Increased firing frequency of spontaneous action potentials in cerebellar Purkinje neurons of db/db mice results from altered auto-rhythmicity and diminished GABAergic tonic inhibition

General Physiology and Biophysics

Volumn 33, Issue 1, 2014, Pages 29-41

  Forero Vivas, María E ^a   Hernández Cruz, Arturo ^b  

^a CENTRO DE INVESTIGACIONES   (Colombia)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Cerebellum; Firing frequency; GABAergic inhibition; Leptin receptor; Patch clamp

Indexed keywords

ACTION POTENTIALS; ANIMALS; BICUCULLINE; CEREBELLUM; ELECTROPHYSIOLOGY; GABA-A RECEPTOR ANTAGONISTS; LEPTIN; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR SKILLS; NEURONS; PERIODICITY; PURKINJE CELLS; RECEPTORS, GABA-A; RECEPTORS, LEPTIN; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 84894170518     PISSN: 02315882     EISSN: 13384325     Source Type: Journal    
DOI: 10.4149/gpb_2013056     Document Type: Article

References (64)

1. Antkowiak B., Heckj D. (1997): Effects of the volatile anesthetic Enflurane on spontaneous discharge rate and GABAA-mediated inhibition of Purkinje cells in rat cerebellar slices. Neurophysiology 77, 2525-2538
2. Ayyildiz M., Yildirim M., Agar E., Baltaci A. K. (2006): The effect of leptin on penicillin-induced epileptiform activity in rats. Brain. Res. Bull. 68, 374-378 http://dx.doi.org/10.1016/j.brainresbull.2005.09.012
3. Banks W. A. (2006): Blood-brain barrier and energy balance. Obesity (Silver Spring) 14, S234-237 http://dx.doi.org/10.1038/oby.2006.315
4. Banks W. A., Farrell C. L. (2003): Impaired transport of leptin across the blood-brain barrier in obesity is acquired and reversible. Am. J. Physiol. Endocrinol. Metab. 285, E10-15
5. Berglund O., Frankel B. J., Hellman B. (1978.): Development of insulin secretory defect in the geneticaly diabetic (db/db) mouse. Acta Endocrinol. 87, 543-545
6. Berman S. M., Paz-Filho G., Wong M. L., Kohno M., Licinio J., Edythe D. (2013): Effects of leptin deficiency and replacement on cerebellar response to food-related cues. Cerebellum 12, 59-67 http://dx.doi.org/10.1007/s12311-012- 0360-z
7. Biggio G., Brodie B. B., Costa E., Guidotti A. (1977): Mechanisms by which diazepam, muscimol, and other drugs change the content of cGMP in cerebellar cortex. Proc. Natl. Acad. Sci. U.S.A. 74, 3592-3596 http://dx.doi.org/10.1073/pnas.74.8.3592
8. Bjørbæck C., Uotani S., da Silva B., Flier J. S. (1997): Divergent signaling capacities of the long and short isoforms of the leptin receptor. J. Biol. Chem. 272, 32686-32695 http://dx.doi.org/10.1074/jbc.272.51. 32686
9. Bjørbaek C., Kahn B. B. (2004): Leptin signaling in the central nervous system and the periphery. Recent Prog. Horm. Res. 59, 305-331 http://dx.doi.org/10.1210/rp.59.1.305
10. Bormann J. (2000): The "ABC" of GABA receptors. Trends Pharmacol. Sci. 21, 16-19 http://dx.doi.org/10.1016/S0165-6147(99)01413-3
11. Calapai G., Corica F., Corsonello A., Sautebin L., Di Rosa M., Campo G.M., Buemi M., Mauro V. N., Caputi A. P. (1999): Leptin increases serotonin turnover by inhibition of brain nitric oxide synthesis. J. Clin. Invest. 104, 975-982 http://dx.doi.org/10.1172/JCI5867
12. Campfield L. A., Smith F. J., Guisez Y., Devos R., Burn P. (1995): Recombinant mouse OB protein: evidence for peripheral signal linking adiposity and central neural networks. Science 269, 546-549 http://dx.doi.org/10.1126/ science.7624778
13. Coleman D. L. (1978): Obesity and diabetes: two mutant genes causing diabetes-obesity syndrome in mice. Diabetologia 14, 141-148 http://dx.doi.org/ 10.1007/BF00429772
