• Please log in or register to access this feature.
You have full text access to this OnlineOpen article

Inspiratory bursts in the preBötzinger complex depend on a calcium-activated non-specific cation current linked to glutamate receptors in neonatal mice

  1. Ryland W. Pace1,
  2. Devin D. Mackay2,
  3. Jack L. Feldman2,
  4. Christopher A. Del Negro1,2

Article first published online: 25 JUN 2007

DOI: 10.1113/jphysiol.2007.133660

Issue

The Journal of Physiology

The Journal of Physiology

Volume 582, Issue 1, pages 113–125, July 2007

Additional Information

How to Cite

Pace, R. W., Mackay, D. D., Feldman, J. L. and Del Negro, C. A. (2007), Inspiratory bursts in the preBötzinger complex depend on a calcium-activated non-specific cation current linked to glutamate receptors in neonatal mice. The Journal of Physiology, 582: 113–125. doi: 10.1113/jphysiol.2007.133660

Author Information

  1. 1

    Department of Applied Science, McGlothlin-Street Hall, Room 303, The College of William and Mary, Williamsburg, VA 23187-8795, USA

  2. 2

    Systems Neurobiology Laboratory, Department of Neurobiology, David Geffen School of Medicine at the University of California Los Angeles, Box 951763, Los Angeles, CA 90095-1763, USA

*Corresponding author C. A. Del Negro: Department of Applied Science, McGlothlin-Street Hall, Room 303, The College of William and Mary, Williamsburg, VA 23187-8795, USA. Email: cadeln@wm.edu

  1. 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 29 March 2007; accepted 17 April 2007; first published online 19 April 2007)

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (597K)

