Serotonin in the inferior colliculus fluctuates with behavioral state and environmental stimuli

Journal of Experimental Biology

Volumn 213, Issue 7, 2010, Pages 1009-1017

  Hall, Ian C ^a   Rebec, George V ^a   Hurley, Laura M ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Auditory; Inferior colliculus; Neuromodulation; Sensory; Serotonin; Stress; Voltammetry

Indexed keywords

SEROTONIN;

ANESTHESIA; ANIMAL; ANIMAL BEHAVIOR; ARTICLE; ELECTRODE; ENVIRONMENT; INFERIOR COLLICULUS; MALE; METABOLISM; MOUSE; MOVEMENT (PHYSIOLOGY); PHYSIOLOGICAL STRESS; PHYSIOLOGY; STIMULATION; WAKEFULNESS;

ANESTHESIA; ANIMALS; BEHAVIOR, ANIMAL; ELECTRODES; ENVIRONMENT; INFERIOR COLLICULI; MALE; MICE; MOVEMENT; PHYSICAL STIMULATION; SEROTONIN; STRESS, PHYSIOLOGICAL; WAKEFULNESS;

MUS;

EID: 77951489488     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.035956     Document Type: Article

References (77)

1. Abrams, J. K., Johnson, P. L., Hollis, J. H. and Lowry, C. A. (2004). Anatomie and functional topography of the dorsal raphe nucleus. Ann. NY Acad. Sci. 1018, 46-57.
2. Adell, A., Celada, P., Abellan, M. T. and Artigas, F. (2002). Origin and functional role of the extracellular serotonin in the midbrain raphe nuclei. Brain Res. Rev. 39, 154-180.
3. Arnargós-Bosch, M., Analía Bortolozzi, M., Puig, V., Serrats, J., Adell, A., Celada, P., Toth, M., Mengod, G. and Artigas, F. (2004). Co-expression and in vivo interaction of serotonin 1A and serotonin 2A receptors in pyramidal neurons of prefrontal cortex. Cerebr. Cortex 14, 281-299.
4. Anastassiou, C. A., Patel, B. A., Arundell, M., Yeoman, M. S., Parker, K. H. and O'Hare, D. (2006). Subsecond voltammetric separation between dopamine and serotonin in the presence of ascorbate. Anal. Chem. 78, 6990-6998.
5. Astl, J., Popelář, J., Kvašňák, E. and Syka, J. (1996). Comparison of response properties of neurons in the inferior colliculus of guinea pigs under different anesthetics. Int. J. Audiol. 35, 335-345.
6. Auerbach, S. B., Minzenberg, M. J. and Wilkinson, L. O. (1989). Extracellular serotonin and 5-hydroxyindoleacetic acid in hypothalamus of the unanesthetized rat measured by in vivo dialysis coupled to high-performance liquid chromatography with electrochemical detection: dialysate serotonin reflects neuronal release. Brain Res. 499, 281-290.
7. Beekman, M., Flachskamm, C. and Linthorst, A. C. E. (2005). Effects of exposure to a predator on behaviour and serotonergic neurotransmission in different brain regions of C57blN mice. Eur. J. Neurosci. 21, 2825-2836.
8. Blier, P., Serrano, A. and Scatton, B. (1990). Differential responsiveness of the rat dorsal and median raphe 5-HT systems to 5-HT1 receptor agonists and pchloroamphetamine. Synapse 5, 120-133.
9. Boutelle, M. G., Zetterstrom, T., Pei, Q., Svensson, L. and Fillenz, M. (1990). in vivo neurochemical effects of tail pinch. J. Neurosci. Methods 34, 151-157.
10. Bouwknecht, J. A., Spiga, F., Staub, D. R., Hale, M. W., Shekhar, A. and Lowry, C. A. (2007). Differential effects of exposure to low-light or high-light open-field on anxiety-related behaviors: relationship to c-Fos expression in serotonergic and nonserotonergic neurons in the dorsal raphe nucleus. Brain Res. Bull. 72, 32-43.
11. Bowers, S. L., Bilbo, S. D., Dhabhar, F. S. and Nelson, R. J. (2007). Stressorspecific alterations in corticosterone and immune responses in mice. Brain Behav. Immun. 22, 105-113.
12. Brazell, M. P., Kasser, R. J., Renner, K. J., Feng, J., Moghaddarn, B. and Adams, R. N. (1987). Electrocoating carbon fiber microelectrodes with Nation improves selectivity for electroactive neurotransmitters. J. Neurosci. Methods 22, 167-172.
13. Bunin, M. A. and Wightman, R. M. (1998). Quantitative evaluation of 5hydroxytryptamine (serotonin) neuronal release and uptake: an investigation of extrasynaptic transmission. J. Neurosci. 18, 4854-4860.
14. Celada, P. and Artigas, F. (1993). 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. 347, 583-590.
