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Abstract:

Here we applied behavioral testing, pharmacology, and in vivo electrophysiology to determine the function of the serotonin 5-HT5A receptor in goldfish startle plasticity and sensorimotor gating. In an initial series of behavioral experiments, we characterized the effects of a selective 5-HT5A antagonist, SB-699551 (3-cyclopentyl-N-[2-(dimethylamino)ethyl]-N-[(4-{[(2-phenylethyl)amino]methyl}-4- biphenylyl)methyl]propanamide dihydrochloride), on prepulse inhibition of the acoustic startle response. Those experiments showed a dose-dependent decline in startle rates in prepulse conditions. Subsequent behavioral experiments showed that SB-699551 also reduced baseline startle rates (i.e., without prepulse). To determine the cellular mechanisms underlying these behaviors, we tested the effects of two distinct selective 5-HT5A antagonists, SB-699551 and A-843277 (N-(2,6-dimethoxybenzyl)-N'[4-(4-fluorophenyl)thiazol- 2-yl]guanidine), on the intrinsic membrane properties and synaptic sound response of the Mauthner cell (M-cell), the decision-making neuron of the startle circuit. Auditory-evoked postsynaptic potentials recorded in the M-cell were similarly attenuated after treatment with either 5-HT5A antagonist (SB-699551, 26.41±3.98% reduction; A-843277, 17.52±6.24% reduction). This attenuation was produced by a tonic (intrinsic) reduction in M-cell input resistance, likely mediated by a Cl- conductance, that added to the extrinsic inhibition produced by an auditory prepulse. Interestingly, the effector mechanisms underlying neural prepulse inhibition itself were unaffected by antagonist treatment. In summary, these results provide an in vivo electrophysiological characterization of the 5-HT5A receptor and its behavioral relevance and provide a new perspective on the interaction of intrinsic and extrinsic modulatory mechanisms in startle plasticity and sensorimotor gating. © 2013 the authors.

Registro:

Documento: Artículo
Título:The 5-HT5A receptor regulates excitability in the auditory startle circuit: Functional implications for sensorimotor gating
Autor:Curtin, P.C.P.; Medan, V.; Neumeister, H.; Bronson, D.R.; Preuss, T.
Filiación:Graduate Center, City University of New York, New York, NY 10065, United States
Research Foundation, City University of New York, New York, NY10065, United States
Hunter College, City University of New York, New York, NY 10065, United States
Physiology and Molecular Biology Department, School of Science, University of Buenos Aires and IFIBYNE-CONICET, Ciudad Universitaria, Intendente Güiraldes 2160, 1428 Buenos Aires, Argentina
Palabras clave:serotonin 5A receptor; serotonin antagonist; biphenyl derivative; guanidine derivative; N (2,6 dimethoxybenzyl) N' (4 (4 fluorophenyl)thiazol 2 yl)guanidine; N-(2,6-dimethoxybenzyl)-N'-(4-(4-fluorophenyl)thiazol-2-yl)guanidine; potassium chloride; SB 699551 A; SB-699551-A; serotonin 5 receptor; serotonin antagonist; serotonin receptor; thiazole derivative; animal experiment; article; auditory stimulation; behavior; brain electrophysiology; chloride conductance; controlled study; evoked auditory response; excitatory postsynaptic potential; goldfish; Mauthner cell; nerve cell excitability; nerve cell membrane steady potential; nerve cell plasticity; nonhuman; prepulse inhibition; priority journal; sensory gating; startle reflex; swimming; acoustics; animal; cytology; dose response; drug effect; electrostimulation; evoked auditory response; female; inhibitory postsynaptic potential; male; metabolism; methodology; nerve cell; nerve cell inhibition; nerve cell network; nerve tract; patch clamp; physiology; sensory gating; spinal cord; time; Acoustic Stimulation; Acoustics; Animals; Biphenyl Compounds; Dose-Response Relationship, Drug; Electric Stimulation; Evoked Potentials, Auditory; Excitatory Postsynaptic Potentials; Female; Goldfish; Guanidines; Inhibitory Postsynaptic Potentials; Male; Nerve Net; Neural Inhibition; Neural Pathways; Neurons; Patch-Clamp Techniques; Potassium Chloride; Receptors, Serotonin; Sensory Gating; Serotonin Antagonists; Spinal Cord; Startle Reaction; Thiazoles; Time Factors
Año:2013
Volumen:33
Número:24
Página de inicio:10011
Página de fin:10020
DOI: http://dx.doi.org/10.1523/JNEUROSCI.4733-12.2013
Título revista:Journal of Neuroscience
Título revista abreviado:J. Neurosci.
