Mechanism of the medium-duration afterhyperpolarization in rat serotonergic neurons

[en] Most serotonergic neurons display a prominent medium-duration afterhyperpolarization (mAHP), which is mediated by small conductance Ca2+-activated K+ (SK) channels. Recent ex vivo and in vivo experiments have suggested that SK channel blockade increases the firing rate and/or bursting in these neurons. The purpose of this study was therefore to characterize the source of Ca2+ which activates the mAHP channels in serotonergic neurons. In voltage clamp experiments, an outward current was recorded at -60 mV after a depolarizing pulse to + 100 mV. A supra-maximal concentration of the SK channel blockers apamin or (-)- bicuculline methiodide blocked this outward current. This current was also sensitive to the broad Ca2+ channel blocker Co2+ and was partially blocked by both ω-conotoxin and mibefradil, which are blockers of N-type and T-type Ca2+ channels, respectively. Neither blockers of other voltage-gated Ca2+ channels nor DBHQ, an inhibitor of Ca2+-induced Ca2+ release, had any effect on the SK current.

Research Center/Unit :

Giga-Neurosciences - ULiège

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Alix, Philippe ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Pharmacologie

Venkatesan, Kumar

Scuvée-Moreau, Jacqueline

Massotte, Laurent ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques

Nguyen Trung, Mai-Linh ; Université de Liège - ULiège > 3e an. méd.

Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau

Seutin, Vincent ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Pharmacologie

Language :

English

Title :

Mechanism of the medium-duration afterhyperpolarization in rat serotonergic neurons

Publication date :

2014

Journal title :

European Journal of Neuroscience

ISSN :

0953-816X

eISSN :

1460-9568

Publisher :

Blackwell Science, Paris, France

Volume :

Issue :

Pages :

186-196

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique
BELSPO - Politique scientifique fédérale

Funding text :

Fonds Spéciaux de la recherche

Available on ORBi :

