Thalamocortical neurons display suppressed burst-firing due to an enhanced Ih current in a genetic model of absence epilepsy

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 6, 2015, Pages 1367-1382

  Cain, Stuart M ^a   Tyson, John R ^a   Jones, Karen L ^a   Snutch, Terrance P ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Absence; Burst firing; Epilepsy; HCN; Ih; Seizure

Indexed keywords

CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL T TYPE; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL; MESSENGER RNA;

ABSENCE; ACTION POTENTIAL; ANIMAL; BRAIN CORTEX; CYTOLOGY; DRUG EFFECTS; FEMALE; GENETICS; INTERNEURON; MALE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; THALAMUS;

ACTION POTENTIALS; ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, T-TYPE; CEREBRAL CORTEX; EPILEPSY, ABSENCE; FEMALE; HYPERPOLARIZATION-ACTIVATED CYCLIC NUCLEOTIDE-GATED CHANNELS; INTERNEURONS; MALE; RATS; RNA, MESSENGER; THALAMUS;

EID: 84939872125     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1549-4     Document Type: Article

References (51)

1. Atherton JF, Kitano K, Baufreton J et al (2010) Selective participation of somatodendritic HCN channels in inhibitory but not excitatory synaptic integration in neurons of the subthalamic nucleus. J Neurosci 30:16025–16040
2. Beenhakker MP, Huguenard JR (2009) Neurons that fire together also conspire together: is normal sleep circuitry hijacked to generate epilepsy? Neuron 62:612–632
3. Benarroch EE (2013) HCN channels: function and clinical implications. Neurology 80:304–310
4. Blumenfeld H (2005) Cellular and network mechanisms of spike-wave seizures. Epilepsia 46:21–33
5. Broicher T, Kanyshkova T, Meuth P et al (2008) Correlation of T-channel coding gene expression, IT, and the low threshold Ca2+ spike in the thalamus of a rat model of absence epilepsy. Mol Cell Neurosci 39:384–399
6. Cain SM, Snutch TP (2010) Contributions of T-type calcium channel isoforms to neuronal firing. Channels 4:44–51
7. Cain SM, Snutch TP (2012) Voltage-gated calcium channels in epilepsy. In: Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta A (eds) Jasper’s basic mechanisms of the epilepsies, 4th edn. Oxford University Press, Bethesda, pp 66–84
8. Cain SM, Snutch TP (2012) T-type calcium channels in burst-firing, network synchrony, and epilepsy. Biochim Biophys Acta 1828:1572–1578
9. Charpier S, Leresche N, Deniau JM et al (1999) On the putative contribution of GABA(B) receptors to the electrical events occurring during spontaneous spike and wave discharges. Neuropharmacology 38:1699–1706
10. Cheong E, Shin H-S (2014) T-type Ca(2+) channels in absence epilepsy. Pflugers Arch 466:719–734
11. Chung WK, Shin M, Jaramillo TC et al (2009) Absence epilepsy in apathetic, a spontaneous mutant mouse lacking the h channel subunit, HCN2. Neurobiol Dis 33:499–508
12. Cicirata F, Angaut P, Cioni M et al (1986) Functional organization of thalamic projections to the motor cortex. An anatomical and electrophysiological study in the rat. Neuroscience 19:81–99
13. Crunelli V, Toth TI, Cope DW et al (2005) The “window” T-type calcium current in brain dynamics of different behavioural states. J Physiol 562:121–129
14. Danober L, Deransart C, Depaulis A et al (1998) Pathophysiological mechanisms of genetic absence epilepsy in the rat. Prog Neurobiol 55:27–57
15. Desbois C, Villanueva L (2001) The organization of lateral ventromedial thalamic connections in the rat: a link for the distribution of nociceptive signals to widespread cortical regions. Neuroscience 102:885–898
16. Dreyfus FM, Tscherter A, Errington AC et al (2010) Selective T-type calcium channel block in thalamic neurons reveals channel redundancy and physiological impact of I(T)window. J Neurosci 30:99–109
17. Ehling P, Cerina M, Meuth P et al (2013) Ca(2+)-dependent large conductance K(+) currents in thalamocortical relay neurons of different rat strains. Pflugers Arch 465:469–480
18. Ernst WL, Zhang Y, Yoo JW et al (2009) Genetic enhancement of thalamocortical network activity by elevating alpha 1 g-mediated low-voltage-activated calcium current induces pure absence epilepsy. J Neurosci 29:1615–1625
19. Gorji A, Mittag C, Shahabi P et al (2011) Seizure-related activity of intralaminar thalamic neurons in a genetic model of absence epilepsy. Neurobiol Dis 43:266–274
20. Holter J, Carter D, Leresche N et al (2005) A TASK3 channel (KCNK9) mutation in a genetic model of absence epilepsy. J Mol Neurosci 25:37–51
21. Inoue M, Duysens J, Vossen JM, Coenen AM (1993) Thalamic multiple-unit activity underlying spike-wave discharges in anesthetized rats. Brain Res 612:35–40
22. Joksovic PM, Bayliss DA, Todorovic SM (2005) Different kinetic properties of two T-type Ca2+ currents of rat reticular thalamic neurones and their modulation by enflurane. J Physiol 566:125–142
23. Kanyshkova T, Meuth P, Bista P et al (2012) Differential regulation of HCN channel isoform expression in thalamic neurons of epileptic and non-epileptic rat strains. Neurobiol Dis 45:450–461
24. Kawana E, Kusama T (1964) Projection of the sensory motor cortex to the thalamus, the dorsal column nucleus, the trigeminal nucleus and the spinal cord in the cat. Psychiatry Clin Neurosci 18:337–338