ISSN:02706474
CODEN:JNRSD
CAS:potassium chloride, 7447-40-7; Biphenyl Compounds; Guanidines; N-(2,6-dimethoxybenzyl)-N'-(4-(4-fluorophenyl)thiazol-2-yl)guanidine; Potassium Chloride, 7447-40-7; Receptors, Serotonin; SB-699551-A; Serotonin Antagonists; Thiazoles; serotonin 5 receptor
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_02706474_v33_n24_p10011_Curtin

Referencias:

  • Antonsen, B.L., Edwards, D.H., Mechanisms of serotonergic facilitation of a command neuron (2007) J Neurophysiol, 98, pp. 3494-3504. , CrossRef Medline
  • Arias, B., Collier, D.A., Gast, O.C., Pintor, L., Gutiérrez, B., Vallèz, V., Fanãnás, L., Genetic variation in the 5-HT5A receptor gene in patients with bipolar disorder and major depression Neurosci Lett, 303, pp. 111-114. , CrossRef Medline
  • Barnes, N.M., Sharp, T., A review of central 5-HT receptors and their function (1999) Neuropharmacology, 38, pp. 1083-1152. , CrossRef Medline
  • Blumenthal, T.D., Prepulse inhibition decreases as startle reactivity habituates (1997) Psychophysiology, 34, pp. 446-450. , CrossRef Medline
  • Bosch, D., Schmid, S., Activation of muscarinic cholinergic receptors inhibits giantneurones in the caudal pontine reticular nucleus (2006) Eur J Neurosci, 24, pp. 1967-1975. , CrossRef Medline
  • Bosch, D., Schmid, S., Cholinergic mechanism underlying prepulse inhibition of the startle response in rats (2008) Neuroscience, 155, pp. 326-335. , CrossRef Medline
  • Braff, D.L., Prepulse inhibition of the startle reflex: A window on the brain in schizophrenia (2010) Curr Top Behav Neurosci, 4, pp. 349-371. , CrossRef Medline
  • Braff, D.L., Geyer, M.A., Swerdlow, N.R., Human studies of prepulse inhibition of startle: Normal subjects, patient groups, and pharmacological studies (2001) Psychopharmacology, 156, pp. 234-258. , CrossRef Medline
  • Burgess, H.A., Granato, M., Sensorimotor gating in larval zebrafish (2007) J Neurosci, 27, pp. 4984-4994. , CrossRef Medline
  • Corbett, D.F., Heightman, T.D., Moss, S.F., Bromidge, S.M., Coggon, S.A., Longley, M.J., Roa, A.M., Thomas, D.R., Discovery of a potent and selective 5-HT5A receptor antagonist by high-throughput chemistry (2005) Bioorg Med Chem Lett, 15, pp. 4014-4018. , CrossRef Medline
  • Cordova, M.S., Braun, C.B., The use of anesthesia during evoked potential audiometry in goldfish (2007) Brain Res, 1153, pp. 78-83. , CrossRef Medline
  • Diamond, J., Huxley, A.F., The activation and distribution of GABA and L-glutamate receptors on goldfish Mauthner neurons: An analysis of dendritic remote inhibition (1968) J Physiol, 194, pp. 669-723. , Medline
  • Diamond, J., Roper, S., Yasargil, G.M., The membrane effects, and sensitivity to strychnine, of neural inhibition of the Mauthner cell, and its inhibition by glycine and GABA (1973) J Physiol, 232, pp. 87-111. , Medline
  • Faber, D.S., Korn, H., Instantaneous inward rectification in the mauthner cell: A postsynaptic booster for excitatory inputs (1986) J Neurosci, 19, pp. 1037-1043. , CrossRef Medline
  • Faber, D.S., Fetcho, J.R., Korn, H., Neuronal networks underlying the escape response in goldfish (1989) Ann N Y Acad Sci, 563, pp. 11-33. , CrossRef Medline