14. Elmquist J. K., Bjørbæk C., Ahima R. S., Flier J. S., Saper C. B. (1998): Distributions of leptin receptor mRNA isoforms in the rat brain. J. Comp. Neurol. 395, 535-547 http://dx.doi.org/10.1002/(SICI)1096- 9861(19980615)395:4〈535::AID-CNE9〉3.0.CO;2-2
15. Elmquist J. K., Coppari R., Balthasar N., Ichinose M., Lowell B. B. (2005): Identifying hypothalamic pathways controlling food intake, body weight, and glucose homeostasis. J. Comp. Neurol. 493, 63-71 http://dx.doi.org/10.1002/ cne.20786
16. Elmquist J. K., Elias C. F., Saper C. B. (1999): From lesions to leptin: hypothalamic control of food intake and body weight. Neuron 22, 221-232 http://dx.doi.org/10.1016/S0896-6273(00)81084-3
17. Fisch K. (2011): The contribution of spike-frequency adaptation to the variability of spike responses in a sensory neuron. Dissertationan der Fakultät für Biologie der Ludwig-Maximilians- Universität München vorgelegt von München. Ed. Ludwig- Maximilians- Universität München. München
18. Friedman J. M., Halaas J. L. (1998): Leptin and the regulation of body weight in mammals. Nature 395, 763-770 http://dx.doi.org/10.1038/27376
19. Gahwiler B. H., Llano I. (1989): Sodium and potassium conductances in somatic membranes of rat Purkinje cells from organotypic cerebellar cultures. J. Physiol. 417, 105-122
20. Greengard P. (1978): Phosphorylated proteins as physiological effectors. Science 199, 146-152 http://dx.doi.org/10.1126/science.22932
21. Grieco T. M., Afshari F. S., Raman I. M. (2002): A role for phosphorylation in the maintenance of resurgent sodium current in cerebellar Purkinje neurons. J. Neurosc. 22, 3100-3107
22. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. (1981): Improved patch-clamp techniques for high-resolution current recording from cells and cell free patches. Pflüg. Arch. Eur. J. Phy. 391, 85-100 http://dx.doi.org/10.1007/BF00656997
23. Hausser M., Clark B. A. (1997): Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19, 665-678 http://dx.doi.org/10.1016/S0896-6273(00)80379-7
24. Häusser M., Raman I. M., Otis T. S., Smith S. L., Nelson A., du Lac S. (2004): Annual meeting mini-symposium the beat goes on: spontaneous firing in mammalian neuronal microcircuits. J. Neurosci. 24, 9215-9219 http://dx.doi.org/10.1523/JNEUROSCI.3375-04.2004
25. Hernandez-Fonseca J. P., Rincon J., Pedreanez A., Viera N., Arcaya J. L., Carrizo E., Mosquera J. (2009): Structural and ultrastructural analysis of cerebral cortex, cerebellum, and hypothalamus from diabetic rats. Exp. Diabetes Res. 2009, 329632 http://dx.doi.org/10.1155/2009/329632
26. Huo L., Gamber K., Greeley S., Silva J., Huntoon N., Leng X. H., Bjørbaek C. (2009): Leptin-dependent control of glucose balance and locomotor activity by POMC neurons. Cell Metab. 9, 537-457 http://dx.doi.org/10. 1016/j.cmet.2009.05.003
27. Irving A. J., Wallace L., Durakoglugil D., Harvey J. (2006): Leptin enhances NR2B-mediated NMDA responses via a MAPKdependent process in cerebellar granule cells. Neuroscience 138, 1137-1148 http://dx.doi.org/10.1016/j. neuroscience.2005.11.042
28. Ito M. (2001): Cerebellar long-term depression: Characterization, signal transduction, and functional roles. Physiol. Rev. 81, 1143-1195
29. Kano M. (1996): Long-lasting potentiation of GABAergic inhibitory synaptic transmission in cerebellar Purkinje cells: Its properties and possible mechanisms. Behav. Brain Sci. 19, 354-361 http://dx.doi.org/10.1017/ S0140525X00081450
