Intrinsic and synaptic dynamics interact to generate emergent patterns of rhythmic bursting in thalamocortical neurons

Journal of Neuroscience

Volumn 26, Issue 16, 2006, Pages 4247-4255

  Sohal, Vikaas S ^a   Pangratz Fuehrer, Susanne ^a   Rudolph, Uwe ^b   Huguenard, John R ^a  

^a STANFORD UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Absence epilepsy; Dynamic clamp; GABAA receptor; Inhibition; Oscillation; Synchrony

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR; PYRIDINE DERIVATIVE; ZOLPIDEM;

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL SYNCHRONIZATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; DEPOLARIZATION; HYPERPOLARIZATION; INHIBITORY POSTSYNAPTIC POTENTIAL; MOUSE; NERVE CELL; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; SLEEP; SYNAPTIC POTENTIAL; THALAMUS; ACTION POTENTIAL; ANIMAL; COMPARATIVE STUDY; DRUG EFFECT; DRUG POTENTIATION; IN VITRO STUDY; MOUSE MUTANT; NERVE CELL INHIBITION; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT; SYNAPSE;

ACTION POTENTIALS; ANIMALS; CEREBRAL CORTEX; MICE; MICE, MUTANT STRAINS; NEURAL INHIBITION; NEURONS; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SYNAPSES; THALAMUS;

EID: 33646439729     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3812-05.2006     Document Type: Article

References (44)