  • Fendt, M., Li, L., Yeomans, J.S., Brain stem circuits mediating prepulse inhibition of the startle reflex (2001) Psychopharmacology, 156, pp. 216-224. , CrossRef Medline
  • Filip, M., Bader, M., Overview on 5-HT receptors and their role in physiology and pathology of the central nervous system (2009) Pharmacol Rep, 61, pp. 761-777. , Medline
  • Francken, B.J., Jurzak, M., Vanhauwe, J.F., Luyten, W.H., Leysen, J.E., The human 5-HT5A receptor couples toGi/Go proteins and inhibits adenylatecyclase in HEK293 cells (1998) Eur J Pharmacol, 361, pp. 299-309. , Medline
  • Fukami, Y., Furukawa, T., Asada, Y., Excitability changes of the Mauthner cell during collateral inhibition (1965) J Gen Physiol, 48, pp. 581-600. , CrossRef Medline
  • Furukawa, T., Ishii, Y., Neurophysiological studies on hearing in goldfish (1967) J Neurophysiol, 30, pp. 1377-1403. , Medline
  • Gannon, R.L., Peglion, J.L., Millan, M.J., Differential influence of selective 5-HT5A vs 5-HT1A, 5-HT1B, or 5-HT2C receptor blockade upon lightinduced phase shifts in circadian activity rhythms: Interaction studies with citalopram (2009) Eur Neuropsychopharmacol, 19, pp. 887-897. , CrossRef Medline
  • Goodfellow, N.M., Bailey, C.D., Lambe, E.K., The native serotonin 5-HT5A receptor: Electrophysiological characterization in rodent cortex and 5-HT1A-mediated compensatory plasticity in the knock-out mouse (2012) J Neurosci, 32, pp. 5804-5809. , CrossRef Medline
  • Gotow, T., Triller, A., Korn, H., Differential distribution of serotonergic inputs on the goldfish Mauthner cell (1990) J Comp Neurol, 292, pp. 255-268. , CrossRef Medline
  • Graham, F.K., Presidential Address, 1974: The more or less startling effects of weak prestimulation (1975) Psychophysiology, 12, pp. 238-248. , Medline
  • Hatta, K., Korn, H., Tonic inhibition alternatives in paired neurons that set direction of fish escape reaction (1999) Proc Natl Acad Sci U S A, 96, pp. 12090-12095. , CrossRef Medline
  • Hoffman, H.S., Ison, J.R., Reflex modification in the domain of startle. I. Some empirical findings and their implications for how the nervous system processes sensory input (1980) Psychol Rev, 87, pp. 175-189. , CrossRef Medline
  • Hurley, P.T., McMahon, R.A., Fanning, P., O'Boyle, K.M., Rogers, M., Martin, F., Functional coupling of a recombinant human 5-HT5a receptor to G- proteins in HEK-293 cells (1998) Br J Pharmacol, 124, pp. 1238-1244. , CrossRef Medline
  • Iwata, N., Ozaki, N., Inada, T., Goldman, D., Association of a 5-HT(5A) receptor polymorphism, Pro15Ser, to schizophrenia (2001) Mol Psychiatry, 6, pp. 217-219. , CrossRef Medline
  • Kassai, F., Schlumberger, C., Kedves, R., Pietraszek, M., Jatzke, C., Lendvai, B., Gyertyán, I., Danysz, W., Effect of 5-HT5A antagonists in animal models of schizophrenia, anxiety, and depression (2012) Behav Pharmacol, 23, pp. 397-406. , CrossRef Medline
  • Koch, M., The neurobiology of startle (1999) Prog Neurobiol, 59, pp. 107-128. , CrossRef Medline
  • Koch, M., Fendt, M., Startle response modulation as a behavioral tool in neuropharmacology (2003) Curr Neuropharmacol, 1, pp. 175-185. , CrossRef