30. Khaliq Z. M., Gouwens N. W., 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
31. Kullmann D. M. (1994): Amplitude fluctuations of dual component EPSCs in hippocampal pyramidal cells: implications for longterm potentiation. Neuron 12, 1111-1120 http://dx.doi.org/10.1016/0896-6273(94)90318-2
32. Llano I., Leresche N., Marty A. (1991): Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron 6, 565-574 http://dx.doi.org/10.1016/0896- 6273(91)90059-9
33. Llinas R., Sugimori M. (1980a): Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J. Physiol. 305, 171-195
34. Matson C. A., Reid D. F., Cannon T. A., Ritter R. C. (2000): Cholecystokinin and leptin act synergistically to reduce body weight. Am. J. Physiol-Reg. I. 278, R882-890
35. Mercer J. G., Moar K. M., Hoggard N. (1998): Localization of leptin receptor (Ob-R) messenger ribonucleic acid in the rodent hindbrain. Endocrinology 139, 29-34 http://dx.doi.org/10.1210/en.139.1.29
36. Morash B, Li S. A., Murphy P. R., Wilkinson M., Ur E. (1999): Leptin gene expression in the brain and pituitary gland. Endocrinology 140, 5995-5998 http://dx.doi.org/10.1210/en.140.12.5995
37. Morton G. J., Cummings D. E., Baskin D. G., Barsh G. S., Schwartz M. W. (2006): Central nervous system control of food intake and body weight. Nature 443, 289-295 http://dx.doi.org/10.1038/nature05026
38. Niswender K. D., Morton G. J., Stearns W.H., Rhodes C. J., Myers M. G. Jr., Schwartz M. W. (2001): Intracellular signalling. Key enzyme in leptin-induced anorexia. Nature 413, 794-795 http://dx.doi.org/10.1038/35101657
39. Oldfield C. S., Marty A., Stell B. M. (2010): Interneurons of the cerebellar cortex toggle Purkinje cells between up and down states. Proc. Natl. Acad. Sci. U S A. 107, 13153-13158 http://dx.doi.org/10.1073/pnas.1002082107
40. Palmer M. R., Tottmar O., Deitrich R. A. (1986): Electrophysiological effects of monoamine-derived aldehydes on single neurons in neocortex and cerebellum in rats. Alcohol. Clin. Exp. Res. 10, 682-685 http://dx.doi.org/10. 1111/j.1530-0277.1986.tb05168.x
41. Qian Z., Yakhnitsa V., Barmack N. H. (2011): Climbing fiber-evoked Purkinje cell discharge reduces expression of GABAa receptorassociated protein and decreases its interation with GABAa receptors. J. Neurochem. 117, 197-208 http://dx.doi.org/10.1111/j.1471-4159.2010.07119.x
42. Raman I. M., Bean B. P. (1999): Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J. Neurosci. 19, 1663-1674
43. Raman I. M., Bean B. P. (2001): Inactivation and recovery of sodium currents in cerebellar Purkinje neurons: evidence for two mechanisms. Biophys. J. 80, 729 -737 http://dx.doi.org/10.1016/S0006-3495(01)76052-3
44. Raman I. M., Bean B. P. (1997): Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J. Neurosci. 17, 4517-4526
45. Richerson G. B. (2004): Looking for GABA in all the wrong places: the relevance of extrasynaptic GABAA receptors to epilepsy. Epilepsy Curr. 4, 239-242 http://dx.doi.org/10.1111/j.1535-7597.2004.46008.x
46. Robertson S. A., Leinninger G. M., Myers M. G. Jr. (2008): Molecular and neural mediators of leptin action. Physiol. Behav. 94, 637-642 http://dx.doi.org/10.1016/j.physbeh.2008.04.005
47. Schwartz M. W., Peskind E., Raskind M., Boyko E. J., Porte D Jr. (1996): Cerebrospinal fluid leptin levels: Relationship to plasma levels and to adiposity in humans. Nat. Med. 2, 589-593 http://dx.doi.org/10.1038/nm0596-589
48. Shafrir E. (1992): Animal models of non insulin dependent diabetes. Diabetes Metab. Rev. 8, 179-208 http://dx.doi.org/10.1002/dmr.5610080302