since 15 October 2013

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Bibliography

Adelman, J.P., Maylie, J. & Sah, P. (2012) Small-conductance Ca2+-activated K+ channels: form and function. Annu. Rev. Physiol., 74, 245-269.
Aghajanian, G.K. & Vandermaelen, C.P. (1982) Intracellular identification of central noradrenergic and serotonergic neurons by a new double labeling procedure. J. Neurosci., 2, 1786-1792.
Allen, D., Fakler, B., Maylie, J. & Adelman, J.P. (2007) Organization and regulation of small conductance Ca2+-activated K+ channel multiprotein complexes. J. Neurosci., 27, 2369-2376.
Beck, S.G., Pan, Y.Z., Akanwa, A.C. & Kirby, L.G. (2004) Median and dorsal raphe neurons are not electrophysiologically identical. J. Neurophysiol., 91, 994-1005.
Benington, J.H., Woudenberg, M.C. & Heller, H.C. (1995) Apamin, a selective SK potassium channel blocker, suppresses REM sleep without a compensatory rebound. Brain Res., 692, 86-92.
Blatz, A.L. & Magleby, K.L. (1986) Single apamin-blocked Ca-activated K+ channels of small conductance in cultured rat skeletal muscle. Nature, 323, 718-720.
Coulon, P., Herr, D., Kanyshkova, T., Meuth, P., Budde, T. & Pape, H.C. (2009) Burst discharges in neurons of the thalamic reticular nucleus are shaped by calcium-induced calcium release. Cell Calcium, 46, 333-346.
Crandall, S.R., Govindaiah, G. & Cox, C.L. (2010) Low-threshold Ca2+ current amplifies distal dendritic signaling in thalamic reticular neurons. J. Neurosci., 30, 15419-15429.
Crawford, L.K., Craige, C.P. & Beck, S.G. (2010) Increased intrinsic excitability of lateral wing serotonin neurons of the dorsal raphe: a mechanism for selective activation in stress circuits. J. Neurophysiol., 103, 2652-2663.
Davies, P.J., Ireland, D.R. & McLachlan, E.M. (1996) Sources of Ca2+ for different Ca(2+)-activated K+ conductances in neurones of the rat superior cervical ganglion. J. Physiol., 495(Pt 2), 353-366.
Defraiteur, C., Plenevaux, A., Scuvee-Moreau, J., Rouchet, N., Goblet, D., Luxen, A. & Seutin, V. (2007) Characterization of 4-(2-hydroxyphenyl)-1-[2'-[N-(2″-pyridinyl)-p-fluorobenzamido]ethyl]piperazine (p-DMPPF) as a new potent 5-HT1A antagonist. Brit. J. Pharmacol., 152, 952-958.
Deignan, J., Lujan, R., Bond, C., Riegel, A., Watanabe, M., Williams, J.T., Maylie, J. & Adelman, J.P. (2012) SK2 and SK3 expression differentially affect firing frequency and precision in dopamine neurons. Neuroscience, 217, 67-76.
Dreyfus, F.M., Tscherter, A., Errington, A.C., Renger, J.J., Shin, H.S., Uebele, V.N., Crunelli, V., Lambert, R.C. & Leresche, N. (2010) Selective T-type calcium channel block in thalamic neurons reveals channel redundancy and physiological impact of I(T)window. J. Neurosci., 30, 99-109.
Faber, E.S. (2010) Functional interplay between NMDA receptors, SK channels and voltage-gated Ca2+ channels regulates synaptic excitability in the medial prefrontal cortex. J. Physiol., 588, 1281-1292.
Fiorillo, C.D. & Williams, J.T. (1998) Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature, 394, 78-82.
Gartside, S.E., Hajos-Korcsok, E., Bagdy, E., Harsing, L.G. Jr., Sharp, T. & Hajos, M. (2000) Neurochemical and electrophysiological studies on the functional significance of burst firing in serotonergic neurons. Neuroscience, 98, 295-300.
Hajos, M., Gartside, S.E., Villa, A.E. & Sharp, T. (1995) Evidence for a repetitive (burst) firing pattern in a sub-population of 5-hydroxytryptamine neurons in the dorsal and median raphe nuclei of the rat. Neuroscience, 69, 189-197.
Hallworth, N.E., Wilson, C.J. & Bevan, M.D. (2003) Apamin-sensitive small conductance calcium-activated potassium channels, through their selective coupling to voltage-gated calcium channels, are critical determinants of the precision, pace, and pattern of action potential generation in rat subthalamic nucleus neurons in vitro. J. Neurosci., 23, 7525-7542.
Jacobs, B.L. & Fornal, C.A. (1991) Activity of brain serotonergic neurons in the behaving animal. Pharmacol. Rev., 43, 563-578.
Johnson, S.W. & Seutin, V. (1997) Bicuculline methiodide potentiates NMDA-dependent burst firing in rat dopamine neurons by blocking apamin-sensitive Ca2+-activated K+ currents. Neurosci. Lett., 231, 13-16.
Kohler, M., Hirschberg, B., Bond, C.T., Kinzie, J.M., Marrion, N.V., Maylie, J. & Adelman, J.P. (1996) Small-conductance, calcium-activated potassium channels from mammalian brain. Science, 273, 1709-1714.
Lang, D.G. & Ritchie, A.K. (1990) Tetraethylammonium blockade of apamin-sensitive and insensitive Ca2(+)-activated K+ channels in a pituitary cell line. J. Physiol., 425, 117-132.
Leinders, T. & Vijverberg, H.P. (1992) Ca2+ dependence of small Ca(2+)-activated K+ channels in cultured N1E-115 mouse neuroblastoma cells. Pflug. Arch.: Eur. J. Phy., 422, 223-232.
Michelsen, K.A., Schmitz, C. & Steinbusch, H.W. (2007) The dorsal raphe nucleus-from silver stainings to a role in depression. Brain Res. Rev., 55, 329-342.
Michelsen, K.A., Prickaerts, J. & Steinbusch, H.W. (2008) The dorsal raphe nucleus and serotonin: implications for neuroplasticity linked to major depression and Alzheimer's disease. Prog. Brain Res., 172, 233-264.