  • Koch, M., Schnitzler, H.U., The acoustic startle response in rats - circuits mediating evocation, inhibition and potentiation (1997) Behav Brain Res, 89, pp. 35-49. , CrossRef Medline
  • Korn, H., Faber, D.S., The Mauthner cell a half a century later: A neurobiological model for decision-making? (2005) Neuron, 47, pp. 13-28. , CrossRef Medline
  • Korn, H., Burnod, Y., Faber, D.S., Spontaneous quantal currents in a central neuron match predictions from binomial analysis of evoked responses (1987) Proc Natl Acad Sci U S A, 84, pp. 5981-5985. , CrossRef Medline
  • Medan, V., Preuss, T., Dopaminergic-induced changes in Mauthner cell excitability disrupt prepulse inhibition in the startle circuit of goldfish (2011) J Neurophysiol, 106, pp. 3195-3204. , CrossRef Medline
  • Mintz, I., Korn, H., Serotonergic facilitation of quantal release at central inhibitory synapses (1991) J Neurosci, 11, pp. 3359-3370. , Medline
  • Nelson, D.L., 5-HT5 receptors (2004) Curr Drug Targets CNS Neurol Disord, 3, pp. 53-58. , CrossRef Medline
  • Neumeister, H., Szabo, T.M., Preuss, T., Behavioral and physiological characterization of sensorimotor gating in the goldfish startle response (2008) J Neurophysiol, 99, pp. 1493-1502. , CrossRef Medline
  • Neumeister, H., Whitaker, K.W., Hofmann, H.A., Preuss, T., Social and ecological regulation of a decision-making circuit (2010) J Neurophysiol, 104, pp. 3180-3188. , CrossRef Medline
  • Noda, M., Yasuda, S., Okada, M., Higashida, H., Shimada, A., Iwata, N., Ozaki, N., Wada, K., Recombinant human serotonin 5A receptors stably expressed in C6 glioma cells couple to multiple signal transduction pathways (2003) J Neurochem, 84, pp. 222-232. , CrossRef Medline
  • Noda, M., Higashida, H., Aoki, S., Wada, K., Multiple signal transduction pathways mediated by 5-HT receptors (2004) Mol Neurobiol, 29, pp. 31-39. , CrossRef Medline
  • Palmer, L.M., Mensinger, A.F., The effect of the anesthetic tricaine (MS- 222) on nerve activity in the anterior lateral line of the oyster toadfish, Opsanus tau (2004) J Neurophysiol, 92, pp. 1034-1041. , CrossRef Medline
  • Parwani, A., Duncan, E.J., Bartlett, E., Madonick, S.H., Efferen, T.R., Rajan, R., Sanfilipo, M., Rotrosen, J.P., Impaired prepulse inhibition of acoustic startle in schizophrenia (2000) Biol Psychiatry, 47, pp. 662-669. , CrossRef Medline
  • Pereda, A.E., Nairn, A.C., Wolszon, L.R., Faber, D.S., Postsynaptic modulation of synaptic efficacy at mixed synapses on the Mauthner cell (1994) J Neurosci, 14, pp. 3704-3712. , Medline
  • Preuss, T., Faber, D.S., Central cellular mechanisms underlying temperature- dependent changes in the goldfish startle-escape behavior (2003) J Neurosci, 23, pp. 5617-5626. , Medline
  • Sandner, G., Canal, N.M., Relationship between PPI and baseline startle response (2007) Cogn Neurodyn, 1, pp. 27-37. , CrossRef Medline
  • Schicatano, E.J., Peshori, K.R., Gopalaswamy, R., Sahay, E., Evinger, C., Reflex excitability regulates prepulse inhibition (2000) J Neurosci, 20, pp. 4240-4247. , Medline
  • Szabo, T.M., Weiss, S.A., Faber, D.S., Preuss, T., Representation of auditory signals in the M-cell: Role of electrical synapses (2006) J Neurophysiol, 95, pp. 2617-2629. , Medline