25. Killackey HP, Sherman SM (2003) Corticothalamic projections from the rat primary somatosensory cortex. J Neurosci 23:7381–7384
26. Kim D, Song I, Keum S et al (2001) Lack of the burst firing of thalamocortical relay neurons and resistance to absence seizures in mice lacking alpha(1G) T-type Ca2+ channels. Neuron 31:35–45
27. Kuisle M, Wanaverbecq N, Brewster AL et al (2006) Functional stabilization of weakened thalamic pacemaker channel regulation in rat absence epilepsy. J Physiol 575:83–100
28. Ludwig A, Budde T, Stieber J et al (2003) Absence epilepsy and sinus dysrhythmia in mice lacking the pacemaker channel HCN2. EMBO J 22:216–224
29. McKay BE, McRory JE, Molineux ML et al (2006) Ca(V)3 T-type calcium channel isoforms differentially distribute to somatic and dendritic compartments in rat central neurons. Eur J Neurosci 24:2581–2594
30. Monconduit L, Villanueva L (2005) The lateral ventromedial thalamic nucleus spreads nociceptive signals from the whole body surface to layer I of the frontal cortex. Eur J Neurosci 21:3395–3402
31. Paz JT, Chavez M, Saillet S et al (2007) Activity of ventral medial thalamic neurons during absence seizures and modulation of cortical paroxysms by the nigrothalamic pathway. J Neurosci 27:929–941
32. Pinault D, Vergnes M, Marescaux C (2001) Medium-voltage 5-9-Hz oscillations give rise to spike-and-wave discharges in a genetic model of absence epilepsy: in vivo dual extracellular recording of thalamic relay and reticular neurons. Neuroscience 105:181–201
33. Pinault D (2003) Cellular interactions in the rat somatosensory thalamocortical system during normal and epileptic 5–9 Hz oscillations. J Physiol 552:881–905
34. Pinault D, Leresche N, Charpier S et al (1998) Intracellular recordings in thalamic neurones during spontaneous spike and wave discharges in rats with absence epilepsy. J Physiol 509(Pt 2):449–456
35. Pinault D, Slezia A, Acsady L (2006) Corticothalamic 5–9 Hz oscillations are more pro-epileptogenic than sleep spindles in rats. J Physiol 574:209–227
36. Polack PO, Guillemain I, Hu E et al (2007) Deep layer somatosensory cortical neurons initiate spike-and-wave discharges in a genetic model of absence seizures. J Neurosci 27:6590–6599
37. Polack PO, Mahon S, Chavez M, Charpier S (2009) Inactivation of the somatosensory cortex prevents paroxysmal oscillations in cortical and related thalamic neurons in a genetic model of absence epilepsy. Cereb Cortex 19:2078–2091
38. Powell KL, Cain SM, Ng C et al (2009) A Cav3.2 T-type calcium channel point mutation has splice-variant-specific effects on function and segregates with seizure expression in a polygenic rat model of absence epilepsy. J Neurosci 29:371–380
39. Powell KL, Cain SM, Snutch TP, O’Brien TJ (2013) Low threshold T-type calcium channels as targets for novel epilepsy treatments. Br J Clin Pharmacol. doi:10.1111/bcp.12205
40. Sánchez-Alonso JL, Halliwell JV, Colino A (2008) ZD 7288 inhibits T-type calcium current in rat hippocampal pyramidal cells. Neurosci Lett 439:275–280
41. Seidenbecher T, Pape HC (2001) Contribution of intralaminar thalamic nuclei to spike-and-wave-discharges during spontaneous seizures in a genetic rat model of absence epilepsy. Eur J Neurosci 13:1537–1546
42. Slaght SJ, Leresche N, Deniau JM et al (2002) Activity of thalamic reticular neurons during spontaneous genetically determined spike and wave discharges. J Neurosci 22:2323–2334
43. Song I, Kim D, Choi S et al (2004) Role of the alpha1G T-type calcium channel in spontaneous absence seizures in mutant mice. J Neurosci 24:5249–5257
44. Talley EM, Cribbs LL, Lee JH et al (1999) Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J Neurosci 19:1895–1911
45. Talley EM, Solorzano G, Depaulis A et al (2000) Low-voltage-activated calcium channel subunit expression in a genetic model of absence epilepsy in the rat. Brain Res Mol Brain Res 75:159–165
46. Tringham E, Powell KL, Cain SM et al (2012) T-type calcium channel blockers that attenuate thalamic burst firing and suppress absence seizures. Sci Transl Med 4:121-19
47. Tsakiridou E, Bertollini L, de Curtis M et al (1995) Selective increase in T-type calcium conductance of reticular thalamic neurons in a rat model of absence epilepsy. J Neurosci 15:3110–3117
48. Wahl-Schott C, Biel M (2009) HCN channels: structure, cellular regulation and physiological function. Cell Mol Life Sci 66:470–494
49. Williams SR, Toth TI, Turner JP et al (1997) The “window” component of the low threshold Ca2+ current produces input signal amplification and bistability in cat and rat thalamocortical neurones. J Physiol 505:689–705
50. Ying S-W, Abbas SY, Harrison NL, Goldstein PA (2006) Propofol block of Ih contributes to the suppression of neuronal excitability and rhythmic burst firing in thalamocortical neurons. Eur J Neurosci 23:465–480
51. Zheng TW, O’Brien TJ, Morris MJ et al (2012) Rhythmic neuronal activity in S2 somatosensory and insular cortices contribute to the initiation of absence-related spike-and-wave discharges. Epilepsia 53:1948–1958