The Influence of Cold Temperature on Cellular Excitability of Hippocampal Networks

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  de la Peña, Elvira ^a   Mälkiä, Annika ^a   Vara, Hugo ^a   Caires, Rebeca ^a   Ballesta, Juan J ^a   Belmonte, Carlos ^a   Viana, Felix ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROFORM; POTASSIUM CHANNEL; PROTEIN TRAAK; PROTEIN TREK; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CHANNEL GATING; COLD; CONTROLLED STUDY; COOLING; EMBRYO; HIPPOCAMPUS; MOUSE; NERVE CELL EXCITABILITY; NEUROMODULATION; NONHUMAN; SYNAPTIC TRANSMISSION; TEMPERATURE SENSITIVITY;

ANIMALS; CELLS, CULTURED; COLD TEMPERATURE; EVOKED POTENTIALS; GLUTAMIC ACID; HIPPOCAMPUS; MEMBRANE POTENTIALS; MICE; NERVE NET; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; SYNAPSES; TETRODOTOXIN; TIME FACTORS;

EID: 84871729191     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052475     Document Type: Article

References (96)

1. Abrams R, Hammel HT, (1964) Hypothalamic temperature in unanesthetized albino rats during feeding and sleeping. Am J Physiol 206: 641-646.
2. Andersen P, Moser EI, (1995) Brain temperature and hippocampal function. Hippocampus 5: 491-498.
3. Kiyatkin EA, (2007) Brain temperature fluctuations during physiological and pathological conditions. Eur J Appl Physiol 101: 3-17.
4. Tancredi V, D'Arcangelo G, Zona C, Siniscalchi A, Avoli M, (1992) Induction of epileptiform activity by temperature elevation in hippocampal slices from young rats: an in vitro model for febrile seizures? Epilepsia 33: 228-234.
5. Wu J, Javedan SP, Ellsworth K, Smith K, Fisher RS, (2001) Gamma oscillation underlies hyperthermia-induced epileptiform-like spikes in immature rat hippocampal slices. BMC Neurosci 2: 18.
6. Dube CM, Brewster AL, Richichi C, Zha Q, Baram TZ, (2007) Fever, febrile seizures and epilepsy. Trends Neurosci 30: 490-496.
7. Obal F Jr, Rubicsek G, Alfoldi P, Sary G, Obal F, (1985) Changes in the brain and core temperatures in relation to the various arousal states in rats in the light and dark periods of the day. Pflugers Arch 404: 73-79.
8. Dragoi G, Carpi D, Recce M, Csicsvari J, Buzsaki G, (1999) Interactions between hippocampus and medial septum during sharp waves and theta oscillation in the behaving rat. J Neurosci 19: 6191-6199.
9. Hodking AL, Katz B, (1949) The effect of temperature on the electrical activity of the giant axon of the squid. J Physiol 109: 240-249.
10. Weight FF, Erulkar SD, (1976) Synaptic transmission and effects of temperature at the squid giant synapse. Nature 261: 720-722.
11. Thompson SM, Masukawa LM, Prince DA, (1985) Temperature dependence of intrinsic membrane properties and synaptic potentials in hippocampal CA1 neurons in vitro. J Neurosci 5: 817-824.
12. Volgushev M, Vidyasagar TR, Chistiakova M, Eysel UT, (2000) Synaptic transmission in the neocortex during reversible cooling. Neuroscience 98: 9-22.
13. Volgushev M, Vidyasagar TR, Chistiakova M, Yousef T, Eysel UT, (2000) Membrane properties and spike generation in rat visual cortical cells during reversible cooling. J Physiol 522 Pt 1: 59-76.
14. Asztely F, Erdemli G, Kullmann DM, (1997) Extrasynaptic glutamate spillover in the hippocampus: dependence on temperature and the role of active glutamate uptake. Neuron 18: 281-293.