49. Shalman A. (2010): Muscarinic M1, M3, nicotinic, GABAA and GABAB receptor subtypes gene expression in insulin induced hypoglycemic rat brain regions: functional regulation through phospholipase C and creb protein. PhD Thesis. Cochin University of Science and Technology. Cochin, India
50. Shanley L. J., Irving A. J., Harvey J. (2001): Leptin enhances NMDA receptor function and modulates hippocampal synaptic plasticity. J. Neurosci. 21, RC186
51. Shanley L. J., Irving A. J., Rae M. G., Ashford M. L., Harvey J. (2002a): Leptin inhibits rat hippocampal neurons via activation of large conductance calcium-activated K+ channels. Nat. Neurosci. 5, 299-300 http://dx.doi.org/10. 1038/nn824
52. Shanley L. J., O'Malley D., Irving A. J., Ashford M. L., Harvey J. (2002b): Leptin inhibits epileptiform-like activity in rat hippocampal neurones via PI 3-kinase-driven activation of BK channels. J. Physiol. 545, 933-944 http://dx.doi.org/10.1113/jphysiol.2002.029488
53. Shin S. L., Hoebeek F. E., Schonewille M., De Zeeuw C. I., Aertsen A., De Schutter E. (2007): Regular patterns in cerebellar purkinje cell simple spike trains. PLoS One 2, e485 http://dx.doi.org/10.1371/journal.pone.0000485
54. Smith S. L., Otis T. S. (2003): Persistent changes in spontaneous firing of Purkinje neurons triggered by the nitric oxide signaling cascade. J. Neurosci. 23, 367-372
55. Spanswick D., Smith M. A., Groppi V.E., Logan S. D., Ashford M. L. (1997): Leptin inhibits hypothalamic neurons by activation of ATP-sensitive potassium channels. Nature 390, 521-525 http://dx.doi.org/10.1038/37379
56. Srinivasan K., Ramarao P. (2007): Animal models in type 2 diabetes research: An overview. Indian J. Med. Res-B. 125, 451-472
57. Takahashi K. A., Cone R. D. (2005): Fasting induces a large, leptindependent increase in the intrinsic action potential frequency of orexigenic arcuate nucleus neuropeptide Y/Agouti-related protein neurons. Endocrinology 146, 1043-1047 http://dx.doi.org/10.1210/en.2004-1397
58. Tartaglia L. A., Dembski M., Weng X., Deng N., Culpepper J., Devos R., Richards G. J., Campfield L. A., Clark F. T., Deeds J. et al. (1995): Identification and expression cloning of a leptin receptor. Cell 83, 1263-1271 http://dx.doi.org/10.1016/0092-8674(95)90151-5
59. Udagawa J., Hashimoto R., Hioki K., Otani H. (2006): The role of leptin inthe development of the cortical neuron in mouse embryos. Brain Res. 1120, 74-82 http://dx.doi.org/10.1016/j.brainres.2006.08.116
60. Udagawa J., Hatta T., Naora H., Otani H. (2000): Expression of the long form of leptin receptor (Ob-Rb) mRNA in the brain of mouse embryos and newborn mice. Brain Res. 868, 251-258 http://dx.doi.org/10.1016/S0006-8993(00)02334-9
61. Ur E., Wilkinson D. A., Morash B. A., Wilkinson M. (2002): Leptin immunoreactivity is localized to neurons in rat brain. Neuroendocrinology 75, 264-272 http://dx.doi.org/10.1159/000054718
62. Waxman S. G., Sabin T. D. (1981): Diabetic truncal polyneuropathy. Arch. Neurol. 38, 46-47 http://dx.doi.org/10.1001/archneur.1981.00510010072013
63. Womack M., Khodakhah K. (2002): Active contribution of dendrites to the tonic and trimodal patterns of activity in cerebellar Purkinje neurons. J. Neurosci. 22, 10603-10612
64. Yadav V. K., Oury F., Tanaka K., Thomas T., Wang Y., Cremers S., Hen R., Krust A., Chambon P., Karsenty G. (2011): Leptin-dependent serotonin control of appetite: temporal specificity, transcriptional regulation, and therapeutic implications. J. Exp. Med. 208, 41-52 http://dx.doi.org/10.1084/jem.20101940