Moore, K.A., Cohen, A.S., Kao, J.P. & Weinreich, D. (1998) Ca2+-induced Ca2+ release mediates a slow post-spike hyperpolarization in rabbit vagal afferent neurons. J. Neurophysiol., 79, 688-694.
Ngo-Anh, T.J., Bloodgood, B.L., Lin, M., Sabatini, B.L., Maylie, J. & Adelman, J.P. (2005) SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines. Nat. Neurosci., 8, 642-649.
Paxinos, G. & Watson, C. (1998) The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic Press, San Diego.
Pedarzani, P., D'hoedt, D., Doorty, K.B., Wadsworth, J.D.F., Joseph, J.S., Jeyaseelan, K., Manjunatha Kini, R., Gadre, S.V., Sapatnekar, S.M., Stocker, M. & Strong, P.N. (2002) Tamapin, a venom peptide from the Indian red scorpion (Mesobuthus tamulus) that targets small conductance Ca2+-activated K+ channels and afterhyperpolarization currents in central neurons. J. Biol. Chem., 277, 46101-46109.
Pedarzani, P., McCutcheon, J.E., Rogge, G., Jensen, B.S., Christophersen, P., Hougaard, C., Strobaek, D. & Stocker, M. (2005) Specific enhancement of SK channel activity selectively potentiates the afterhyperpolarizing current I(AHP) and modulates the firing properties of hippocampal pyramidal neurons. J. Biol. Chem., 280, 41404-41411.
Penington, N.J. & Fox, A.P. (1995) Toxin-insensitive Ca current in dorsal raphe neurons. J. Neurosci., 15, 5719-5726.
Penington, N.J., Kelly, J.S. & Fox, A.P. (1992) Action potential waveforms reveal simultaneous changes in ICa and IK produced by 5-HT in rat dorsal raphe neurons. Proc. Biol. Sci., 248, 171-179.
Pineda, J.C., Waters, R.S. & Foehring, R.C. (1998) Specificity in the interaction of HVA Ca2+ channel types with Ca2+-dependent AHPs and firing behavior in neocortical pyramidal neurons. J. Neurophysiol., 79, 2522-2534.
Rouchet, N., Waroux, O., Lamy, C., Massotte, L., Scuvee-Moreau, J., Liegeois, J.F. & Seutin, V. (2008) SK channel blockade promotes burst firing in dorsal raphe serotonergic neurons. Eur. J. Neurosci., 28, 1108-1115.
Sah, P. (1995) Different calcium channels are coupled to potassium channels with distinct physiological roles in vagal neurons. Proc. Biol. Sci., 260, 105-111.
Sailer, C.A., Hu, H., Kaufmann, W.A., Trieb, M., Schwarzer, C., Storm, J.F. & Knaus, H.G. (2002) Regional differences in distribution and functional expression of small-conductance Ca2+-activated K+ channels in rat brain. J. Neurosci., 22, 9698-9707.
Scuvee-Moreau, J., Boland, A., Graulich, A., Van Overmeire, L., D'Hoedt, D., Graulich-Lorge, F., Thomas, E., Abras, A., Stocker, M., Liegeois, J.F. & Seutin, V. (2004) Electrophysiological characterization of the SK channel blockers methyl-laudanosine and methyl-noscapine in cell lines and rat brain slices. Brit. J. Pharmacol., 143, 753-764.
Scuvee-Moreau, J., Waroux, O., Alleva, L., Boland, A., Graulich, A., Liegeois, J.F. & Seutin, V. (2005) T-Type calcium channels do not play a major role in the activation of SK channels in rat midbrain dopaminergic neurons. Program No. 376.13. 2005 Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience, 2005. Online.
Seutin, V. & Johnson, S.W. (1999) Recent advances in the pharmacology of quaternary salts of bicuculline. Trends Pharmacol. Sci., 20, 268-270.
Seutin, V., Mkahli, F., Massotte, L. & Dresse, A. (2000) Calcium release from internal stores is required for the generation of spontaneous hyperpolarizations in dopaminergic neurons of neonatal rats. J. Neurophysiol., 83, 192-197.
Simic, G., Stanic, G., Mladinov, M., Jovanov-Milosevic, N., Kostovic, I. & Hof, P.R. (2009) Does Alzheimer's disease begin in the brainstem? Neuropath. Appl. Neuro., 35, 532-554.
Snyder, S.H. (2002) Neurobiology: serotonin sustains serenity. Nature, 416, 377-380.
Stocker, M. & Pedarzani, P. (2000) Differential distribution of three Ca(2+)-activated K(+) channel subunits, SK1, SK2, and SK3, in the adult rat central nervous system. Mol. Cell. Neurosci., 15, 476-493.
Stocker, M., Krause, M. & Pedarzani, P. (1999) An apamin-sensitive Ca2+-activated K+ current in hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. USA, 96, 4662-4667.
Umemiya, M. & Berger, A.J. (1994) Properties and function of low- and high-voltage-activated Ca2+ channels in hypoglossal motoneurons. J. Neurosci., 14, 5652-5660.
Vandermaelen, C.P. & Aghajanian, G.K. (1983) Electrophysiological and pharmacological characterization of serotonergic dorsal raphe neurons recorded extracellularly and intracellularly in rat brain slices. Brain Res., 289, 109-119.
Viana, F., Bayliss, D.A. & Berger, A.J. (1993) Multiple potassium conductances and their role in action potential repolarization and repetitive firing behavior of neonatal rat hypoglossal motoneurons. J. Neurophysiol., 69, 2150-2163.
Williams, S., Serafin, M., Muhlethaler, M. & Bernheim, L. (1997) Distinct contributions of high- and low-voltage-activated calcium currents to afterhyperpolarizations in cholinergic nucleus basalis neurons of the guinea pig. J. Neurosci., 17, 7307-7315.
Wolfart, J. & Roeper, J. (2002) Selective coupling of T-type calcium channels to SK potassium channels prevents intrinsic bursting in dopaminergic midbrain neurons. J. Neurosci., 22, 3404-3413.
Wolfart, J., Neuhoff, H., Franz, O. & Roeper, J. (2001) Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J. Neurosci., 21, 3443-3456.