Sodium and calcium mechanisms of rhythmic bursting in excitatory neural networks of the pre-Bötzinger complex: A computational modelling study

European Journal of Neuroscience

Volumn 37, Issue 2, 2013, Pages 212-230

  Jasinski, Patrick E ^a   Molkov, Yaroslav I ^a,b   Shevtsova, Natalia A ^a   Smith, Jeffrey C ^c   Rybak, Ilya A ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b INDIANA UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Ca2+ activated nonspecific cation current; Na+ K+ pump; Neural oscillations; Persistent Na+ current; Respiration

Indexed keywords

ARTICLE; BRAIN NERVE CELL; BRAIN STEM; CALCIUM CURRENT; CALCIUM TRANSPORT; MATHEMATICAL MODEL; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; PRE BOTZINGER COMPLEX; PRIORITY JOURNAL; RESPIRATORY BURST; SIGNAL TRANSDUCTION; SODIUM CURRENT; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; BRAIN STEM; CALCIUM; CALCIUM CHANNELS; HUMANS; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; POTASSIUM; SODIUM; SODIUM-POTASSIUM-EXCHANGING ATPASE; SPINAL CORD; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84872670622     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12042     Document Type: Article

References (56)

1. Anwyl, R. (1999) Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res. Rev., 29, 83-120.
2. Ballerini, L., Bracci, E. & Nistri, A. (1997) Pharmacological block of the electrogenic sodium pump disrupts rhythmic bursting induced by strychnine and bicuculline in the neonatal rat spinal cord. J. Neurophysiol., 77, 17-23.
3. Ben-Mabrouk, F., Amos, L.B. & Tryba, A.K. (2012) Metabotropic glutamate receptors (mGluR5) activate TRPC channels to improve the regularity of the respiratory rhythm generated by the pre-Bötzinger complex in mice. Eur. J. Neurosci., 35, 1725-1737.
4. Berridge, M.J. (1998) Neuronal calcium signaling. Neuron, 21, 13-26.
5. Bevan, M.D. & Wilson, C.J. (1999) Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J. Neurosci., 19, 7617-7628.
6. Butera, R.J., Rinzel, J. & Smith, J.C. (1999a) Models of respiratory rhythm generation in the pre-Bötzinger complex. I. Bursting pacemaker neurons. J. Neurophysiol., 82, 382-397.
7. Butera, R.J., Rinzel, J.R. & Smith, J.C. (1999b) Models of respiratory rhythm generation in the pre-Bötzinger complex: II. Populations of coupled pacemaker neurons. J. Neurophysiol., 82, 398-415.
8. Cohen, A., Rossignol, S. & Grillner, S. (eds) (1988) Neural Control of Rhythmic Movement in Vertebrates. Wiley, New York, NY.
9. Cowley, K.C. & Schmidt, B.J. (1995) Effects of inhibitory amino acid antagonists on reciprocal inhibitory interactions during rhythmic motor activity in the in vitro neonatal rat spinal cord. J. Neurophysiol., 74, 1109-1117.
10. Crowder, E.A., Saha, M.S., Pace, R.W., Zhang, H., Prestwich, G.D. & Del Negro, C.A. (2007) Phosphatidylinositol 4, 5-bisphosphate regulates inspiratory burst activity in the neonatal mouse prebotzinger complex. J. Physiol., 582 (Pt 3), 1047-1058.
11. Darbon, P., Tscherter, A., Yvon, C. & Streit, J. (2003) Role of the electrogenic Na/K pump in disinhibition-induced bursting in cultured spinal networks. J. Neurophysiol., 90, 3119-3129.
12. Del Negro, C.A., Koshiya, N., Butera, R.J. & Smith, J.C. (2002a) Persistent sodium current, membrane properties and bursting behavior of pre-botzinger complex inspiratory neurons in vitro. J. Neurophysiol., 88, 2242-2250.
13. Del Negro, C.A., Morgado-Valle, C. & Feldman, J.L. (2002b) Respiratory rhythm: an emergent network property? Neuron, 34, 821-830.
14. Del Negro, C.A., Morgado-Valle, C., Hayes, J.A., Mackay, D.D., Pace, R.W., Crowder, E.A. & Feldman, J.L. (2005) Sodium and calcium current-mediated pacemaker neurons and respiratory rhythm generation. J. Neurosci., 25, 446-453.
15. Del Negro, C.A., Kam, K., Hayes, J.A. & Feldman, J.L. (2009) Asymmetric control of inspiratory and expiratory phases by excitability in the respiratory network of neonatal mice in vitro. J. Physiol., 587, 1217-1231.