15. Postlethwaite M, Hennig MH, Steinert JR, Graham BP, Forsythe ID, (2007) Acceleration of AMPA receptor kinetics underlies temperature-dependent changes in synaptic strength at the rat calyx of Held. J Physiol 579: 69-84.
16. Moser E, Mathiesen I, Andersen P, (1993) Association between brain temperature and dentate field potentials in exploring and swimming rats. Science 259: 1324-1326.
17. Cain DP, Hargreaves EL, Boon F, (1994) Brain temperature- and behavior-related changes in the dentate gyrus field potential during sleep, cold water immersion, radiant heating, and urethane anesthesia. Brain Res 658: 135-144.
18. Aihara H, Okada Y, Tamaki N, (2001) The effects of cooling and rewarming on the neuronal activity of pyramidal neurons in guinea pig hippocampal slices. Brain Res 893: 36-45.
19. Reig R, Mattia M, Compte A, Belmonte C, Sanchez-Vives MV, (2010) Temperature modulation of slow and fast cortical rhythms. J Neurophysiol 103: 1253-1261.
20. Caterina MJ, (2007) Transient receptor potential ion channels as participants in thermosensation and thermoregulation. Am J Physiol Regul Integr Comp Physiol 292: R64-R76.
21. Bayliss DA, Barrett PQ, (2008) Emerging roles for two-pore-domain potassium channels and their potential therapeutic impact. Trends Pharmacol Sci 29: 566-575.
22. Dhaka A, Viswanath V, Patapoutian A, (2006) Trp ion channels and temperature sensation. Annu Rev Neurosci 29: 135-161.
23. Noel J, Zimmermann K, Busserolles J, Deval E, Alloui A, et al. (2009) The mechano-activated K+ channels TRAAK and TREK-1 control both warm and cold perception. EMBO J 28: 1308-1318.
24. Lesage F, Lazdunski M, (2000) Molecular and functional properties of two-pore-domain potassium channels. Am J Physiol Renal Physiol 279: F793-F801.
25. Honore E, (2007) The neuronal background K2P channels: focus on TREK1. Nat Rev Neurosci 8: 251-261.
26. Enyedi P, Czirjak G, (2010) Molecular background of leak K+ currents: two-pore domain potassium channels. Physiol Rev 90: 559-605.
27. Bagriantsev SN, Peyronnet R, Clark KA, Honore E, Minor DL Jr, (2011) Multiple modalities converge on a common gate to control K2P channel function. EMBO J 30: 3594-3606.
28. de la Peña E, Mälkiä A, Cabedo H, Belmonte C, Viana F, (2005) The contribution of TRPM8 channels to cold sensing in mammalian neurones. J Physiol 567: 415-426.
29. Khirug S, Huttu K, Ludwig A, Smirnov S, Voipio J, et al. (2005) Distinct properties of functional KCC2 expression in immature mouse hippocampal neurons in culture and in acute slices. Eur J Neurosci 21: 899-904.
30. Clayton GH, Owens GC, Wolff JS, Smith RL, (1998) Ontogeny of cation-Cl- cotransporter expression in rat neocortex. Brain Res Dev Brain Res 109: 281-292.
31. Maier N, Morris G, Johenning FW, Schmitz D, (2009) An approach for reliably investigating hippocampal sharp wave-ripples in vitro. PLoS One 4: e6925.
32. Buzsaki G, (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398: 242-252.
33. Karnup S, Stelzer A, (2001) Seizure-like activity in the disinhibited CA1 minislice of adult guinea-pigs. J Physiol 532: 713-730.
34. Heurteaux C, Guy N, Laigle C, Blondeau N, Duprat F, et al. (2004) TREK-1, a K+ channel involved in neuroprotection and general anesthesia. EMBO J 23: 2684-2695.
35. McBain CJ, Eaton JV, Brown T, Dingledine R, (1992) CNQX increases spontaneous inhibitory input to CA3 pyramidal neurones in neonatal rat hippocampal slices. Brain Res 592: 255-260.