  • Thomas, D.R., 5-HT5A receptors as a therapeutic target (2006) Pharmacol Ther, 3, pp. 707-714. , CrossRef Medline
  • Thomas, E.A., Matli, J.R., Hu, J.L., Carson, M.J., Sutcliffe, J.G., Purtussistoxin treatment prevent 5-HT5A receptor-mediated inhibition of cyclic AMP accumulation in rat C6 glioma cells (2000) J Neurosci Res, 61, pp. 75-81. , CrossRef Medline
  • Weiss, S.A., Zottoli, S.J., Do, S.C., Faber, D.S., Preuss, T., Correlation of C-start behaviors with neural activity recorded from the hindbrain in freeswimming goldfish (Carassius auratus) (2006) J Exp Biol, 209, pp. 4788-4801. , CrossRef Medline
  • Weiss, S.A., Preuss, T., Faber, D.S., Phase encoding in the Mauthner sys-tem: Implications in left-right sound source discrimination (2009) J Neurosci, 29, pp. 3431-3441. , CrossRef Medline
  • Whitaker, K.W., Neumeister, H., Huffman, L.S., Kidd, C.E., Preuss, T., Hofmann, H.A., Serotonergic modulation of startle-escape plasticity in an African cichlid fish: A single-cell molecular and physiological analysis of a vital neural circuit (2011) J Neurophysiol, 106, pp. 127-137. , CrossRef Medline
  • Wolszon, L.R., Faber, D.S., The effects of postsynaptic levels of cyclic AMP on excitatory and inhibitory responses of an identified central neuron (1989) J Neurosci, 9, pp. 784-797. , Medline
  • Yeomans, J.S., Lee, J., Yeomans, M.H., Steidl, S., Li, L., Midbrain pathways for prepulse inhibition and startle activation in rat (2006) Neuroscience, 142, pp. 921-929. , CrossRef Medline
  • Yeomans, J.S., Bosch, D., Alves, N., Daros, A., Ure, R.J., Schmid, S., GABA receptors and prepulse inhibition of acoustic startle in mice and rats (2010) Eur J Neurosci, 31, pp. 2053-2061. , CrossRef Medline
  • Zottoli, S.J., Correlation of the startle reflex in Mauthner cell auditory responses in unrestrained goldfish (1977) J Exp Biol, 66, pp. 243-254. , Medline

Citas:

---------- APA ----------
Curtin, P.C.P., Medan, V., Neumeister, H., Bronson, D.R. & Preuss, T. (2013) . The 5-HT5A receptor regulates excitability in the auditory startle circuit: Functional implications for sensorimotor gating. Journal of Neuroscience, 33(24), 10011-10020.
http://dx.doi.org/10.1523/JNEUROSCI.4733-12.2013
---------- CHICAGO ----------
Curtin, P.C.P., Medan, V., Neumeister, H., Bronson, D.R., Preuss, T. "The 5-HT5A receptor regulates excitability in the auditory startle circuit: Functional implications for sensorimotor gating" . Journal of Neuroscience 33, no. 24 (2013) : 10011-10020.
http://dx.doi.org/10.1523/JNEUROSCI.4733-12.2013
---------- MLA ----------
Curtin, P.C.P., Medan, V., Neumeister, H., Bronson, D.R., Preuss, T. "The 5-HT5A receptor regulates excitability in the auditory startle circuit: Functional implications for sensorimotor gating" . Journal of Neuroscience, vol. 33, no. 24, 2013, pp. 10011-10020.
http://dx.doi.org/10.1523/JNEUROSCI.4733-12.2013
---------- VANCOUVER ----------
Curtin, P.C.P., Medan, V., Neumeister, H., Bronson, D.R., Preuss, T. The 5-HT5A receptor regulates excitability in the auditory startle circuit: Functional implications for sensorimotor gating. J. Neurosci. 2013;33(24):10011-10020.
http://dx.doi.org/10.1523/JNEUROSCI.4733-12.2013