1. Bacci A, Rudolph U, Huguenard JR, Prince DA (2003) Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses. J Neurosci 23:9664-9674.
2. Benson JA, Low K, Keist R, Mohler H, Rudolph U (1998) Pharmacology of recombinant gamma-aminobutyric acidA receptors rendered diazepam-insensitive by point-mutated alpha-subunits. FEBS Lett 431:400-404.
3. Bevan MD, Magill PJ, Hallworth NE, Bolam JP, Wilson CJ (2002) Regulation of the timing and pattern of action potential generation in rat subthalamic neurons in vitro by GABA-A IPSPs. J Neurophysiol 87:1348-1362.
4. Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G (1995) Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47-60.
5. Buhl EH, Tamas G, Fisahn A (1998) Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J Physiol (Lond) 513:117-126.
6. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-78.
7. Coulter DA, Huguenard JR, Prince DA (1989) Specific petit mal anticonvulsants reduce calcium currents in thalamic neurons. Neurosci Lett 98:74-78.
8. Cox CL, Huguenard JR, Prince DA (1997) Nucleus reticularis neurons mediate diverse inhibitory effects in thalamus. Proc Natl Acad Sci USA 94:8854-8859.
9. Crestani F, Martin JR, Mohler H, Rudolph U (2000) Mechanism of action of the hypnotic zolpidem in vivo. Br J Pharmacol 131:1251-1254.
10. 2+ potentials in cells of the cat and rat lateral geniculate nucleus. J Physiol (Lond) 413:543-561.
11. Fisahn A, Pike FG, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394:186-189.
12. Huguenard JR, Prince DA (1994) Intrathalamic rhythmicity studied in vitro: nominal T-current modulation causes robust antioscillatory effects. J Neurosci 14:5485-5502.
13. Jahnsen H, Llinas R (1984) Voltage-dependent burst-to-tonic switching of thalamic cell activity: an in vitro study. Arch Ital Biol 122:73-82.
14. Kapetanovic IM, Yonekawa WD, Kupferberg HJ (1993) Time-related loss of glutamine from hippocampal slices and concomitant changes in neurotransmitter amino acids. J Neurochem 61:865-872.
15. 2+ channels. Neuron 31:35-45.
16. Le Masson G, Renaud-Le Masson S, Debay D, Bal T (2002) Feedback inhibition controls spike transfer in hybrid thalamic circuits. Nature 417:854-858.
17. Liu XB, Honda CN, Jones EG (1995) Distribution of four types of synapse on physiologically identified relay neurons in the ventral posterior thalamic nucleus of the cat. J Comp Neurol 352:69-91.
18. Low K, Crestani F, Keist R, Benke D, Brunig I, Benson JA, Fritschy JM, Rulicke T, Bluethmann H, Mohler H, Rudolph U (2000) Molecular and neuronal substrate for the selective attenuation of anxiety. Science 290:131-134.
19. Ludwig A, Budde T, Stieber J, Moosmang S, Wahl C, Holthoff K, Langebartels A, Wotjak C, Munsch T, Zong X, Feil S, Feil R, Lancel M, Chien KR, Konnerth A, Pape HC, Biel M, Hofmann F (2003) Absence epilepsy and sinus dysrhythmia in mice lacking the pacemaker channel HCN2. EMBO J 22:216-224.
20. McCormick DA, Bal T (1997) Sleep and arousal: thalamocortical mechanisms. Annu Rev Neurosci 20:185-215.
21. A receptors in central synapses. J Neurosci 19:578-588.
22. Pinault D (2003) Cellular interactions in the rat somatosensory thalamocortical system during normal and epileptic 5-9 Hz oscillations. J Physiol (Lond) 552:881-905.
23. Pinault D, Leresche N, Charpier S, Deniau JM, Marescaux C, Vergnes M, Crunelli V (1998) Intracellular recordings in thalamic neurones during spontaneous spike and wave discharges in rats with absence epilepsy. J Physiol (Lond) 509:449-456.
24. Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G (2000) GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101:815-850.
25. Plenz D, Kital ST (1999) A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 400:677-682.
26. Rudolph U, Mohler H (2004) Analysis of GABAA receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu Rev Pharmacol Toxicol 44:475-498.
27. Salek-Haddadi A, Lemieux L, Merschhemke M, Friston KJ, Duncan JS, Fish DR (2003) Functional magnetic resonance imaging of human absence seizures. Ann Neurol 53:663-667.
28. Sanchez-Vives MV, McCormick DA (1997) Functional properties of peri-geniculate inhibition of dorsal lateral geniculate nucleus thalamocortical neurons in vitro. J Neurosci 17:8880-8893.
29. Sherman SM (2001) Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci 24:122-126.
30. Snead OC, Depaulis A, Vergnes M, Marescaux C (1999) Absence epilepsy: advances in experimental animal models. Adv Neurol 79:253-278.
31. Sohal VS, Huguenard JR (2003) Inhibitory interconnections control burst pattern and emergent network synchrony in reticular thalamus. J Neurosci 23:8978-8988.
32. Sohal VS, Huntsman MM, Huguenard JR (2000) Reciprocal inhibitory connections regulate the spatiotemporal properties of intrathalamic oscillations. J Neurosci 20:1735-1745.
33. A receptor subtype-specific modulation of the synchrony and duration of thalamic oscillations. J Neurosci 23:3649-3657.
34. Soltesz I, Deschenes M (1993) Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J Neurophysiol 70:97-116.
35. Steriade M, Deschenes M, Domich L, Mulle C (1985) Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. J Neurophysiol 54:1473-1497.
36. Talley EM, Cribbs LL, Lee JH, Daud A, Perez-Reyes E, Bayliss DA (1999) Differential distribution of three members of a gene family encoding low voltage-activated (T-type) calcium channels. J Neurosci 19:1895-1911.
37. Ulrich D, Huguenard JR (1996) Gamma-aminobutyric acid type B receptor-dependent burst-firing in thalamic neurons: a dynamic clamp study. Proc Natl Acad Sci USA 93:13245-13249.
38. Ulrich D, Huguenard JR (1997) Nucleus-specific chloride homeostasis in rat thalamus. J Neurosci 17:2348-2354.
39. von Krosigk M, Bal T, McCormick DA (1993) Cellular mechanisms of a synchronized oscillation in the thalamus. Science 261:361-364.
40. Wieland HA, Luddens H, Seeburg PH (1992) A single histidine in GABAA receptors is essential for benzodiazepine agonist binding. J Biol Chem 267:1426-1429.
41. Williams D (1953) A study of thalamic and cortical rhythms in petit mal. Brain 76:50-69.
42. A receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 12:1040-1062.
43. Wolfart J, Debay D, Le Masson G, Destexhe A, Bal T (2005) Synaptic background activity controls spike transfer from thalamus to cortex. Nat Neurosci 8:1760-1767.
44. Ylinen A, Soltesz I, Bragin A, Penttonen M, Sik A, Buzsaki G (1995) Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus 5:78-90.