Computational modeling predicts the ionic mechanism of late-onset responses in unipolar brush cells

Frontiers in Cellular Neuroscience

Volumn 8, Issue AUG, 2014, Pages

  Subramaniyam, Sathyaa ^a,b   Solinas, Sergio ^c   Perin, Paola ^a   Locatelli, Francesca ^a   Masetto, Sergio ^a   D'Angelo, Egidio ^a,c  

^a UNIVERSITY OF PAVIA   (Italy)

^b Consorzio Interuniversitario per le Scienze Fisiche della Materia ^*  (Italy)

^c C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

Author keywords

Biorealistic modeling; Ionic channel regulation; Slow synaptic responses; Unipolar brush cells; Vestibular cerebellum

Indexed keywords

ION CHANNEL;

ARTICLE; BRUSH BORDER; CALCIUM CURRENT; CELLULAR STRESS RESPONSE; CHANNEL GATING; COMPUTER MODEL; COMPUTER SIMULATION; ELECTRIC ACTIVITY; ELECTROSTIMULATION; HYPERPOLARIZATION; ION CURRENT; MOLECULAR MODEL; MOSSY FIBER; NERVE FIBER MEMBRANE CONDUCTANCE; NEUROTRANSMISSION; NONHUMAN; POTASSIUM CURRENT; SODIUM CURRENT; SYNAPSE; VOLTAGE CLAMP TECHNIQUE;

EID: 84907983111     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00237     Document Type: Article

References (80)