36. Thompson SM, Capogna M, Scanziani M, (1993) Presynaptic inhibition in the hippocampus. Trends Neurosci 16: 222-227.
37. Luscher C, Jan LY, Stoffel M, Malenka RC, Nicoll RA, (1997) G protein-coupled inwardly rectifying K+ channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19: 687-695.
38. Cao YQ, Tsien RW, (2005) Effects of familial hemiplegic migraine type 1 mutations on neuronal P/Q-type Ca2+ channel activity and inhibitory synaptic transmission. Proc Natl Acad Sci U S A 102: 2590-2595.
39. Jabaudon D, Shimamoto K, Yasuda-Kamatani Y, Scanziani M, Gahwiler BH, et al. (1999) Inhibition of uptake unmasks rapid extracellular turnover of glutamate of nonvesicular origin. Proc Natl Acad Sci U S A 96: 8733-8738.
40. Mezey E, Toth ZE, Cortright DN, Arzubi MK, Krause JE, et al. (2000) Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1like immunoreactivity, in the central nervous system of the rat and human. Proc Natl Acad Sci U S A 97: 3655-3660.
41. Toth A, Boczan J, Kedei N, Lizanecz E, Bagi Z, et al. (2005) Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res Mol Brain Res 135: 162-168.
42. Shibasaki K, Suzuki M, Mizuno A, Tominaga M, (2007) Effects of body temperature on neural activity in the hippocampus: regulation of resting membrane potentials by transient receptor potential vanilloid 4. J Neurosci 27: 1566-1575.
43. Gibson HE, Edwards JG, Page RS, Van Hook MJ, Kauer JA, (2008) TRPV1 channels mediate long-term depression at synapses on hippocampal interneurons. Neuron 57: 746-759.
44. Vriens J, Appendino G, Nilius B, (2009) Pharmacology of vanilloid transient receptor potential cation channels. Mol Pharmacol 75: 1262-1279.
45. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, et al. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824.
46. McKemy DD, Neuhausser WM, Julius D, (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416: 52-58.
47. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, et al. (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427: 260-265.
48. Zhang XB, Jiang P, Gong N, Hu XL, Fei D, et al. (2008) A-type GABA receptor as a central target of TRPM8 agonist menthol. PLoS One 3: e3386.
49. Valenzano KJ, Grant ER, Wu G, Hachicha M, Schmid L, Tafesse L, et al. (2003) N-(4-tertiarybutylphenyl)-4-(3-chloropyridin-2-yl)tetrahydropyrazine-1(2H)-carbox-amide (BCTC), a novel, orally effective vanilloid receptor 1 antagonist with analgesic properties: I. in vitro characterization and pharmacokinetic properties. J Pharmacol Exp Ther 306: 377-386.
50. Madrid R, Donovan-Rodriguez T, Meseguer V, Acosta MC, Belmonte C, et al. (2006) Contribution of TRPM8 channels to cold transduction in primary sensory neurons and peripheral nerve terminals. J Neurosci 26: 12512-12525.
51. Mälkiä A, Madrid R, Meseguer V, de la Peña E, Valero M, et al. (2007) Bidirectional shifts of TRPM8 channel gating by temperature and chemical agents modulate the cold sensitivity of mammalian thermoreceptors. J Physiol 581: 155-174.
52. McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, et al. (2007) TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci U S A 104: 13525-13530.
53. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D, (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398: 436-441.
54. Guler AD, Lee H, Iida T, Shimizu I, Tominaga M, et al. (2002) Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22: 6408-6414.
55. Xu H, Ramsey IS, Kotecha SA, Moran MM, Chong JA, et al. (2002) TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418: 181-186.
56. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, et al. (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112: 819-829.
57. Takigawa T, Alzheimer C, (2003) Interplay between activation of GIRK current and deactivation of Ih modifies temporal integration of excitatory input in CA1 pyramidal cells. J Neurophysiol 89: 2238-2244.