16. Doi, A. & Ramirez, J.M. (2010) State-dependent interactions between excitatory neuromodulators in the neuronal control of breathing. J. Neurosci., 30, 8251-8262.
17. Dunmyre, J.R., Del Negro, C.A. & Rubin, J.E. (2011) Interactions of persistent sodium and calcium-activated nonspecific cationic currents yield dynamically distinct bursting regimes in a model of respiratory neurons. J. Comput. Neurosci., 31, 305-328.
18. El Manira, A., Tegnér, J. & Grillner, S. (1994) Calcium-dependent potassium channels play a critical role for burst termination in the locomotor network in lamprey. J. Neurophysiol., 72, 1852-1861.
19. Elsen, F.P. & Ramirez, J.M. (1998) Calcium currents of rhythmic neurons recorded in the isolated respiratory network of neonatal mice. J. Neurosci., 18, 10652-10662.
20. Feldman, J.L. & Smith, J.C. (1989) Cellular mechanisms underlying modulation of breathing pattern in mammals. Ann. N. Y. Acad. Sci., 563, 114-130.
21. Gossard, J.P., Dubic, R. & Kolta, A. (eds) (2010) Breathe, walk and chew, vol 187. The neural challenge: Part 1, Progress in Brain Research, Elsevier, Oxford, UK, pp. 2-230.
22. Gray, P.A., Janczewski, W.A., Mellen, N., McCrimmon, D.R. & Feldman, J.L. (2001) Normal breathing requires preBotzinger complex neurokinin-1 receptor-expressing neurons. Nat. Neurosci., 4, 927-930.
23. Huguenard, J.R. & McCormick, D.A. (2004) Electrophysiology of the Neuron. An Interactive Tutorial. A Companion to Neurobiology by Gordon Shepherd. Oxford University Press, Oxford.
24. Johnson, S.M., Koshiya, N. & Smith, J.C. (2001) Isolation of the kernel for respiratory rhythm generation in a novel preparation: the pre-Bötzinger complex 'island'. J. Neurophysiol., 85, 1772-1776.
25. +-dominated leak currents contribute to respiratory rhythm generation in the pre-botzinger complex in vitro. J. Neurosci., 287, 1773-1785.
26. Koizumi, H., Wilson, C.G., Wong, S., Yamanishi, T., Koshiya, N. & Smith, J.C. (2008) Functional imaging, spatial reconstruction, and biophysical analysis of a respiratory motor circuit isolated in vitro. J. Neurosci., 28, 2353-2365.
27. Koshiya, N. & Smith, J.C. (1999) Neuronal pacemaker for breathing visualized in vitro. Nature, 400, 360-363.
28. Krey, R.A., Goodreau, A.M., Arnold, T.B. & Del Negro, C.A. (2010) Outward currents contributing to inspiratory burst termination in prebotzinger complex neurons of neonatal mice studied in vitro. Front. Neural Circuits, 4, 124.
29. 2+]i oscillations derived from a detailed kinetic model: a Hodgkin-Huxley like formalism. J. Theor. Biol., 166, 461-473.
30. Li, Y.X., Bertram, R. & Rinzel, J. (1996) Modeling N-methyl-D-aspartate-induced bursting in dopamine neurons. Neuroscience, 71, 397-410.
31. Lieske, S.P. & Ramirez, J.M. (2006) Pattern-specific synaptic mechanisms in a multifunctional network. I. Effects of alterations in synapse strength. J. Neurophysiol., 95, 1323-1333.
32. Lieske, S.P., Thoby-Brisson, M., Telgkamp, P. & Ramirez, J.M. (2000) Reconfiguration of the neural network controlling multiple breathing patterns: eupnea, sighs and gasps. Nat. Neurosci., 3, 600-607.
33. Mazza, E. Jr, Edelman, N.H. & Neubauer, J.A. (2000) Hypoxic excitation in neurons cultured from the rostral ventrolateral medulla of the neonatal rat. J. Appl. Physiol., 88, 2319-2329.
34. 2+-dependent conductances to membrane potential fluctuations of medullary respiratory neurons of newborn rats in vitro. J. Physiol., 552 (Pt 3), 727-741.
35. Pace, R.W. & Del Negro, C.A. (2008) AMPA and metabotropic glutamate receptors cooperatively generate inspiratory-like depolarization in mouse respiratory neurons in vitro. Eur. J. Neurosci., 28, 2434-2442.
36. Pace, R.W., Mackay, D.D., Feldman, J.L. & 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. J. Physiol., 582 (Pt 1), 113-125.
37. Peña, F. & Ramirez, J.M. (2004) Substance-P mediated modulation of pacemaker properties in the mammalian respiratory network. J. Neurosci., 24, 7549-7556.
