Neuropharmacology 2007, 52:854-862.
85. Papadopoulos G.C., Parnavelas J.G. Monoamine systems in the cerebral cortex: evidence for anatomical specificity. Prog. Neurobiol. 1991, 36:195-200.
86. Pape H.C., McCormick D.A. Noradrenaline and serotonin selectively modulate thalamic burst firing by enhancing a hyperpolarization-activated cation current. Nature 1989, 340:715-718.
87. Peroutka S.J. Molecular biology of serotonin (5-HT) receptors. Synapse 1994, 18:241-260.
88. Peroutka S.J. 5-HT receptors: past, present and future. Trends Neurosci. 1995, 18:68-69.
89. Peruzzi D., Dut A. GABA, serotonin and serotonin receptors in the rat inferior colliculus. Brain Res. 2004, 998:247-250.
90. Peyron C., Petit J.M., Rampon C., Jouvet M., Luppi P.H. Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neurosci 1998, 82:443-468.
91. Pompeiano M., Palacios J.M., Mengod G. Distribution and cellular localization of mRNA coding for 5-HT1A receptor in the rat brain: correlation with receptor binding. J. Neurosci. 1992, 12:440-453.
92. Pompeiano M., Palacios J.M., Mengod G. Distribution of the serotonin 5-HT2 receptor family mRNAs: comparison between 5-HT2A and 5-HT2C receptors. Brain Res. Mol. Brain Res. 1994, 23:163-178.
93. Portas C.M., Bjorvatn B., Ursin R. Serotonin and the sleep/wake cycle: special emphasis on microdialysis studies. Prog. Neurobiol. 2000, 60:13-35.
94. Pum M.E., Huston J.P., De Souza Silva M.A., Muller C.P. Visual sensory-motor gating by serotonin activation in the medial prefrontal and occipital, but not in the rhinal, cortices in rats. Neuroscience 2008, 153:361-372.
95. Rao D., Basura G.J., Roche J., Daniels S., Mancilla J.G., Manis P.B. Hearing loss alters serotonergic modulation of intrinsic excitability in auditory cortex. J. Neurophysiol. 2010, 104:2693-2703.
96. Robinson S. Antidepressants for treatment of tinnitus. Prog. Brain Res. 2007, 166:263-271.
97. Rueter L.E., Jacobs B.L. A microdialysis examination of serotonin release in the rat forebrain induced by behavioral/environmental manipulations. Brain Res. 1996, 739:57-69.
98. Sakurai A., Darghouth N.R., Butera R.J., Katz P.S. Serotonergic enhancement of a 4-AP-sensitive current mediates the synaptic depression phase of spike timing-dependent neuromodulation. J. Neurosci. 2006, 26:2010-2021.
99. Sari Y. Serotonin1B receptors: from protein to physiological function and behavior. Neurosci. Biobehav. Rev. 2004, 28:565-582.
100. Simpson J.J., Davies W.E. A review of evidence in support of a role for 5-HT in the perception of tinnitus. Hear. Res. 2000, 145:1-7.
101. Smith D.G., Davis R.J., Gehlert D.R., Nomikos G.G. Exposure to predator odor stress increases efflux of frontal cortex acetylcholine and monoamines in mice: comparisons with immobilization stress and reversal by chlordiazepoxide. Brain Res. 2006, 1114:24-30.
102. Stark H., Scheich H. Dopaminergic and serotonergic neurotransmission systems are differentially involved in auditory cortex learning: a long-term microdialysis study of metabolites. J. Neurochem. 1997, 68:691-697.
103. Steinbusch H.W. Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neurosci 1981, 6:557-618.
104. Tadros S.F., D'Souza M., Zettel M.L., Zhu X., Lynch-Erhardt M., Frisina R.D. Serotonin 2B receptor: upregulated with age and hearing loss in mouse auditory system. Neurobiol. Aging 2007, 28:1112-1123.
105. Takase L.F., Nogueira M.I. Patterns of fos activation in rat raphe nuclei during feeding behavior. Brain Res. 2008, 1200:10-18.
106. Thompson A.M. Non-serotonergic lateral superior olivary neurons of the neonatal mouse contain serotonin. Brain Res. 2006, 1122:122-125.
107. Thompson A.M., Schofield B.R. Afferent projections of the superior olivary complex. Microsc. Res. Tech. 2000, 51:330-354.
108. Thompson A.M., Thompson G.C. Serotonin projection patterns to the cochlear nucleus. Brain Res. 2001, 907:195-207.
109. Thompson A.M., Wiechmann A.F. 5-HT(1A) receptor subtype mRNA expression in cochlear nucleus. Hear. Res. 2002, 164:77-81.