References

  • Attwell D & Gibb A (2005). Neuroenergetics and the kinetic design of excitatory synapses. Nat Rev Neurosci 6, 841–849.
  • Barnes BJ, Tuong CM & Mellen NM (2007). Functional imaging reveals respiratory network activity during hypoxic and opioid challenge in the neonate rat tilted sagittal slab preparation. J Neurophysiol 97, 2283–2292.
  • Bellingham M (2006). Riluzole decreases synaptic excitation and repetitive firing in rat hypoglossal motor neurons. Society for Neuroscience Annual Meeting: Neuroscience 2006, Atlanta, GA, USA. 237.235.
  • Bocchiaro CM & Feldman JL (2004). Synaptic activity-independent persistent plasticity in endogenously active mammalian motoneurons. Proc Natl Acad Sci U S A 101, 4292–4295.
  • Brockhaus J & Ballanyi K (1998). Synaptic inhibition in the isolated respiratory network of neonatal rats. Eur J Neurosci 10, 3823–3839.
    Direct Link:
  • Canepari M, Papageorgiou G, Corrie JE, Watkins C & Ogden D (2001). The conductance underlying the parallel fibre slow EPSP in rat cerebellar Purkinje neurones studied with photolytic release of l-glutamate. J Physiol 533, 765–772.
    Direct Link:
  • Congar P, Leinekugel X, Ben-Ari Y & Crepel V (1997). A long-lasting calcium-activated nonselective cationic current is generated by synaptic stimulation or exogenous activation of group I metabotropic glutamate receptors in CA1 pyramidal neurons. J Neurosci 17, 5366–5379.
  • Del Negro CA, Koshiya N, Butera RJ Jr & Smith JC (2002a). Persistent sodium current, membrane properties and bursting behavior of pre-bötzinger complex inspiratory neurons in vitro. J Neurophysiol 88, 2242–2250.
  • Del Negro CA, Morgado-Valle C & Feldman JL (2002b). Respiratory rhythm: an emergent network property? Neuron 34, 821–830.
  • Del Negro CA, Morgado-Valle C, Hayes JA, Mackay DD, Pace RW, Crowder EA & Feldman JL (2005). Sodium and calcium dependent pacemaker neurons and respiratory rhythm generation. J Neurosci 25, 446–453.
  • Egorov AV, Hamam BN, Fransen E, Hasselmo ME & Alonso AA (2002). Graded persistent activity in entorhinal cortex neurons. Nature 420, 173–178.
  • Elsen FP & Ramirez JM (2005). Postnatal development differentially affects voltage-activated calcium currents in respiratory rhythmic versus nonrhythmic neurons of the pre-Bötzinger complex. J Neurophysiol 94, 1423–1431.
  • Feldman JL & Del Negro CA (2006). Looking for inspiration: new perspectives on respiratory rhythm. Nat Rev Neurosci 7, 232–241.
  • Ferraguti F & Shigemoto R (2006). Metabotropic glutamate receptors. Cell Tissue Res 326, 483–504.
  • Fransen E, Tahvildari B, Egorov AV, Hasselmo ME & Alonso AA (2006). Mechanism of graded persistent cellular activity of entorhinal cortex layer v neurons. Neuron 49, 735–746.
  • Frermann D, Keller BU & Richter DW (1999). Calcium oscillations in rhythmically active respiratory neurones in the brainstem of the mouse. J Physiol 515, 119–131.
    Direct Link:
  • Funk GD, Johnson SM, Smith JC, Dong XW, Lai J & Feldman JL (1997). Functional respiratory rhythm generating networks in neonatal mice lacking NMDAR1 gene. J Neurophysiol 78, 1414–1420.
  • Funk GD, Smith JC & Feldman JL (1993). Generation and transmission of respiratory oscillations in medullary slices: role of excitatory amino acids. J Neurophysiol 70, 1497–1515.
  • Funk GD, Smith JC & Feldman JL (1995). Modulation of neural network activity in vitro by cyclothiazide, a drug that blocks desensitization of AMPA receptors. J Neurosci 15, 4046–4056.
  • Gafni J, Munsch JA, Lam TH, Catlin MC, Costa LG, Molinski TF & Pessah IN (1997). Xestospongins: potent membrane permeable blockers of the inositol 1,4,5-trisphosphate receptor. Neuron 19, 723–733.
  • Ge Q & Feldman JL (1998). AMPA receptor activation and phosphatase inhibition affect neonatal rat respiratory rhythm generation. J Physiol 509, 255–266.
    Direct Link:
  • Greenwood IA & Large WA (1995). Comparison of the effects of fenamates on Ca-activated chloride and potassium currents in rabbit portal vein smooth muscle cells. Br J Pharmacol 116, 2939–2948.
  • Greer JJ, Smith JC & Feldman JL (1991). Role of excitatory amino acids in the generation and transmission of respiratory drive in neonatal rat. J Physiol 437, 727–749.
  • Harks EG, De Roos AD, Peters PH, De Haan LH, Brouwer A, Ypey DL, Van Zoelen EJ & Theuvenet AP (2001). Fenamates: a novel class of reversible gap junction blockers. J Pharmacol Exp Ther 298, 1033–1041.
  • Hofmann T, Chubanov V, Gudermann T & Montell C (2003). TRPM5 is a voltage-modulated and Ca2+-activated monovalent selective cation channel. Curr Biol 13, 1153–1158.
  • Janczewski WA & Feldman JL (2006). Distinct rhythm generators for inspiration and expiration in the juvenile rat. J Physiol 570, 407–420.
  • Kettunen P, Hess D & El Manira A (2003). mGluR1, but not mGluR5, mediates depolarization of spinal cord neurons by blocking a leak current. J Neurophysiol 90, 2341–2348.
  • Kochetkov KV, Kazachenko VN & Marinov BS (2000). Dose-dependent potentiation and inhibition of single Ca2+-activated K+ channels by flufenamic acid. Membr Cell Biol 14, 285–298.
  • Koshiya N & Smith JC (1999). Neuronal pacemaker for breathing visualized in vitro. Nature 400, 360–363.
  • Launay P, Fleig A, Perraud AL, Scharenberg AM, Penner R & Kinet JP (2002). TRPM4 is a Ca2+-activated nonselective cation channel mediating cell membrane depolarization. Cell 109, 397–407.
  • Lieske SP & Ramirez JM (2006). Pattern-specific synaptic mechanisms in a multifunctional network. II. Intrinsic modulation by metabotropic glutamate receptors. J Neurophysiol 95, 1334–1344.
  • Mironov SL & Richter DW (1998). L-type Ca2+ channels in inspiratory neurones of mice and their modulation by hypoxia. J Physiol 512, 75–87.
    Direct Link:
