You have full text access to this OnlineOpen article

Adenosine modulates transmission at the hippocampal mossy fibre synapse via direct inhibition of presynaptic calcium channels

  1. A. Gundlfinger1,2,
  2. J. Bischofberger3,
  3. F. W. Johenning1,
  4. M. Torvinen1,
  5. D. Schmitz1,2,
  6. J. Breustedt1

Article first published online: 25 JUN 2007

DOI: 10.1113/jphysiol.2007.132613

Issue

The Journal of Physiology

The Journal of Physiology

Volume 582, Issue 1, pages 263–277, July 2007

Additional Information

How to Cite

Gundlfinger, A., Bischofberger, J., Johenning, F. W., Torvinen, M., Schmitz, D. and Breustedt, J. (2007), Adenosine modulates transmission at the hippocampal mossy fibre synapse via direct inhibition of presynaptic calcium channels. The Journal of Physiology, 582: 263–277. doi: 10.1113/jphysiol.2007.132613

Author Information

  1. 1

    Neurowissenschaftliches Forschungszentrum der Charité, Universitätsmedizin Berlin, Germany

  2. 2

    Bernstein Center for Computational Neuroscience Berlin, Germany

  3. 3

    Physiologisches Institut der Universität Freiburg, Abteilung I, Freiburg, Germany

*Corresponding author J. Breustedt: Neuroscience Research Centre of the Charité, Universitätsmedizin Berlin, Germany. Email: joerg.breustedt@charite.de

  1. D. Schmitz and J. Breustedt contributed equally to this work. This paper has online Supplemental material.

Publication History

  1. Issue published online: 25 JUN 2007
  2. Article first published online: 25 JUN 2007
  3. (Resubmitted 17 March 2007; accepted after revision 1 May 2007; first published online 3 May 2007)

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (658K)