1. Achard, P., and De Schutter, E. (2006). Complex parameter landscape for a complex neuron model. PLoS Comput. Biol. 2: e94. doi: 10.1371/journal.pcbi.0020094
2. Afshari, F. S., Ptak, K., Khaliq, Z. M., Grieco, T. M., Slater, N. T., McCrimmon, D. R., et al. (2004). Resurgent Na currents in four classes of neurons of the cerebellum. J. Neurophysiol. 92, 2831-2843. doi: 10.1152/jn.00261.2004
3. Anwar, H., Hong, S., and De Schutter, E. (2012). Controlling Ca2+-activated K+ channels with models of Ca2+buffering in Purkinje cells. Cerebellum 11, 681-693. doi: 10.1007/s12311-010-0224-3
4. Bhalla, U. S., and Bower, J. M. (1993). Exploring parameter space in detailed single neuron models: simulations of the mitral and granule cells of the olfactory bulb. J. Neurophysiol. 69, 1948-1965.
5. Birnstiel, S., Slater, N. T., McCrimmon, D. R., Mugnaini, E., and Hartell, N. A. (2009). Voltage-dependent calcium signaling in rat cerebellar unipolar brush cells. Neuroscience 162, 702-712. doi: 10.1016/j.neuroscience.2009.01.051
6. Brown, D. A., Constanti, A., and Adams, P. R. (1981). Slow cholinergic and peptidergic transmission in sympathetic ganglia. Fed. Proc. 40, 2625-2630.
7. Clapham, D. E. (2003). TRP channels as cellular sensors. Nature 426, 517-524. doi: 10.1038/nature02196
8. Dai, M., Raphan, T., and Cohen, B. (2007). Labyrinthine lesions and motion sickness susceptibility. Exp. Brain Res. 178, 477-487. doi: 10.1007/s00221-006-0759-1
9. D'Angelo, E., De Filippi, G., Rossi, P., and Taglietti, V. (1995). Synaptic excitation of individual rat cerebellar granule cells in situ: evidence for the role of NMDA receptors. J. Physiol. 484(Pt 2), 397-413.
10. D'Angelo, E., De Filippi, G., Rossi, P., and Taglietti, V. (1998). Ionic mechanism of electroresponsiveness in cerebellar granule cells implicates the action of a persistent sodium current. J. Neurophysiol. 80, 493-503.
11. D'Angelo, E., Nieus, T., Maffei, A., Armano, S., Rossi, P., Taglietti, V., et al. (2001). Theta-frequency bursting and resonance in cerebellar granule cells: experimental evidence and modeling of a slow k+-dependent mechanism. J. Neurosci. 21, 759-770.
12. D'Angelo, E., Rossi, P., and Taglietti, V. (1993). Different proportions of N-methyl-D-aspartate and non-N-methyl-D-aspartate receptor currents at the mossy fibre-granule cell synapse of developing rat cerebellum. Neuroscience 53, 121-130. doi: 10.1016/0306-4522(93)90290-V
13. Davison, A. P., Hines, M. L., and Muller, E. (2009). Trends in programming languages for neuroscience simulations. Front. Neurosci. 3, 374-380. doi: 10.3389/neuro.01.036.2009
14. Dean, P., and Porrill, J. (2008). Adaptive-filter models of the cerebellum: computational analysis. Cerebellum 7, 567-571. doi: 10.1007/s12311-008-0067-3
15. De Schutter, E., and Smolen, P. (1998). "Calcium dynamics in large neuronal models, " in Methods in Neuronal Modeling: from Ions to Networks, 2nd Edn., eds C. Koch and I. Segev (Cambridge, MA: MIT Press), 211-250.
16. Destexhe, A., Contreras, D., Sejnowski, T. J., and Steriade, M. (1994). A model of spindle rhythmicity in the isolated thalamic reticular nucleus. J. Neurophysiol. 72, 803-818.
17. Diana, M. A., Otsu, Y., Maton, G., Collin, T., Chat, M., and Dieudonné, S. (2007). T-type and L-type Ca2+conductances define and encode the bimodal firing pattern of vestibulocerebellar unipolar brush cells. J. Neurosci. 27, 3823-3838. doi: 10.1523/JNEUROSCI.4719-06.2007
18. DiFrancesco, D., and Mangoni, M. (1994). Modulation of single hyperpolarization-activated channels (i(f) by cAMP in the rabbit sino-atrial node. J. Physiol. 474, 473-482.
19. Diño, M. R., and Mugnaini, E. (2000). Postsynaptic actin filaments at the giant mossy fiber-unipolar brush cell synapse. Synapse 38, 499-510.
20. Diwakar, S., Lombardo, P., Solinas, S., Naldi, G., and D'Angelo, E. (2011). Local field potential modeling predicts dense activation in cerebellar granule cells clusters under LTP and LTD control. PLoS ONE 6: e21928. doi: 10.1371/journal.pone.0021928
21. Diwakar, S., Magistretti, J., Goldfarb, M., Naldi, G., and D'Angelo, E. (2009). Axonal Na+ channels ensure fast spike activation and back-propagation in cerebellar granule cells. J. Neurophysiol. 101, 519-532. doi: 10.1152/jn.90382.2008
