A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex

Neuron

Volumn 38, Issue 5, 2003, Pages 805-817

  Blatow, Maria ^a   Rozov, Andrei ^a,b   Katona, Istvan ^a,d   Hormuzdi, Sheriar G ^a   Meyer, Axel H ^a   Whittington, Miles A ^c   Caputi, Antonio ^a   Monyer, Hannah ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c UNIVERSITY OF LEEDS   (United Kingdom)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; CARBACHOL; PARVALBUMIN;

ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL STRUCTURE; CONTROLLED STUDY; DRUG EFFECT; FACILITATION; GABAERGIC SYSTEM; GAP JUNCTION; INTERNEURON; MOUSE; NEOCORTEX; NERVE CELL NETWORK; NEUROCHEMISTRY; NEUROPHYSIOLOGY; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYNAPSE; THETA RHYTHM;

EID: 0038182516     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(03)00300-3     Document Type: Article

References (44)

1. Alcantara S., de Lecea L., Del Rio J.A., Ferrer I., Soriano E. Transient colocalization of parvalbumin and calbindin D28k in the postnatal cerebral cortex. evidence for a phenotypic shift in developing nonpyramidal neurons Eur. J. Neurosci. 8:1996;1329-1339.
2. Beierlein M., Gibson J.R., Connors B.W. A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat. Neurosci. 3:2000;904-910.
3. Buhl E.H., Tamas G., Fisahn A. Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J. Physiol. 513:1998;117-126.
4. Buzsaki G., Chrobak J.J. Temporal structure in spatially organized neuronal ensembles. a role for interneuronal networks Curr. Opin. Neurobiol. 5:1995;504-510.
5. Caputi, A., Meyer, A., Fuchs, E., and Monyer, H. (2000). Generation of transgenic mice expressing a green fluorescent protein in calretinin-positive neurons. Paper presented at: Society for Neuroscience Meeting (New Orleans, LA).
6. Cauli B., Porter J.T., Tsuzuki K., Lambolez B., Rossier J., Quenet B., Audinat E. Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc. Natl. Acad. Sci. USA. 97:2000;6144-6149.
7. Cobb S.R., Buhl E.H., Halasy K., Paulsen O., Somogyi P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature. 378:1995;75-78.
8. Condorelli D.F., Belluardo N., Trovato-Salinaro A., Mudo G. Expression of Cx36 in mammalian neurons. Brain Res. Brain Res. Rev. 32:2000;72-85.
9. Deans M.R., Gibson J.R., Sellitto C., Connors B.W., Paul D.L. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron. 31:2001;477-485.
10. Du J., Zhang L., Weiser M., Rudy B., McBain C.J. Developmental expression and functional characterization of the potassium-channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus. J. Neurosci. 16:1996;506-518.
11. Fisahn A., Pike F.G., Buhl E.H., Paulsen O. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature. 394:1998;186-189.
12. Freund T.F., Buzsaki G. Interneurons of the hippocampus. Hippocampus. 6:1996;347-470.
13. Galarreta M., Hestrin S. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature. 402:1999;72-75.
14. Geiger J.R., Lubke J., Roth A., Frotscher M., Jonas P. Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron. 18:1997;1009-1023.
15. Gibson J.R., Beierlein M., Connors B.W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature. 402:1999;75-79.
16. Gupta A., Wang Y., Markram H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science. 287:2000;273-278.
17. Hormuzdi S.G., Pais I., LeBeau F.E., Towers S.K., Rozov A., Buhl E.H., Whittington M.A., Monyer H. Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron. 31:2001;487-495.
18. Kawaguchi Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J. Neurosci. 15:1995;2638-2655.
19. Kawaguchi Y., Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex. 7:1997;476-486.
20. Lubke J., Egger V., Sakmann B., Feldmeyer D. Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex. J. Neurosci. 20:2000;5300-5311.