References

  • Bagley EE, Vaughan CW & Christie MJ (1999). Inhibition by adenosine receptor agonists of synaptic transmission in rat periaqueductal grey neurons. J Physiol 516, 219–225.
    Direct Link:
  • Bean BP (1989). Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature 340, 153–156.
  • Bischofberger J, Engel D, Li L, Geiger J & Jonas P (2006). Patch-clamp recordings from mossy fiber terminals in hippocampal slices. Nat Protoc 1, 2075–2081.
  • Bischofberger J, Geiger JR & Jonas P (2002). Timing and efficacy of Ca2+ channel activation in hippocampal mossy fiber boutons. J Neurosci 22, 10593–10602.
  • Blackmer T, Larsen EC, Takahashi M, Martin TF, Alford S & Hamm HE (2001). G protein βγ subunit-mediated presynaptic inhibition: regulation of exocytotic fusion downstream of Ca2+ entry. Science 292, 293–297.
  • Blatow M, Caputi A, Burnashev N, Monyer H & Rozov A (2003). Ca2+ buffer saturation underlies paired pulse facilitation in calbindin-D28k-containing terminals. Neuron 38, 79–88.
  • Breustedt J, Vogt KE, Miller RJ, Nicoll RA & Schmitz D (2003). α1E-containing Ca2+ channels are involved in synaptic plasticity. Proc Natl Acad Sci U S A 100, 12450–12455.
  • Brown SP, Safo PK & Regehr WG (2004). Endocannabinoids inhibit transmission at granule cell to Purkinje cell synapses by modulating three types of presynaptic calcium channels. J Neurosci 24, 5623–5631.
  • Castillo PE, Weisskopf MG & Nicoll RA (1994). The role of Ca2+ channels in hippocampal mossy fiber synaptic transmission and long-term potentiation. Neuron 12, 261–269.
  • Catterall WA (2000). Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol 16, 521–555.
  • Dietrich D, Kirschstein T, Kukley M, Von Der Pereverzev ABC, Schneider T & Beck H (2003). Functional specialization of presynaptic Cav2.3 Ca2+ channels. Neuron 39, 483–496.
  • Dittman JS & Regehr WG (1996). Contributions of calcium-dependent and calcium-independent mechanisms to presynaptic inhibition at a cerebellar synapse. J Neurosci 16, 1623–1633.
  • Dodge FA Jr & Rahamimoff R (1967). On the relationship between calcium concentration and the amplitude of the end-plate potential. J Physiol 189, 90P–92P.
  • Dunwiddie TV & Masino SA (2001). The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 24, 31–55.
  • Ebersolt C, Premont J, Prochiantz A, Perez M & Bockaert J (1983). Inhibition of brain adenylate cyclase by A1 adenosine receptors: pharmacological characteristics and locations. Brain Res 267, 123–129.
  • Egner A & Hell SW (2005). Fluorescence microscopy with super-resolved optical sections. Trends Cell Biol 15, 207–215.
  • Faber DS & Korn H (1991). Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys J 60, 1288–1294.
  • Fedele DE, Gouder N, Guttinger M, Gabernet L, Scheurer L, Rulicke T, Crestani F & Boison D (2005). Astrogliosis in epilepsy leads to overexpression of adenosine kinase, resulting in seizure aggravation. Brain 128, 2383–2395.
  • Forsythe ID (1994). Direct patch recording from identified presynaptic terminals mediating glutamatergic EPSCs in the rat CNS, in vitro. J Physiol 479, 381–387.
  • Fredholm BB, IJzerman AP, Jacobson KA, Klotz KN & Linden J (2001). International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol Rev 53, 527–552.
  • Gasparini S, Kasyanov AM, Pietrobon D, Voronin LL & Cherubini E (2001). Presynaptic R-type calcium channels contribute to fast excitatory synaptic transmission in the rat hippocampus. J Neurosci 21, 8715–8721.
  • Geiger JR, Bischofberger J, Vida I, Frobe U, Pfitzinger S, Weber HJ, Haverkampf K & Jonas P (2002). Patch-clamp recording in brain slices with improved slicer technology. Pflugers Arch 443, 491–501.
  • Geiger JR & Jonas P (2000). Dynamic control of presynaptic Ca2+ inflow by fast-inactivating K+ channels in hippocampal mossy fiber boutons. Neuron 28, 927–939.
  • Gerachshenko T, Blackmer T, Yoon EJ, Bartleson C, Hamm HE & Alford S (2005). Gβγ acts at the C terminus of SNAP-25 to mediate presynaptic inhibition. Nat Neurosci 8, 597–605.
  • Herlitze S, Garcia DE, Mackie K, Hille B, Scheuer T & Catterall WA (1996). Modulation of Ca2+ channels by G-protein βγ subunits. Nature 380, 258–262.
  • Huang YY, Li XC & Kandel ER (1994). cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79, 69–79.
  • Jeong HJ, Jang IS, Nabekura J & Akaike N (2003). Adenosine A1 receptor-mediated presynaptic inhibition of GABAergic transmission in immature rat hippocampal CA1 neurons. J Neurophysiol 89, 1214–1222.
  • Kajikawa Y, Saitoh N & Takahashi T (2001). GTP-binding protein βγ subunits mediate presynaptic calcium current inhibition by GABAB receptor. Proc Natl Acad Sci U S A 98, 8054–8058.
  • Kamiya H & Ozawa S (1998). Kainate receptor-mediated inhibition of presynaptic Ca2+ influx and EPSP in area CA1 of the rat hippocampus. J Physiol 509, 833–845.
    Direct Link:
  • Kamiya H & Ozawa S (1999). Dual mechanism for presynaptic modulation by axonal metabotropic glutamate receptor at the mouse mossy fibre-CA3 synapse. J Physiol 518, 497–506.
    Direct Link:
  • Kamiya H & Yamamoto C (1997). Phorbol ester and forskolin suppress the presynaptic inhibitory action of group-II metabotropic glutamate receptor at rat hippocampal mossy fibre synapse. Neuroscience 80, 89–94.
  • Kimura M, Saitoh N & Takahashi T (2003). Adenosine A1 receptor-mediated presynaptic inhibition at the calyx of Held of immature rats. J Physiol 553, 415–426.