  • Mironov SL & Richter DW (2000). Hypoxic modulation of L-type Ca2+ channels in inspiratory brainstem neurones: intracellular signalling pathways and metabotropic glutamate receptors. Brain Res 869, 166–177.
  • Montell C (2005). The TRP superfamily of cation channels. Sci STKE 2005, re3.
  • Nistri A, Ostroumov K, Sharifullina E & Taccola G (2006). Tuning and playing a motor rhythm: how metabotropic glutamate receptors orchestrate generation of motor patterns in the mammalian central nervous system. J Physiol 572, 323–334.
    Direct Link:
  • Onimaru H, Ballanyi K & Homma I (2003). Contribution of Ca2+-dependent conductances to membrane potential fluctuations of medullary respiratory neurons of newborn rats in vitro. J Physiol 552, 727–741.
    Direct Link:
  • Onimaru H, Ballanyi K & Richter DW (1996). Calcium-dependent responses in neurons of the isolated respiratory network of newborn rats. J Physiol 491, 677–695.
  • Onimaru H & Homma I (2003). A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J Neurosci 23, 1478–1486.
  • Ottolia M & Toro L (1994). Potentiation of large conductance KCa channels by niflumic, flufenamic, and mefenamic acids. Biophys J 67, 2272–2279.
  • Paarmann I, Frermann D, Keller BU & Hollmann M (2000). Expression of 15 glutamate receptor subunits and various splice variants in tissue slices and single neurons of brainstem nuclei and potential functional implications. J Neurochem 74, 1335–1345.
    Direct Link:
  • Paarmann I, Frermann D, Keller BU, Villmann C, Breitinger HG & Hollmann M (2005). Kinetics and subunit composition of NMDA receptors in respiratory-related neurons. J Neurochem 93, 812–824.
    Direct Link:
  • Pace RW, Mackay DD, Feldman JL & Del Negro CA (2007). Role of persistent sodium current in mouse preBotzinger Complex neurons and respiratory rhythm generation. J Physiol 580, 485–496.
    Direct Link:
  • Partridge LD & Valenzuela CF (1999). Ca2+ store-dependent potentiation of Ca2+-activated non-selective cation channels in rat hippocampal neurones in vitro. J Physiol 521, 617–627.
    Direct Link:
  • Patneau DK, Mayer ML, Jane DE & Watkins JC (1992). Activation and desensitization of AMPA/kainate receptors by novel derivatives of willardiine. J Neurosci 12, 595–606.
  • Peña F, Parkis MA, Tryba AK & Ramirez JM (2004). Differential contribution of pacemaker properties to the generation of respiratory rhythms during normoxia and hypoxia. Neuron 43, 105–117.
  • Pierrefiche O, Haji A, Bischoff A & Richter DW (1999). Calcium currents in respiratory neurons of the cat in vivo. Pflugers Arch 438, 817–826.
  • Pressler RT & Strowbridge BW (2006). Blanes cells mediate persistent feedforward inhibition onto granule cells in the olfactory bulb. Neuron 49, 889–904.
  • Rekling JC, Champagnat J & Denavit-Saubie M (1996). Electroresponsive properties and membrane potential trajectories of three types of inspiratory neurons in the newborn mouse brain stem in vitro. J Neurophysiol 75, 795–810.
  • Rekling JC & Feldman JL (1997a). Bidirectional electrical coupling between inspiratory motoneurons in the newborn mouse nucleus ambiguus. J Neurophysiol 78, 3508–3510.
  • Rekling JC & Feldman JL (1997b). Calcium-dependent plateau potentials in rostral ambiguus neurons in the newborn mouse brain stem in vitro. J Neurophysiol 78, 2483–2492.
  • Rekling JC & Feldman JL (1998). Preötzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu Rev Physiol 60, 385–405.
  • Ruangkittisakul A, Schwarzacher SW, Secchia L, Poon BY, Ma Y, Funk GD & Ballanyi K (2006). High sensitivity to neuromodulator-activated signaling pathways at physiological [K+] of confocally imaged respiratory center neurons in on-line-calibrated newborn rat brainstem slices. J Neurosci 26, 11870–11880.
  • Sakmann B & Neher E (1995). Single-Channel Recording. Plenum Press, New York .
  • Schiller Y (2004). Activation of a calcium-activated cation current during epileptiform discharges and its possible role in sustaining seizure-like events in neocortical slices. J Neurophysiol 92, 862–872.
  • Sharifullina E, Ostroumov K & Nistri A (2004). Activation of group I metabotropic glutamate receptors enhances efficacy of glutamatergic inputs to neonatal rat hypoglossal motoneurons in vitro. Eur J Neurosci 20, 1245–1254.
    Direct Link:
  • Smith JC, Ellenberger HH, Ballanyi K, Richter DW & Feldman JL (1991). Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254, 726–729.
  • Stuart G, Spruston N & Häusser M (1999). Dendrites. Oxford University Press, Oxford, New York .
  • Teulon J (2000). Ca2+-activated nonselective cation channels. In Pharmacology of Ionic Channel Function: Activators and Inhibitors, ed. EndoM, KurachiY, MishinaM, pp. 625–649. Springer-Verlag, Berlin .
  • Trussell LO & Fischbach GD (1989). Glutamate receptor desensitization and its role in synaptic transmission. Neuron 3, 209–218.
  • Trussell LO, Zhang S & Raman IM (1993). Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10, 1185–1196.
  • Tryba AK, Peña F & Ramirez JM (2006). Gasping activity in vitro: A rhythm dependent on 5-HT2A receptors. J Neurosci 26, 2623–2634.
  • Ullrich ND, Voets T, Prenen J, Vennekens R, Talavera K, Droogmans G & Nilius B (2005). Comparison of functional properties of the Ca2+-activated cation channels TRPM4 and TRPM5 from mice. Cell Calcium 37, 267–278.
  • Zhu ZT, Munhall A, Shen KZ & Johnson SW (2004a). Calcium-dependent subthreshold oscillations determine bursting activity induced by N-methyl-d-aspartate in rat subthalamic neurons in vitro. Eur J Neurosci 19, 1296–1304.
    Direct Link:
  • Zhu ZT, Munhall A, Shen KZ & Johnson SW (2004b). Involvement of Ca2+-activated nonselective cation conductance in potentiation of depolarization-gated inward currents evoked by NMDA in subthalamic neurons. Society for Neuroscience 34th Annual Meeting, San Diego, CA, USA. 169.162.
View Full Article (HTML) Get PDF (597K)