15. Chen, Y.-P., Liu, S.-Y. and Yu, H.-Q. (2007). A simple and rapid method for measuring dissolved oxygen in waters with gold microelectrode. Anal. Chim. Acta 598, 249-253.
16. Clement, H. W., Kirsh, M., Hasse, C., Opper, C., Gernsa, D. and Wesemann, W. (1998). Effect of repeated immobilization on serotonin metablization in different brain areas and on serum corticosterone. J. Neural Transmission 105, 1155-1170.
17. Cransac, H., Cottet-Emard, J.-M., Hellstroëm, S. and Peyrin, L. (1998). Specific sound-induced noradrenergic and serotonergic activation in central auditory structures. Hearing Res. 118, 151-156.
18. Crespi, F. (1990). In vivo voltammetry with micro-biosensors for analysis of neurotransmitter release and metabolism. J. Neurosci. Methods 34, 53-65.
19. Crespi, F., Garratt, J. C., Sleight, A. J. and Marsden, C. A. (1990). In vivo evidence that 5-hydroxytryptamine (5HT) neuronal firing and release are not necessarily correlated with 5-HT metabolism. Neuroscience 35, 134-144.
20. Dahlin, A., Xia, L., Kong, W., Hevner, R. and Wang, J. (2007). Expression and immunolocalization of the plasma membrane monoamine transporter in the brain. Neuroscience 146, 1193-1211.
21. Day, H. E. W., Masini, C. V. and Campeau, S. (2009). Reversible inactivation of the auditory thalamus disrupts HPA axis habituation to repeated loud noise stress exposures. Brain Res. 1278, 123-130.
22. Ebert, U. and Ostwald, J. (1992). Serotonin modulates auditory information processing, in, the cochlear nucleus of the rat. Neurosci. Lett. 145, 51-54.
23. Fitzgerald, K. K. and Sanes, D. H. (1999). Serotonergic modulation of synapses in the developing gerbil lateral superior olive. J. Neurophysiol. 81, 2743-2752.
24. Fujino, K., Yoshitake, T., Inoue, O., Ibii, N., Kehr, J., Ishida, J., Nohta, H. and Yamaguchi, M. (2002). Increased serotonin release in mice frontal cortex and hippocampus induced by acute physiological stressors. Neurosci. Lett. 320, 91-95.
25. Gasser, P. J., Lowry, C. A. and Orchinik, M. (2006). Gorticosterone- sensitive monoamine transport in the rat dorsomedial hypothalamus: potential role for organic cation transporter 3 in stress-induced modulation of monoaminergic neurotransmission. J. Neurosci. 26, 8758-8766.
26. Gasser, P. J., Orchinik, M., Raju, I. and Lowry, C. A. (2009). Distribution of organic cation transporter 3, a corticosterone-sensitive monoamine transporter, in the rat brain. J. Comp. Neurol. 512, 529-555.
27. Gehlert, D. R., Thompson, L. K., Hemrick-Luecke, S. K. and Shaw, J. (2008). Monoaminergic compensation in the neuropeptide Y deficient mouse brain. Neuropeptides 42, 367-375.
28. Gonon, F. G., Fombariet, C. M., Buda, M. J. and Pujol, J. F. (1981). Electrochemical treatment of pyrolytic carbon fiber electrodes. Anal. Chem. 53, 1386-1389.
29. Grahn, R. E., Will, M. J., Hammack, S. E., Maswood, S., McQueen, M. B., Watkins, L. R. and Maier, S. F. (1999). Activation of serotonin-im m unoreactive cells in the dorsal raphe nucleus in rats exposed to an uncontrollable stressor. Brain Res. 826, 35-43.
30. Hajos, M., Gartside, S. E., Villa, A. E. and Sharp, T. (1995). Evidence for repetative (burst) firing in a sub-population of 5-hydroxytriptamine neurons in the dorsal and median raphe nuclei of the rat. Neuroscience 61, 189-197.
31. Hayley, S., Borowski, T., Merali, Z. and Anisman, H. (2001). Central monoamine activity in genetically distinct strains of mice following a psychogenic stressor: effects of predator exposure. Brain Res. 892, 293-300.
32. Hensler, J. G. (2006). Serotonergic modulation of the limbic system. Neurosci. Biobehav. Rev. 30, 203-214.
33. Heym, J., Trulson, M. E. and Jacobs, B. L. (1982). Raphe unit activity in freely moving cats: effects of phasic auditory and visual stimuli. Brain Res. 232, 29-39.
34. Heym, J., Steinfels, G. F. and Jacobs, B. L. (1984). Chloral hydrate anesthesia alters the responsiveness of central serotonergic neurons in the cat. Brain Res. 291, 63-72.
35. Hornung, J.-P. (2003). The human raphe nuclei and the serotonergic system. J. Chem. Neuroanat. 26, 331-343.