    Direct Link:
  • Kukley M, Schwan M, Fredholm BB & Dietrich D (2005). The role of extracellular adenosine in regulating mossy fiber synaptic plasticity. J Neurosci 25, 2832–2837.
  • Luscher C, Jan LY, Stoffel M, Malenka RC & Nicoll RA (1997). G protein-coupled inwardly rectifying K+ channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19, 687–695.
  • Maccaferri G, Toth K & McBain CJ (1998). Target-specific expression of presynaptic mossy fiber plasticity. Science 279, 1368–1370.
  • MacDermott AB, Role LW & Siegelbaum SA (1999). Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci 22, 443–485.
  • Meinrenken CJ, Borst JG & Sakmann B (2002). Calcium secretion coupling at calyx of held governed by nonuniform channel-vesicle topography. J Neurosci 22, 1648–1667.
  • Miller RJ (1998). Presynaptic receptors. Annu Rev Pharmacol Toxicol 38, 201–227.
  • Mintz IM, Sabatini BL & Regehr WG (1995). Calcium control of transmitter release at a cerebellar synapse. Neuron 15, 675–688.
  • Miyazaki K, Ishizuka T & Yawo H (2005). Synapse-to-synapse variation of calcium channel subtype contributions in large mossy fiber terminals of mouse hippocampus. Neuroscience 136, 1003–1014.
  • Moore KA, Nicoll RA & Schmitz D (2003). Adenosine gates synaptic plasticity at hippocampal mossy fiber synapses. Proc Natl Acad Sci U S A 100, 14397–14402.
  • Nicoll RA & Schmitz D (2005). Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci 6, 863–876.
  • Patil PG, De Leon M, Reed RR, Dubel S, Snutch TP & Yue DT (1996). Elementary events underlying voltage-dependent G-protein inhibition of N-type calcium channels. Biophys J 71, 2509–2521.
  • Proctor WR & Dunwiddie TV (1987). Pre- and postsynaptic actions of adenosine in the in vitro rat hippocampus. Brain Res 426, 187–190.
  • Qian J & Saggau P (1999). Modulation of transmitter release by action potential duration at the hippocampal CA3-CA1 synapse. J Neurophysiol 81, 288–298.
  • Regehr WG & Tank DW (1991). Selective fura-2 loading of presynaptic terminals and nerve cell processes by local perfusion in mammalian brain slice. J Neurosci Methods 37, 111–119.
  • Ruiz A, Fabian-Fine R, Scott R, Walker MC, Rusakov DA & Kullmann DM (2003). GABAA receptors at hippocampal mossy fibers. Neuron 39, 961–973.
  • Sabatini BL & Regehr WG (1997). Control of neurotransmitter release by presynaptic waveform at the granule cell to Purkinje cell synapse. J Neurosci 17, 3425–3435.
  • Salin PA, Scanziani M, Malenka RC & Nicoll RA (1996). Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc Natl Acad Sci U S A 93, 13304–13309.
  • Sara Y, Virmani T, Deak F, Liu X & Kavalali ET (2005). An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 45, 563–573.
  • Scanziani M, Capogna M, Gahwiler BH & Thompson SM (1992). Presynaptic inhibition of miniature excitatory synaptic currents by baclofen and adenosine in the hippocampus. Neuron 9, 919–927.
  • Schmitz D, Mellor J, Breustedt J & Nicoll RA (2003). Presynaptic kainate receptors impart an associative property to hippocampal mossy fiber long-term potentiation. Nat Neurosci 6, 1058–1063.
  • Scholz KP & Miller RJ (1992). Inhibition of quantal transmitter release in the absence of calcium influx by a G protein-linked adenosine receptor at hippocampal synapses. Neuron 8, 1139–1150.
  • Takahashi T, Kajikawa Y & Tsujimoto T (1998). G-protein-coupled modulation of presynaptic calcium currents and transmitter release by a GABAB receptor. J Neurosci 18, 3138–3146.
  • Thompson SM, Capogna M & Scanziani M (1993). Presynaptic inhibition in the hippocampus. Trends Neurosci 16, 222–227.
  • Toth K & McBain CJ (2000). Target-specific expression of pre- and postsynaptic mechanisms. J Physiol 525, 41–51.
    Direct Link:
  • Trussell LO & Jackson MB (1985). Adenosine-activated potassium conductance in cultured striatal neurons. Proc Natl Acad Sci U S A 82, 4857–4861.
  • Tzounopoulos T, Janz R, Sudhof TC, Nicoll RA & Malenka RC (1998). A role for cAMP in long-term depression at hippocampal mossy fiber synapses. Neuron 21, 837–845.
  • Umemiya M & Berger AJ (1994). Activation of adenosine A1 and A2 receptors differentially modulates calcium channels and glycinergic synaptic transmission in rat brainstem. Neuron 13, 1439–1446.
  • Van Calker D, Muller M & Hamprecht B (1978). Adenosine inhibits the accumulation of cyclic AMP in cultured brain cells. Nature 276, 839–841.
  • Wang E, Babbey CM & Dunn KW (2005). Performance comparison between the high-speed Yokogawa spinning disc confocal system and single-point scanning confocal systems. J Microsc 218, 148–159.
    Direct Link:
  • Weisskopf MG, Castillo PE, Zalutsky RA & Nicoll RA (1994). Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 265, 1878–1882.
  • Wu LG & Saggau P (1994). Adenosine inhibits evoked synaptic transmission primarily by reducing presynaptic calcium influx in area CA1 of hippocampus. Neuron 12, 1139–1148.
  • Wu LG & Saggau P (1997). Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci 20, 204–212.
  • Yawo H & Chuhma N (1993). Preferential inhibition of ω-conotoxin-sensitive presynaptic Ca2+ channels by adenosine autoreceptors. Nature 365, 256–258.
  • Zucker RS & Regehr WG (2002). Short-term synaptic plasticity. Annu Rev Physiol 64, 355–405.
View Full Article (HTML) Get PDF (658K)