22. Dover, K., Solinas, S., D'Angelo, E., and Goldfarb, M. (2010). Long-term inactivation particle for voltage-gated sodium channels. J. Physiol. 588, 3695-3711. doi: 10.1113/jphysiol.2010.192559
23. Druckmann, S., Banitt, Y., Gidon, A., Schürmann, F., Markram, H., and Segev, I. (2007). A novel multiple objective optimization framework for constraining conductance-based neuron models by experimental data. Front. Neurosci. 1, 7-18. doi: 10.3389/neuro.01.1.1.001.2007
24. Druckmann, S., Berger, T. K., Hill, S., Schürmann, F., Markram, H., and Segev, I. (2008). Evaluating automated parameter constraining procedures of neuron models by experimental and surrogate data. Biol. Cybern. 99, 371-379. doi: 10.1007/s00422-008-0269-2
25. Druckmann, S., Berger, T. K., Schürmann, F., Hill, S., Markram, H., and Segev, I. (2011). Effective stimuli for constructing reliable neuron models. PLoS Comput. Biol. 7: e1002133. doi: 10.1371/journal.pcbi.1002133
26. Druckmann, S., Hill, S., Schürmann, F., Markram, H., and Segev, I. (2013). A hierarchical structure of cortical interneuron electrical diversity revealed by automated statistical analysis. Cereb. Cortex 23, 2994-3006. doi: 10.1093/cercor/bhs290
27. Fitz, J. G. (2007). Regulation of cellular ATP release. Trans. Am. Clin. Climatol. Assoc. 118, 199-208.
28. Forti, L., Cesana, E., Mapelli, J., and D'Angelo, E. (2006). Ionic mechanisms of autorhythmic firing in rat cerebellar Golgi cells. J. Physiol. 574, 711-729. doi: 10.1113/jphysiol.2006.110858
29. Gabbiani, F., Midtgaard, J., and Knpfel, T. (1994). Synaptic integration in a model of cerebellar granule cells. J. Neurophysiol. 72, 999-1009.
30. Gall, D., Roussel, C., Susa, I., D'Angelo, E., Rossi, P., Bearzatto, B., et al. (2003). Altered neuronal excitability in cerebellar granule cells of mice lacking calretinin. J. Neurosci. 23, 9320-9327.
31. Gao, Z., van Beugen, B. J., and De Zeeuw, C. I. (2012). Distributed synergistic plasticity and cerebellar learning. Nat. Rev. Neurosci. 13, 619-635. doi: 10.1038/nrn3312
32. Goldberg, J. M., Smith, C. E., and Fernández, C. (1984). Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J. Neurophysiol. 51, 1236-1256.
33. Gutfreund, Y., and Yarom, Y., and Segev, I. (1995). Subthreshold oscillations and resonant frequency in guinea-pig cortical neurons: physiology and modelling. J. Physiol. 483(Pt 3), 621-640.
34. Hildebrand, M. E., Isope, P., Miyazaki, T., Nakaya, T., Garcia, E., Feltz, A., et al., (2009). Functional coupling between mGluR1 and Cav3. 1 T-type calcium channels contributes to parallel fiber-induced fast calcium signaling within Purkinje cell dendritic spines. J. Neurosci. 29, 9668-9682. doi: 10.1523/JNEUROSCI.0362-09.2009
35. Hines, M. L., and Carnevale, N. T. (2001). NEURON: a tool for neuroscientists. Neuroscientist 7, 123-135. doi: 10.1177/107385840100700207
36. Hines, M. L., Morse, T. M., and Carnevale, N. T. (2007). Model structure analysis in NEURON: toward interoperability among neural simulators. Methods Mol. Biol. 401, 91-102. doi: 10.1007/978-1-59745-520-6_6
37. Hirschberg, B., Maylie, J., Adelman, J. P., and Marrion, N. V. (1998). Gating of recombinant small-conductance Ca-activated K+ channels by calcium. J. Gen. Physiol. 111, 565-581. doi: 10.1085/jgp.111.4.565
38. Hodgkin, A. L., and Huxley, A. F. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117, 500-544.
39. Kalinichenko, S. G., and Okhotin, V. E. (2005). Unipolar brush cells-a new type of excitatory interneuron in the cerebellar cortex and cochlear nuclei of the brainstem. Neurosci. Behav. Physiol. 35, 21-36. doi: 10.1023/B:NEAB.0000049648.20702.ad
40. Katz, B., and Miledi, R. (1964). Further observations on the distribution of Actylcholine-Reactive sites in skeletal muscle. J. Physiol. 170, 379-388.
41. Kennedy, A., Wayne, G., Kaifosh, P., Alviña, K., Abbott, L. F., and Sawtell, N. B. (2014). A temporal basis for predicting the sensory consequences of motor commands in an electric fish. Nat. Neurosci. 17, 416-422. doi: 10.1038/nn.3650
42. Khaliq, Z. M., Gouwens, N. W., and Raman, I. M. (2003). The contribution of resurgent sodium current to high-frequency firing in Purkinje neurons: an experimental and modeling study. J. Neurosci. 23, 4899-4912.