110. Thompson A.M., Hurley L.M. Dense serotonergic innervation of principal nuclei of the superior olivary complex in mouse. Neurosci. Lett. 2004, 356:179-182.
111. Thompson A.M., Thompson G.C. Experimental evidence that the serotonin transporter mediates serotonin accumulation in LSO neurons of the postnatal mouse. Brain Res. 2009, 1253:60-68.
112. Thompson A.M., Moore K.R., Thompson G.C. Distribution and origin of serotoninergic afferents to guinea pig cochlear nucleus. J. Comp. Neurol. 1995, 351:104-116.
113. Thompson G.C., Thompson A.M., Garrett K.M., Britton B.H. Serotonin and serotonin receptors in the central auditory system. Otolaryngol. Head Neck Surg. 1994, 110:93-102.
114. To Z.P., Bonhaus D.W., Eglen R.M., Jakeman L.B. Characterization and distribution of putative 5-ht7 receptors in guinea-pig brain. Br. J. Pharmacol. 1995, 115:107-116.
115. Trulson M.E. Simultaneous recording of dorsal raphe unit activity and serotonin release in the striatum using voltammetry in awake, behaving cats. Life Sci. 1985, 37:2199-2204.
116. Vahabzadeh A., Fillenz M. Comparison of stress-induced changes in noradrenergic and serotonergic neurons in the rat hippocampus using microdialysis. Eur. J. Neurosci. 1994, 6:1205-1212.
117. Vergé D., Calas A. Serotoninergic neurons and serotonin receptors: gains from cytochemical approaches. J. Chem. Neuroanat. 2000, 18:41-56.
118. Vertes R.P., Linley S.B., Hoover W.B. Pattern of distribution of serotonergic fibers to the thalamus of the rat. Brain Struct. Funct. 2010, 215:1-28.
119. Viemari J.C., Tryba A.K. Bioaminergic neuromodulation of respiratory rhythm in vitro. Respir. Physiol. Neurobiol. 2009, 168:69-75.
120. Vu D.H., Törk I. Differential development of the dual serotoninergic fiber system in the cerebral cortex of the cat. J. Comp. Neurol. 1992, 317:156-174.
121. Waeber C., Sebben M., Nieoullon A., Bockaert J., Dumuis A. Regional distribution and ontogeny of 5-HT4 binding sites in rodent brain. Neuropharmacology 1994, 33:527-541.
122. Wang H.T., Luo B., Huang Y.N., Zhou K.Q., Chen L. Sodium salicylate suppresses serotonin-induced enhancement of GABAergic spontaneous inhibitory postsynaptic currents in rat inferior colliculus in vitro. Hear Res. 2008, 236:42-51.
123. Wang X., Robertson D. Effects of bioamines and peptides on neurones in the ventral nucleus of trapezoid body and rostral periolivary regions of the rat superior olivary complex: an in vitro investigation. Hear Res. 1997, 106:20-28.
124. Waterhouse B.D., Devilbiss D., Seiple S., Markowitz R. Sensorimotor-related discharge of simultaneously recorded, single neurons in the dorsal raphe nucleus of the awake, unrestrained rat. Brain Res. 2004, 1000:183-191.
125. White S.A., Fisher S.E., Geschwind D.H., Scharff C., Holy T.E. Singing mice, songbirds, and more: models for FOXP2 function and dysfunction in human speech and language. J. Neurosci. 2006, 26:10376-10379.
126. Willard F.H., Ho R.H., Martin G.F. The neuronal types and the distribution of 5-hydroxytryptamine and enkephalin-like immunoreactive fibers in the dorsal cochlear nucleus of the North American opossum. Brain Res. Bull. 1984, 12:253-266.
127. Wright D.E., Seroogy K.B., Lundgren K.H., Davis B.M., Jennes L. Comparative localization of serotonin1A, 1C, and 2 receptor subtype mRNAs in rat brain. J. Comp. Neurol. 1995, 351:357-373.
128. Xiang Z., Prince D.A. Heterogeneous actions of serotonin on interneurons in rat visual cortex. J. Neurophysiol. 2003, 89:1278-1287.
129. Ye Y., Kim D.O. Connections between the dorsal raphe nucleus and a hindbrain region consisting of the cochlear nucleus and neighboring structures. Acta Otolaryngol. 2001, 121:284-288.
130. Zeng S., Li J., Zhang X., Zuo M. Distinction of neurochemistry between the cores and their shells of auditory nuclei in tetrapod species. Brain Behav. Evol. 2007, 70:1-20.
131. Zhang B., Harris-Warrick R.M. Multiple receptors mediate the modulatory effects of serotonergic neurons in a small neural network. J. Exp. Biol. 1994, 190:55-77.