36. Houdouin, F., Cespuglio, R., Gharib, A., Sarda, N. and Jouvet, M. (1991). Detection of the release of 5-hydroxyindole compounds in the hypothalamus and the n. raphe dorsalis throughout the sleep-waking cycle and during stressful situations in the rat: a polygraphic and voltammetric approach. Exp. Brain Res. 85, 153-162.
37. Hurley, L. M. (2006). Different serotonin receptor agonists have distinct effects on sound-evoked responses in inferior colliculus. J. Neurophysiol. 96, 2177-2188.
38. Hurley, L. M. and Pollak, G. D. (1999). Serotonin differentially modulates responses to tones and frequency-modulated sweeps in the inferior colliculus. J. Neurosci. 19, 8071-8082.
39. Hurley, L. M. and Pollak, G. D. (2001). Serotonin effects on frequency tuning of inferior colliculus neurons. J. Neurophysiol. 85, 828-842.
40. Hurley, L. M. and Pollak, G. D. (2005a). Serotonin modulates responses to speciesspecific vocalizations in the inferior colliculus. J. Comp. Physiol. A 191, 535-546.
41. Hurley, L. M. and Pollak, G. D. (2005b). Serotonin shifts first-spike latencies of inferior colliculus neurons. J. Neurosci. 25, 7876-7886.
42. Hurley, L. M. and Thompson, A. M. (2001). Serotonergic innervation of the auditory brainstem of the Mexican free-tailed bat, Tadarida brasiliensis. J. Comp. Neurol. 435, 78-88.
43. Hurley, L. M., Thompson, A. M. and Pollak, G. D. (2002). Serotonin in the inferior colliculus. Hearing Res. 168, 1-11.
44. Hurley, L. M., Devilbiss, D. M. and Waterhouse, B. D. (2004). A matter of focus: monoaminergic modulation of stimulus coding in mammalian sensory networks. Curr. Opin. Neurobioi. 14, 488-495.
45. Inoue, T., Tsuchiya, K. and Koyama, T. (1994). Regional changes in dopamine and serotonin activation with various intensity of physical and psychological stress in the rat brain. Pharmacol. Biochem. Behav. 49, 911-920.
46. Jacobs, B. L. and Fornal, C. A. (1999). Activity of serotonergic neurons in behaving animals. Neuropsychopharmacoiogy 21, S9-S15.
47. Jaquins-Gerstl, A. and Michael, A. C. (2009). Comparison of the brain penetration injury associated with microdialysis and voltammetry. J. Neurosci. Methods 183, 127-135.
48. Klepper, A. and Herbert, H. (1991). Distribution and origin of norandrenergic and serotonergic fibers in the cochlear nucleus and the inferior colliculus of the rat. Brain Res. 557, 190-201.
49. Lanfumey, L., Mongeau, R., Cohen-Salmon, C. and Hamona, M. (2008). Corticosteroid-serotonin interactions in the neurobiological mechanisms of stressrelated disorders. Neurosci. Biobehav. Rev. 32, 1174-1184.
50. Lindefors, N., Barati, S. and O'Connor, W. T. (1997). Differential effects of single and repeated ketamine administration on dopamine, serotonin and GABA transmission in rat medial prefrontal cortex. Brain Res. 759, 205-212.
51. Linthorst, A. C. E. and Reul, J. M. (2007). Stress and the brain: solving the puzzle using microdialysis. Pharmacol. Biochem. Behav. 90, 163-173.
52. Marinesco, S. and Carew, T. J. (2002). Improved electrochemical detection of biogenic aminoes in Aplysia using base-hydrolyzed cellulose-coated carbon fiber microelectrodes. J. Neurosci. Methods 117, 87-97.
53. Marinesco, S., Poncet, L., Debilly, G., Jouvet, M. and Cespuglio, R. (1996). Effects of tianeptine, sertraline and clomipramine on brain serotonin metabolism: a voltammetric approach in the rat. Brain Res. 736, 82-90.
54. Mas, M., Fumero, B. and Gonzalez-Mora, J. L. (1995). Voltammetric and microdialysis monitoring of brain monoamine neurotransmitter release during sociosexual interactions. Behav. Brain Res. 71, 69-79.
55. Mitsushima, D., Yamada, K., Takase, K., Funabashi, T. and Kimura, F. (2006). Sex differences in the basolateral amygdala: The extracellular levels of serotonin and dopamine, and their responses to restraint stress in rats. Eur. J. Neurosci. 24, 3245-3254.
56. Molli ver, M. (1987). Serotonergic neuronal systems: what their anatomic organization tells us about function. J. Clin. Psychopharmacol. 7, S3-S23.
57. Morales-Cobas, G., Ferreira, M. I. and Velluti, R. A. (1995). Firing of inferior colliculus neurons in response to low-frequency sound stimulation during sleep and waking. J. Sleep Res. 4, 242-251.