43. Khaliq, Z. M., and Raman, I. M. (2006). Relative contributions of axonal and somatic Na channels to action potential initiation in cerebellar Purkinje neurons. J. Neurosci. 26, 1935-1944. doi: 10.1523/JNEUROSCI.4664-05.2006
44. Locatelli, F., Bottà, L., Prestori, F., Masetto, S., and D'Angelo, E. (2013). Late-onset bursts evoked by mossy fibre bundle stimulation in unipolar brush cells: evidence for the involvement of H-and TRP-currents. J. Physiol. 591, 899-918. doi: 10.1113/jphysiol.2012.242180
45. Magistretti, J., Castelli, L., Forti, L., and D'Angelo, E. (2006). Kinetic and functional analysis of transient, persistent and resurgent sodium currents in rat cerebellar granule cells in situ: an electrophysiological and modelling study. J. Physiol. 573, 83-106. doi: 10.1113/jphysiol.2006.106682
46. McCormick, D. A., and Huguenard, J. R. (1992). A model of the electrophysiological properties of thalamocortical relay neurons. J. Neurophysiol. 68, 1384-1400.
47. McCormick, D. A., and Pape, H. C. (1990). Noradrenergic and serotonergic modulation of a hyperpolarization-activated cation current in thalamic relay neurones. J. Physiol. 431, 319-342.
48. McKay, B. E., Molineux, M. L., Mehaffey, W. H., and Turner, R. W. (2005). Kv1 K+ channels control Purkinje cell output to facilitate postsynaptic rebound discharge in deep cerebellar neurons. J. Neurosci. 25, 1481-1492. doi: 10.1523/JNEUROSCI.3523-04.2005
49. Morin, F., Diño, M. R., and Mugnaini, E. (2001). Postnatal differentiation of unipolar brush cells and mossy fiber-unipolar brush cell synapses in rat cerebellum. Neuroscience 104, 1127-1139. doi: 10.1016/S0306-4522(01)00144-0
50. Mugnaini, E., Diño, M. R., and Jaarsma, D. (1997). The unipolar brush cells of the mammalian cerebellum and cochlear nucleus: cytology and microcircuitry. Prog. Brain Res. 114, 131-150.
51. Mugnaini, E., and Floris, A. (1994). The unipolar brush cell: a neglected neuron of the mammalian cerebellar cortex. J. Comp. Neurol. 339, 174-180. doi: 10.1002/cne.903390203
52. Mugnaini, E., Sekerková, G., and Martina, M. (2011). The unipolar brush cell: a remarkable neuron finally receiving the deserved attention. Brain Res. Rev. 66, 220-245. doi: 10.1016/j.brainresrev.2010.10.001
53. Nieus, T., Sola, E., Mapelli, J., Saftenku, E., Rossi, P., and D'Angelo, E. (2006). LTP regulates burst initiation and frequency at mossy fiber-granule cell synapses of rat cerebellum: experimental observations and theoretical predictions. J. Neurophysiol. 95, 686-699. doi: 10.1152/jn.00696.2005
54. Nunzi, M. G., Birnstiel, S., Bhattacharyya, B. J., Slater, N. T., and Mugnaini, E. (2001). Unipolar brush cells form a glutamatergic projection system within the mouse cerebellar cortex. J. Comp. Neurol. 434, 329-341. doi: 10.1002/cne.1180
55. Nunzi, M. G., and Mugnaini, E. (2000). Unipolar brush cell axons form a large system of intrinsic mossy fibers in the postnatal vestibulocerebellum. J. Comp. Neurol. 422, 55-65. doi: 10.1002/(SICI)1096-9861(20000619)422:1%3C55::AID-CNE4%3E3.0.CO;2-9
56. Okada, T., Grunfeld, E., Shallo-Hoffmann, J., and Bronstein, A. M. (1999). Vestibular perception of angular velocity in normal subjects and in patients with congenital nystagmus. Brain 122(Pt 7), 1293-1303. doi: 10.1093/brain/122.7.1293
57. Palmer, L. M., Clark, B. A., Gründemann, J., Roth, A., Stuart, G. J., and Häusser, M. (2010). Initiation of simple and complex spikes in cerebellar Purkinje cells. J. Physiol. 588, 1709-1717. doi: 10.1113/jphysiol.2010.188300
58. Petersson, M. E., Yoshida, M., and Fransén, E. A. (2011). Low-frequency summation of synaptically activated transient receptor potential channel-mediated depolarizations. Eur. J. Neurosci. 34, 578-593. doi: 10.1111/j.1460-9568.2011.07791.x
59. Prestori, F., Rossi, P., Bearzatto, B., Lainé, J., Necchi, D., Diwakar, S., et al. (2008). Altered neuron excitability and synaptic plasticity in the cerebellar granular layer of juvenile prion protein knock-out mice with impaired motor control. J. Neurosci. 28, 7091-7103. doi: 10.1523/JNEUROSCI.0409-08.2008
60. Raman, I. M., and Bean, B. P. (1997). Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J. Neurosci. 17, 4517-4526.
