Intrinsic excitability is altered by hypothyroidism in the developing hippocampal CA1 pyramidal cells

Neuroscience

Volumn 207, Issue , 2012, Pages 37-51

  Sanchez Alonso J L ^a   Sanchez Aguilera A ^a   Vicente Torres, M A ^a   Colino, A ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

A type potassium current; Action potential; D type potassium current; Kv1.2; Kv4; Neuronal discharge

Indexed keywords

POTASSIUM CHANNEL KV1.2; SHAL POTASSIUM CHANNEL; SHAL POTASSIUM CHANNEL KV4.2; SHAL POTASSIUM CHANNEL KV4.3; THYROID HORMONE; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EVOKED RESPONSE; HIPPOCAMPUS; HORMONE RESPONSE; HYPOTHYROIDISM; MEMBRANE RESISTANCE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE EXCITABILITY; NONHUMAN; POSTNATAL DEVELOPMENT; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; REPOLARIZATION;

ACTION POTENTIALS; ANIMALS; BRAIN DISEASES, METABOLIC; CA1 REGION, HIPPOCAMPAL; FEMALE; HYPOTHYROIDISM; MALE; ORGAN CULTURE TECHNIQUES; PREGNANCY; PYRAMIDAL CELLS; RATS; RATS, WISTAR; THYROID HORMONES;

EID: 84858449404     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.01.030     Document Type: Article

References (50)