58. Hu H, Vervaeke K, Storm JF, (2007) M-channels (Kv7/KCNQ channels) that regulate synaptic integration, excitability, and spike pattern of CA1 pyramidal cells are located in the perisomatic region. J Neurosci 27: 1853-1867.
59. Maingret F, Lauritzen I, Patel AJ, Heurteaux C, Reyes R, et al. (2000) TREK-1 is a heat-activated background K(+) channel. EMBO J 19: 2483-2491.
60. Kang D, Choe C, Kim D, (2005) Thermosensitivity of the two-pore domain K+ channels TREK-2 and TRAAK. J Physiol 564: 103-116.
61. Fink M, Duprat F, Lesage F, Reyes R, Romey G, et al. (1996) Cloning, functional expression and brain localization of a novel unconventional outward rectifier K+ channel. EMBO J 15: 6854-6862.
62. Fink M, Lesage F, Duprat F, Heurteaux C, Reyes R, et al. (1998) A neuronal two P domain K+ channel stimulated by arachidonic acid and polyunsaturated fatty acids. EMBO J 17: 3297-3308.
63. Talley EM, Solorzano G, Lei Q, Kim D, Bayliss DA, (2001) Cns distribution of members of the two-pore-domain (KCNK) potassium channel family. J Neurosci 21: 7491-7505.
64. Lesage F, Terrenoire C, Romey G, Lazdunski M, (2000) Human TREK2, a 2P domain mechano-sensitive K+ channel with multiple regulations by polyunsaturated fatty acids, lysophospholipids, and Gs, Gi, and Gq protein-coupled receptors. J Biol Chem 275: 28398-28405.
65. Aller MI, Wisden W, (2008) Changes in expression of some two-pore domain potassium channel genes (KCNK) in selected brain regions of developing mice. Neuroscience 151: 1154-1172.
66. Rath A, Glibowicka M, Nadeau VG, Chen G, Deber CM, (2009) Detergent binding explains anomalous SDS-PAGE migration of membrane proteins. Proc Natl Acad Sci U S A 106: 1760-1765.
67. Patel AJ, Honore E, Maingret F, Lesage F, Fink M, et al. (1998) A mammalian two pore domain mechano-gated S-like K+ channel. EMBO J 17: 4283-4290.
68. Bang H, Kim Y, Kim D, (2000) TREK-2, a new member of the mechanosensitive tandem-pore K+ channel family. J Biol Chem 275: 17412-17419.
69. Danthi S, Enyeart JA, Enyeart JJ, (2003) Modulation of native TREK-1 and Kv1.4 K+ channels by polyunsaturated fatty acids and lysophospholipids. J Membr Biol 195: 147-164.
70. Duprat F, Lesage F, Patel AJ, Fink M, Romey G, et al. (2000) The neuroprotective agent riluzole activates the two P domain K(+) channels TREK-1 and TRAAK. Mol Pharmacol 57: 906-912.
71. Cadaveira-Mosquera A, Ribeiro SJ, Reboreda A, Perez M, Lamas JA, (2011) Activation of TREK currents by the neuroprotective agent riluzole in mouse sympathetic neurons. J Neurosci 31: 1375-1385.
72. Mathie A, Veale EL, (2007) Therapeutic potential of neuronal two-pore domain potassium-channel modulators. Curr Opin Investig Drugs 8: 555-562.
73. Patel AJ, Honore E, Lesage F, Fink M, Romey G, et al. (1999) Inhalational anesthetics activate two-pore-domain background K+ channels. Nat Neurosci 2: 422-426.
74. Czirjak G, Enyedi P, (2002) TASK-3 dominates the background potassium conductance in rat adrenal glomerulosa cells. Mol Endocrinol 16: 621-629.