38. Peña, F., Parkis, M.A., Tryba, A.K. & Ramirez, J.M. (2004) Differential contribution of pacemaker properties to the generation of respiratory rhythms during normoxia and hypoxia. Neuron, 43, 105-117.
39. Purvis, L.K., Smith, J.C., Koizumi, H. & Butera, R.J. (2007) Intrinsic bursters increase the robustness of rhythm generation in an excitatory network. J. Neurophysiol., 97, 1515-1526.
40. Ramirez, J.M., Quellmalz, U.J. & Richter, D.W. (1996) Postnatal changes in the mammalian respiratory network as revealed by the transverse brainstem slice of mice. J. Physiol., 491 (Pt 3), 819-812.
41. Rekling, J.C. & Feldman, J.L. (1998) PreBötzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu. Rev. Physiol., 60, 385-405.
42. Rubin, J.E., Hayes, J.A., Mendenhall, J.L. & Del Negro, C.A. (2009) Calcium-activated nonspecific cation current and synaptic depression promote network-dependent burst oscillations. Proc. Natl Acad. Sci. USA, 106, 2939-2944.
43. Rybak, I.A., Ptak, K., Shevtsova, N.A. & McCrimmon, D.R. (2003a) Sodium currents in neurons from the rostroventrolateral medulla of the rat. J. Neurophysiol., 90, 1635-1642.
44. Rybak, I.A., Shevtsova, N.A., St-John, W.M., Paton, J.F. & Pierrefiche, O. (2003b) Endogenous rhythm generation in the pre-Bötzinger complex and ionic currents: modelling and in vitro studies. Eur. J. Neurosci., 18, 239-257.
45. Rybak, I.A., Abdala, A.P., Markin, S.N., Paton, J.F. & Smith, J.C. (2007) Spatial organization and state-dependent mechanisms for respiratory rhythm and pattern generation. Prog. Brain Res., 165, 201-220.
46. Ryczko, D., Charrier, V., Ijspeert, A. & Cabelguen, J.M. (2010) Segmental oscillators in axial motor circuits of the salamander: distribution and bursting mechanisms. J. Neurophysiol., 104, 2677-2692.
47. Smith, J.C., Ellenberger, H.H., Ballanyi, K., Richter, D.W. & Feldman, J.L. (1991) Pre-Bötzinger complex: a brain stem region that may generate respiratory rhythm in mammals. Science, 254, 726-729.
48. Smith, J.C., Abdala, A.P., Koizumi, H., Rybak, I.A. & Paton, J.F. (2007) Spatial and functional architecture of the mammalian brain stem respiratory network: a hierarchy of three oscillatory mechanisms. J. Neurophysiol., 98, 3370-3387.
49. Stain, P.S.G., Grillner, S., Selverston, A.I. & Stuart, D.G. (eds) (1999) Neurons, Networks, and Motor Behavior. MIT Press, Cambridge, MA.
50. Thoby-Brisson, M. & Ramirez, J.M. (2001) Identification of two types of inspiratory pacemaker neurons in the isolated respiratory neural network of mice. J. Neurophysiol., 86, 104-112.
51. Toporikova, N. & Butera, R.J. (2011) Two types of independent bursting mechanisms in inspiratory neurons: an integrative model. J. Comput. Neurosci., 30, 515-528.
52. Tryba, A.K., Peña, F., Lieske, S.P., Viemari, J.C., Thoby-Brisson, M. & Ramirez, J.M. (2008) Differential modulation of neural network and pacemaker activity underlying eupnea and sigh-breathing activities. J. Neurophysiol., 99, 2114-2125.
53. Wallen, P., Robertson, B., Cangiano, L., Löw, P., Bhattacharjee, A., Kaczmarek, L.K. & Grillner, S. (2007) Sodium-dependent potassium channels of a Slack-like subtype contribute to the slow afterhyperpolarization in lamprey spinal neurons. J. Physiol., 585 (Pt 1), 75-90.
54. Yau, H.-J., Baranauskas, G. & Martina, M. (2010) Flufenamic acid decreases neuronal excitability through modulation of voltage-gated sodium channel gating. J. Physiol., 588, 3869-3882.
55. Yuan, A., Santi, C.M, Wei, A., Wang, Z.W., Pollak, K., Nonet, M., Kaczmarek, L., Crowder, C.M. & Salkoff, L. (2003) The sodium-activated potassium channel is encoded by a member of the Slo gene family. Neuron, 37, 765-773.
56. Zavala-Tecuapetla, C., Aguileta, M.A., Lopez-Guerrero, J.J., González-Marín, M.C. & Peña, F. (2008) Calcium-activated potassium currents differentially modulate respiratory rhythm generation. Eur. J. Neurosci., 27, 2871-2884.