1. Akaike M., Kato N., Ohno H., Kobayashi T. Hyperactivity and spatial maze learning impairment of adult rats with temporary neonatal hypothyroidism. Neurotoxicol Teratol 1991, 13:317-322.
2. Aldrich R.W. Inactivation of voltage-gated delayed potassium current in molluscan neurons: a kinetic model. Biophys J 1981, 36:519-532.
3. Aldrich R.W., Getting P.A., Thompson S.H. Mechanism of frequency-dependent broadening of molluscan neurone soma spikes. J Physiol 1979, 291:531-544.
4. An W.F., Bowlby M.R., Betty M., Cao J., Ling H.P., Mendoza G., Hinson J.W., Mattsson K.I., Strassle B.W., Trimmer J.S., Rhodes K.J. Modulation of A-type potassium channels by a family of calcium sensors. Nature 2000, 403:553-556.
5. Blanton M.G., Lo Turco J.J., Kriegstein A.R. Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. J Neurosci Methods 1989, 30:203-210.
6. Cai X., Liang C.W., Muralidharan S., Kao J.P., Tang C.M., Thompson S.M. Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 2004, 44:351-364.
7. Carter B.C., Bean B.P. Sodium entry during action potentials of mammalian neurons: incomplete inactivation and reduced metabolic efficiency in fast-spiking neurons. Neuron 2009, 64:898-909.
8. Coleman P.A., Miller R.F. Measurement of passive membrane parameters with whole-cell recording from neurons in the intact amphibian retina. J Neurophysiol 1989, 61:218-230.
9. Connor J.A., Stevens C.F. Prediction of repetitive firing behaviour from voltage clamp data on an isolated neurone soma. J Physiol 1971, 213:31-53.
10. DeLong G.R. Observations on the neurology of endemic cretinism. Iodine and the Brain 1989, 231-238. Plenum, New York. G.R. DeLong, J. Robbins, P.G. Condliffe (Eds.).
11. Giné E., Morales-Garcia J.A., Perez-Castillo A., Santos A. Developmental hypothyroidism increases the expression of kainate receptors in the hippocampus and the sensitivity to kainic acid-induced seizures in the rat. Endocrinology 2010, 151:3267-3276.
12. Goldey E.S., Kehn L.S., Rehnberg G.L., Crofton K.M. Effects of developmental hypothyroidism on auditory and motor function in the rat. Toxicol Appl Pharmacol 1995, 135:67-76.
13. Gu N., Vervaeke K., Storm J.F. BK potassium channels facilitate high-frequency firing and cause early spike frequency adaptation in rat CA1 hippocampal pyramidal cells. J Physiol 2007, 580:859-882.
14. Gutman G.A., Chandy K.G., Grissmer S., Lazdunski M., McKinnon D., Pardo L.A., Robertson G.A., Rudy B., Sanguinetti M.C., Stühmer W., Wang X. International union of pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol Rev 2005, 57:473-508.
15. Hashimoto K., Curty F.H., Borges P.P., Lee C.E., Abel E.D., Elmquist J.K., Cohen R.N., Wondisford F.E. An unliganded thyroid hormone receptor causes severe neurological dysfunction. Proc Natl Acad Sci U S A 2001, 98:3998-4003.
16. Hodgkin A.L., Huxley A.F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 1952, 117:500-544.
17. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 1997, 387:869-875.
18. Hoffmann G., Dietzel I.D. Thyroid hormone regulates excitability in central neurons from postnatal rats. Neuroscience 2004, 125:369-379.
19. Huguenard J.R., Hamill O.P., Prince D.A. Developmental changes in Na+ conductances in rat neocortical neurons: appearance of a slowly inactivating component. J Neurophysiol 1988, 59:778-795.
20. Jerng H.H., Pfaffinger P.J., Covarrubias M. Molecular physiology and modulation of somatodendritic A-type potassium channels. Mol Cell Neurosci 2004, 27:343-369.
21. Johnston D., Hoffman D.A., Magee J.C., Poolos N.P., Watanabe S., Colbert C.M., Migliore M. Dendritic potassium channels in hippocampal pyramidal neurons. J Physiol 2000, 525:75-81.
22. Kay A.R., Wong R.K.S. Isolation of neurons suitable for patch-clamping from adult mammalian central nervous systems. J Neurosci Methods 1986, 16:227-238.
23. Kim J., Wei D.S., Hoffman D.A. Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J Physiol 2005, 569:41-57.
24. Klee R., Ficker E., Heinemann U. Comparison of voltage-dependent potassium currents in rat pyramidal neurons acutely isolated from hippocampal regions CA1 and CA3. J Neurophysiol 1995, 74. 1982-1955.
25. Lorenzo P.I., Ménard C., Miller F.D., Bernal J. Thyroid hormone-dependent regulation of Tα1 α-tubulin during brain development. Mol Cell Neurosci 2002, 19:333-343.
26. Losonczy A., Magee J.C. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 2006, 50:291-307.
27. Ma M., Koester J. The role of K+ currents in frequency-dependent spike broadening in Aplysia R20 neurons: a dynamic clamp analysis. J Neurosci 1996, 16:4089-4101.
28. Maffie J., Rudy B. Weighing the evidence for a ternary protein complex mediating A-type K+ currents in neurons. J Physiol 2008, 586:5609-5623.
29. Martina M., Schultz J.H., Ehmke H., Monyer H., Jonas P. Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. J Neurosci 1998, 18:8111-8125.
30. Mitterdorfer J., Bean B.P. Potassium currents during the action potential of hippocampal CA3 neurons. J Neurosci 2002, 22:10106-10115.
31. Moody W.J. Control of spontaneous activity during development. J Neurobiol 1998, 37:97-109.
32. Moyer J.R., Thompson L.T., Disterhoft J.F. Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J Neurosci 1996, 16:5536-5546.
33. Numann R.E., Wadman W.J., Wong R.K. Outward currents of single hippocampal cells obtained from the adult guinea-pig. J Physiol 1987, 393:331-353.
34. Oh-Nishi A., Saji M., Furudate S.I., Suzuki N. Dopamine D2-like receptor function is converted from excitatory to inhibitory by thyroxine in the developmental hippocampus. J Neuroendocrinol 2005, 17:836-845.
35. Oppenheimer J.H., Schwartz H.L. Molecular basis of thyroid hormone-dependent brain development. Endocr Rev 1997, 18:462-475.
36. + channels. Physiol Rev 2010, 90:755-796.
37. Rami A., Patel J., Rabié A. Thyroid hormone and development of the rat hippocampus: morphological alterations in granule and pyramidal cells. Neuroscience 1986, 19:1217-1226.
38. Rami A., Rabié A., Patel A.J. Thyroid hormone and development of the rat hippocampus: cell acquisition in the dentate gyrus. Neuroscience 1986, 19:1207-1216.
39. Rhodes K.J., Carroll K.I., Sung M.A., Doliveira L.C., Monaghan M.M., Burke S.L., Strassle B.W., Buchwalder L., Menegola M., Cao J., An W.F., Trimmer J.S. KChIPs and Kv4α subunits as integral components of A-type potassium channels in mammalian brain. J Neurosci 2004, 24:7903-7915.
40. Sah P. Ca(2+)-activated K+ currents in neurones: types, physiological roles and modulation. Trends Neurosci 1996, 19:150-154.
41. Sánchez-Alonso J.L., Muñoz-Cuevas J., Vicente-Torres M.A., Colino A. Role of low-voltage-activated calcium current on the firing pattern alterations induced by hypothyroidism in the rat hippocampus. Neuroscience 2010, 171:993-1005.
42. Schwartz H.L. Effect of thyroid hormone in growth and development. Molecular basis of thyroid hormone action 1983, 413-444. Academic Press, New York. J.H. Oppenhemer, H.H. Samuels (Eds.).
43. Serodio P., Kentros C., Rudy B. Identification of molecular components of A-type channels activating at subthreshold potentials. J Neurophysiol 1994, 72:1516-1529.
44. + channels operating at subthreshold potentials with unique expression in heart and brain. J Neurophysiol 1996, 75:2174-2179.
45. Shao L.R., Halvorsrud R., Borg-Graham L., Storm J.F. The role of BK-type Ca2+-dependent K+ channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. J Physiol 1999, 521:135-146.
46. Spigelman I., Zhang L., Carlen P.L. Patch-clamp study of postnatal development of CA1 neurons in rat hippocampal slices: membrane excitability and K+ currents. J Neurophysiol 1992, 68:55-69.
47. Storm J.F. Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J Physiol 1987, 385:733-759.
48. Storm J.F. Temporal integration by a slowly inactivating K+ current in hippocampal neurons. Nature 1988, 336:379-381.
49. Thompson L.T., Moyer J.R., Disterhoft J.F. Transient changes in excitability of rabbit CA3 neurons with a time course appropriate to support memory consolidation. J Neurophysiol 1996, 76:1836-1849.
50. Vara H., Martínez B., Santos A., Colino A. Thyroid hormone regulates neurotransmitter release in neonatal rat hippocampus. Neuroscience 2002, 110:19-22.