75. Czirjak G, Enyedi P, (2006) Targeting of calcineurin to an NFAT-like docking site is required for the calcium-dependent activation of the background K+ channel, TRESK. J Biol Chem 281: 14677-14682.
76. Liu H, Enyeart JA, Enyeart JJ, (2007) Potent inhibition of native TREK-1 K+ channels by selected dihydropyridine Ca2+ channel antagonists. J Pharmacol Exp Ther 323: 39-48.
77. Lee TS, Kaku T, Takebayashi S, Uchino T, Miyamoto S, et al. (2006) Actions of mibefradil, efonidipine and nifedipine block of recombinant T- and L-type Ca channels with distinct inhibitory mechanisms. Pharmacology 78: 11-20.
78. Shigetomi E, Tong X, Kwan KY, Corey DP, Khakh BS, (2012) TRPA1 channels regulate astrocyte resting calcium and inhibitory synapse efficacy through GAT-3. Nat Neurosci 15: 70-80.
79. Lotshaw DP, (2007) Biophysical, pharmacological, and functional characteristics of cloned and native mammalian two-pore domain K+ channels. Cell Biochem Biophys 47: 209-256.
80. Hervieu GJ, Cluderay JE, Gray CW, Green PJ, Ranson JL, et al. (2001) Distribution and expression of TREK-1, a two-pore-domain potassium channel, in the adult rat CNS. Neuroscience 103: 899-919.
81. de la Prida LM, Huberfeld G, Cohen I, Miles R, (2006) Threshold behavior in the initiation of hippocampal population bursts. Neuron 49: 131-142.
82. Soriano J, Rodriguez MM, Tlusty T, Moses E, (2008) Development of input connections in neural cultures. Proc Natl Acad Sci U S A 105: 13758-13763.
83. Miles R, Wong RK, (1983) Single neurones can initiate synchronized population discharge in the hippocampus. Nature 306: 371-373.
84. Ben Ari Y, Cherubini E, Corradetti R, Gaiarsa JL, (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416: 303-325.
85. Garaschuk O, Hanse E, Konnerth A, (1998) Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus. J Physiol 507 (Pt 1): 219-236.
86. Leinekugel X, (2003) Developmental patterns and plasticities: the hippocampal model. J Physiol Paris 97: 27-37.
87. Ben Ari Y, (2001) Developing networks play a similar melody. Trends Neurosci 24: 353-360.
88. Leinekugel X, Khazipov R, Cannon R, Hirase H, Ben Ari Y, et al. (2002) Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296: 2049-2052.
89. Maier N, Nimmrich V, Draguhn A, (2003) Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices. J Physiol 550: 873-887.
90. Buzsaki G, Leung LW, Vanderwolf CH, (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287: 139-171.
91. Morris M, Lack L, Dawson D, (1990) Sleep-onset insomniacs have delayed temperature rhythms. Sleep 13: 1-14.
92. Heurteaux C, Lucas G, Guy N, El Yacoubi M, Thummler S, et al. (2006) Deletion of the background potassium channel TREK-1 results in a depression-resistant phenotype. Nat Neurosci 9: 1134-1141.
93. Kennard LE, Chumbley JR, Ranatunga KM, Armstrong SJ, Veale EL, et al. (2005) Inhibition of the human two-pore domain potassium channel, TREK-1, by fluoxetine and its metabolite norfluoxetine. Br J Pharmacol 144: 821-829.
94. Gao B, Duncan WC Jr, Wehr TA, (1992) Fluoxetine decreases brain temperature and REM sleep in Syrian hamsters. Psychopharmacology (Berl) 106: 321-329.
95. Duncan WC Jr, Johnson KA, Wehr TA, (1995) Antidepressant drug-induced hypothalamic cooling in Syrian hamsters. Neuropsychopharmacology 12: 17-37.
96. Salerian AJ, Saleri NG, Salerian JA, (2008) Brain temperature may influence mood: a hypothesis. Med Hypotheses 70: 497-500.