21. Markram H., Lubke J., Frotscher M., Roth A., Sakmann B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J. Physiol. 500:1997;409-440.
22. 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. 18:1998;8111-8125.
23. McBain C.J., Fisahn A. Interneurons unbound. Nat. Rev. Neurosci. 2:2001;11-23.
24. McCormick D.A. Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog. Neurobiol. 39:1992;337-388.
25. Meyer A.H., Katona I., Blatow M., Rozov A., Monyer H. In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J. Neurosci. 22:2002;7055-7064.
26. Penttonen M., Kamondi A., Acsady L., Buzsaki G. Gamma frequency oscillation in the hippocampus of the rat. intracellular analysis in vivo Eur. J. Neurosci. 10:1998;718-728.
27. Reyes A., Lujan R., Rozov A., Burnashev N., Somogyi P., Sakmann B. Target-cell-specific facilitation and depression in neocortical circuits. Nat. Neurosci. 1:1998;279-285.
28. Rozov A., Jerecic J., Sakmann B., Burnashev N. AMPA receptor channels with long-lasting desensitization in bipolar interneurons contribute to synaptic depression in a novel feedback circuit in layer 2/3 of rat neocortex. J. Neurosci. 21:2001;8062-8071.
29. Sik A., Penttonen M., Buzsaki G. Interneurons in the hippocampal dentate gyrus. an in vivo intracellular study Eur. J. Neurosci. 9:1997;573-588.
30. Singer W., Gray C.M. Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18:1995;555-586.
31. Skinner F.K., Zhang L., Velazquez J.L., Carlen P.L. Bursting in inhibitory interneuronal networks. a role for gap- junctional coupling J. Neurophysiol. 81:1999;1274-1283.
32. Somogyi P., Tamas G., Lujan R., Buhl E.H. Salient features of synaptic organisation in the cerebral cortex. Brain Res. Brain Res. Rev. 26:1998;113-135.
33. Stuart G.J., Dodt H.U., Sakmann B. Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflugers Arch. 423:1993;511-518.
34. Szabadics J., Lorincz A., Tamas G. Beta and gamma frequency synchronization by dendritic gabaergic synapses and gap junctions in a network of cortical interneurons. J. Neurosci. 21:2001;5824-5831.
35. Tamas G., Buhl E.H., Lorincz A., Somogyi P. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat. Neurosci. 3:2000;366-371.
36. Traub R.D., Bibbig A., Fisahn A., LeBeau F.E., Whittington M.A., Buhl E.H. A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro. Eur. J. Neurosci. 12:2000;4093-4106.
37. Traub R.D., Jefferys J.G.R., Whittington M.A. Fast Oscillation in Cortical Circuits. 1999;MIT Press, Cambridge, MA.
38. Traub R.D., Kopell N., Bibbig A., Buhl E.H., LeBeau F.E., Whittington M.A. Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distributed networks. J. Neurosci. 21:2001;9478-9486.
39. Tsodyks M., Uziel A., Markram H. Synchrony generation in recurrent networks with frequency-dependent synapses. J. Neurosci. 20:2000;RC50.
40. van Brederode J.F., Helliesen M.K., Hendrickson A.E. Distribution of the calcium-binding proteins parvalbumin and calbindin-D28k in the sensorimotor cortex of the rat. Neuroscience. 44:1991;157-171.
41. Venance L., Rozov A., Blatow M., Burnashev N., Feldmeyer D., Monyer H. Connexin expression in electrically coupled postnatal rat brain neurons. Proc. Natl. Acad. Sci. USA. 97:2000;10260-10265.
42. Whittington M.A., Traub R.D., Jefferys J.G. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature. 373:1995;612-615.
43. Ylinen A., Bragin A., Nadasdy Z., Jando G., Szabo I., Sik A., Buzsaki G. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus. network and intracellular mechanisms J. Neurosci. 15:1995;30-46. a.
44. Ylinen A., Soltesz I., Bragin A., Penttonen M., Sik A., Buzsaki G. Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus. 5:1995;78-90. b.