61. Raman, I. M., and Bean, B. P. (2001). Inactivation and recovery of sodium currents in cerebellar Purkinje neurons: evidence for two mechanisms. Biophys. J. 80, 729-737. doi: 10.1016/S0006-3495(01)76052-3
62. Rossi, D. J., Alford, S., Mugnaini, E., and Slater, N. T. (1995). Properties of transmission at a giant glutamatergic synapse in cerebellum: the mossy fiber-unipolar brush cell synapse. J. Neurophysiol. 74, 24-42.
63. Roth, A., and Häusser, M. (2001). Compartmental models of rat cerebellar Purkinje cells based on simultaneous somatic and dendritic patch-clamp recordings. J. Physiol. 535, 445-472. doi: 10.1111/j.1469-7793.2001.00445.x
64. Rousseau, C. V., Dugué, G. P., Dumoulin, A., Mugnaini, E., Dieudonné, S., and Diana, M. A. (2012). Mixed inhibitory synaptic balance correlates with glutamatergic synaptic phenotype in cerebellar unipolar brush cells. J. Neurosci. 32, 4632-4644. doi: 10.1523/JNEUROSCI.5122-11.2012
65. Ruigrok, T. J., Hensbroek, R. A., and Simpson, J. I. (2011). Spontaneous activity signatures of morphologically identified interneurons in the vestibulocerebellum. J. Neurosci. 31, 712-724. doi: 10.1523/JNEUROSCI.1959-10.2011
66. Russo, M. J., Mugnaini, E., and Martina, M. (2007). Intrinsic properties and mechanisms of spontaneous firing in mouse cerebellar unipolar brush cells. Society 2, 709-724. doi: 10.1113/jphysiol.2007.129106
67. Russo, M. J., Yau, H. J., Nunzi, M. G., Mugnaini, E., and Martina, M. (2008). Dynamic metabotropic control of intrinsic firing in cerebellar unipolar brush cells. J. Neurophysiol. 100, 3351-3360. doi: 10.1152/jn.90533.2008
68. Santoro, B., Chen, S., Luthi, A., Pavlidis, P., Shumyatsky, G. P., Tibbs, G. R., et al. (2000). Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J. Neurosci. 20, 5264-5275.
69. Shen, B., Kwan, H. Y., Ma, X., Wong, C. O., Du, J., Huang, Y., et al. (2011). cAMP activates TRPC6 channels via the phosphatidylinositol 3-kinase (PI3K)-protein kinase B (PKB)-mitogen-activated protein kinase kinase (MEK)-ERK1/2 signaling pathway. J. Biol. Chem. 286, 19439-19445. doi: 10.1074/jbc.M110.210294
70. Solinas, S., Forti, L., Cesana, E., Mapelli, J., De Schutter, E., and D'Angelo, E. (2007a). Fast-reset of pacemaking and theta-frequency resonance patterns in cerebellar golgi cells: simulations of their impact In vivo. Front. Cell. Neurosci. 1: 4. doi: 10.3389/neuro.03.004.2007
71. Solinas, S., Forti, L., Cesana, E., Mapelli, J., De Schutter, E., and D'Angelo, E. (2007b). Computational reconstruction of pacemaking and intrinsic electroresponsiveness in cerebellar Golgi cells. Front. Cell. Neurosci. 1: 2. doi: 10.3389/neuro.03.002.2007
72. Traub, R. D. (1982). Simulation of intrinsic bursting in CA3 hippocampal neurons. Neuroscience 7, 1233-1242. doi: 10.1016/0306-4522(82)91130-7
73. Traub, R. D., and Llinás, R. (1979). Hippocampal pyramidal cells: significance of dendritic ionic conductances for neuronal function and epileptogenesis. J. Neurophysiol. 42, 476-496.
74. Traub, R. D., Wong, R. K., Miles, R., and Michelson, H. (1991). A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. J. Neurophysiol. 66, 635-650.
75. van Dorp, S., and De Zeeuw, C. I. (2014). Variable timing of synaptic transmission in cerebellar unipolar brush cells. Proc. Natl. Acad. Sci. U. S. A. 111, 5403-5408. doi: 10.1073/pnas.1314219111
76. Vanier, M. C., and Bower, J. M. (1999). A comparative survey of automated parameter-search methods for compartmental neural models. J. Comput. Neurosci. 7, 149-171. doi: 10.1023/A:1008972005316
77. Vos, B. P., Maex, R., Volny-Luraghi, A., and De Schutter, E. (1999). Parallel fibers synchronize spontaneous activity in cerebellar Golgi cells. J. Neurosci. 19, RC6.
78. Wainger, B. J., DeGennaro, M., Santoro, B., Siegelbaum, S. A., and Tibbs, G. R. (2001). Molecular mechanism of cAMP modulation of HCN pacemaker channels. Nature 411, 805-810. doi: 10.1038/35081088
79. Yamada, W. M., Koch, C., and Adams, P. R. (1989). "Multiple channels and calcium dynamics, " in Methods in Neuronal Modeling (Cambridge, MA: MIT Press), 137-170.
80. Zhou, F. W., Jin, Y., Matta, S. G., Xu, M., and Zhou, F. M. (2009). An ultra-short dopamine pathway regulates basal ganglia output. J. Neurosci. 29, 10424-10435. doi: 10.1523/JNEUROSCI.4402-08.2009