58. Nakatani, Y., Sato-Suzuki, I., Tsujino, N., Nakasato, A., Seki, Y., Fumoto, M. and Arita, H. (2008). Augmented brain 5-HT crosses the blood-brain barrier through the 5-HT transporter in rat. Eur. J. Neurosci. 27, 2466-2472.
59. Okada, F., Saito, Y., Fujeida, T. and Yamashita, I. (1972). Monoamine changes in the brain of rats injected with L-5-hydroxytryptophan. Nature 238, 355-356.
60. Portas, C. M., Bjorvatn, B. and Ursin, R. (2000). Serotonin and the sleep/wake cycle: special emphasis on microdialysis studies. Prog. Neurobiol. 60, 13-35.
61. Pum, M., Huston, J. P., De Souza Silva, M. A. and Muller, C. P. (2008). Visual sensory-motor gating by serotonin activation in the medial prefrontal and occipital, but not in the rhinal, cortices in rats. Neuroscience 153, 361-372.
62. Rebec, G. V., Langley, P. E., Pierce, R. C., Wang, Z. and Heidenreich, B. A. (1993). A simple micromanipulator for multiple uses in freely moving rats: electrophysiology, voltammetry, and simultaneous intracerebral infusions. J. Neurosci. Methods 47, 53-59.
63. Rex, A., Voigt, J. P. and Fink, H. (2005). Anxiety but not arousal increases 5hydroxytryptamine release in the rat ventral hippocampus in vivo. Eur. J. Neurosci. 22, 1185-1189.
64. Rivot, J.-P., Cespuglio, R., Puig, S., Jouvet, M. and Besson, J.-M. (1995). In vivo electrochemical monitoring of serotonin in spinal dorsal horn with nafion-coated multi-carbon fiber electrodes. J. Neurochem. 65, 1257-1263.
65. Rueter, L. E. and Jacobs, B. L. (1996). A microdialysis examination of serotonin release in the rat forebrain induced by behavioural environmental manipulations. Brain Res. 739, 57-69.
66. Shimizu, N., Oomura, Y. and Aoyagi, K. (1989). Electrochemical analysis of hypothalamic serotonin metabolism accompanied by immobilization stress in rats. Physiol. Behav. 46, 829-834.
67. Smith, D. G., Davis, R. J., Gehlert, D. R. and Nomikos, G. G. (2006). 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. 1114, 24-30.
68. Stenfors, C. and Ross, S. B. (2004). Changes in extracellular 5-HIAA concentrations as measured by in vivo microdialysis technique in relation to changes in 5-HT release. Psychopharmacology 172, 119-128.
69. Takase, L. F. and Nogueira, M. I. (2008). Patterns of fos activation in rat raphe nuclei during feeding behavior. Brain Res. 1200, 10-18.
70. Torterolo, P., Falconi, A., Morales-Cobas, G. and Velluti, R. A. (2002). Inferior colliculus unitary activity in wakefulness, sleep and under barbiturates. Brain Res. 935, 9-15.
71. Trulson, M. E. (1985). Simultaneous recording of dorsal raphe unit activity and serotonin release in the striatum using voltammetry in awake, behaving cats. Life Sci. 37, 2199-2204.
72. Vahabzadeh, A. and Fillenz, M. (1994). Comparison of stress-induced changes in norandrenergic and serotonergic neurons in the rat hippocampus using microdialysis. Eur. J. Neurosci. 6, 1205-1212.
73. Vitale, G., Ar lett i, R. and Sandrini, M. (2005). Acute noise stress analgesia in relation to 5-HT2 and mu-opioid receptor changes in the frontal cortex of young mice. Life Sci. 77, 2500-2513.
74. Waterhouse, B. D., Mihailoff, G. A., Baack, J. C. and Woodward, D. J. (1986). Topographic distribution of dorsal and median raphe neurons projecting to motor, sensorimotor, and visual cortical areas in the rat. J. Comp. Neurol. 249, 460-476.
75. Waterhouse, B. D., Border, B., Wahl, L. and Mihailoff, G. A. (1993). Topographic organization of rat locus coeruleus and dorsal raphe nuclei: distribution of cells projecting to visaul system structures. J. Comp. Neurol. 336, 345-361.
76. Waterhouse, B., DeviIbIiss, D., Seiple, S. and Markowitz, R. (2004). Sensorimotorrelated discharge of simultaneously recorded, single neurons in the dorsal raphe nucleus of the awake, unrestrained rat. Brain Res. 1000, 183-191.
77. Woods, C. and Azeredo, W. (1999). Noradrenergic and serotonergic projections to the superior olive: potential for modulation of olivocochlear neurons. Brain Res. 836, 9-18.