Parvalbumin-deficiency facilitates repetitive IPSCs and gamma oscillations in the hippocampus

Journal of Neurophysiology

Volumn 89, Issue 3, 2003, Pages 1414-1422

  Vreugdenhil, Martin ^a   Jefferys, John G R ^a   Celio, Marco R ^b   Schwaller, Beat ^b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

PARVALBUMIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MOUSE; NERVE CELL EXCITABILITY; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL;

ANIMALS; CHIMERA; EXCITATORY AMINO ACID AGONISTS; FEMALE; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; KAINIC ACID; MALE; MICE; MICE, INBRED C57BL; NEURAL INHIBITION; NEURONS; PARVALBUMINS; PERIODICITY; PREGNANCY; PRESYNAPTIC TERMINALS;

EID: 0037342021     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00576.2002     Document Type: Article

References (56)

1. Adler EM, Augustine GJ, Duffy SN, and Charlton MP. Intracellular calcium chelators attenuate neurotransmitter release at the Squid giant synapse. J Neurosci 11: 1496-1507, 1991.
2. Aika Y, Ren JQ, Kosaka K, and Kosaka T. Quantitative analysis of GABA-like-immunoreactive and PV-containing neurons in the CA1 region of the rat hippocampus using a stereological method, the dissector. Exp Brain Res 99: 267-276, 1994.
3. Ali AB, Bannister AP, and Thomson AM. IPSPs elicited in CA1 pyramidal cells by putative basket cells in slices of adult rat hippocampus. Eur J Neurosci 11: 1741-1753, 1999.
4. Buhl EH, Cobb SR, Halasy K, and Somogyi P. Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. Eur J Neurosci 7: 1989-2004, 1995.
5. Buhl EH, Tamas G, and Fisahn A. Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J Physiol 513: 117-126, 1998.
6. Caillard O, Moreno H, Schwaller B, Llano I, Celio MR, and Marty A. Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. Proc Natl Acad Sci USA 97: 13372-13377, 2000.
7. 28k and parvalbumin in the rat nervous system. Neuroscience 35: 375-475, 1990.
8. Celio MR and Heizmann CW. Calcium-binding protein parvalbumin is associated with fast contracting muscle fibres. Nature 297: 504-506, 1982.
9. 28k and parvalbumin in rat sensory neurons. J Physiol 472: 341-357, 1993.
10. Cossart R, Tyzio R, Dinoncourt C, Esclapez M, Hirsch JC, Ben-Ari Y, and Bernard C. Presynaptic kainate receptors that enhance the release of GABA on CA1 hippocampal interneurons. Neuron 29: 497-508, 2001.
11. Cossart R, Esclapez M, Hirsch JC, Bernard C, and Ben-Ari Y. GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat Neurosci 1: 470-478, 1998.
12. B autoreceptors in rat hippocampus. J Physiol 472: 245-265, 1993.
13. Dickson CT, Biella G, and de Curtis M. Evidence for spatial modules mediated by temporal synchronization of carbachol-induced gamma rhythm in medial entorhinal cortex. J Neurosci 20: 6846-6854, 2000.
14. Drake CT, Mulligan KA, Wimpey TL, Hendrickson A, and Chavkin C. Characterization of Vicia villosa agglutinin-labeled GABAergic interneurons in the hippocampal formation and in acutely dissociated hippocampus. Brain Res 554: 176-185, 1991.
15. Engel AK and Singer W. Temporal binding and the neural correlates of sensory awareness. Trends Cogn Sci 5: 16-25, 2001.
16. Fisahn A, Pike FG, Buhl EH, and Paulsen O. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394: 186-189, 1998.
17. Freund TF and Buzsáki G. Interneurons in the hippocampus. Hippocampus 6: 347-470, 1996.
18. Freund TF, Ylinen A, Miettinen R, Pitkänen A, Lahtinen H, Baimbridge KG, and Riekkinen PJ. Pattern of neuronal death in the rat hippocampus after status epilepticus. Relationship to calcium binding protein content and ischemic vulnerability. Brain Res Bull 28: 27-38, 1992.
19. Fukuda T, Aika Y, Heizmann CW, and Kosaka T. Dense GABAergic input on somata of parvalbumin-immunoreactive GABAergic neurons in the hippocampus of the mouse. Neurosci Res 26: 181-194, 1996.
20. Fukuda T and Kosaka T. Gap junctions linking the dendritic network of GABAergic interneurons in the hippocampus. J Neurosci 20: 1519-1528, 2000.
21. Gulyás AI, Miles R, Hájos N, and Freund TF. Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur J Neurosci 5: 1729-1751, 1993.
22. Hack SP, Köhling R, and Jefferys JGR. Modulation of cholinergically induced gamma oscillations by chronic estrogen treatment. Eur J Neurosci 12, Suppl 11: 481, 2000.
23. Hajos N, Papp EC, Acsady L, Levey AI, and Freund TF. Distinct interneuron types express m2 muscarinic receptor immunoreactivity on their dendrites or axon terminals in the hippocampus. Neuroscience 82: 355-376, 1998.
24. Hajos N, Katona I, Naiem SS, Mackie K, Ledent C, Mody I, and Freund TF. Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12: 3239-3249, 2000.
25. Hartley DM, Neve RL, Bryan J, Ullrey DB, Bak SY, Lang P, and Geller AI. Expression of the calcium-binding protein, parvalbumin, in cultured cortical neurons, using a HSV-1 vector system enhances NMDA neurotoxicity. Brain Res Mol Brain Res 40: 285-296, 1996.
26. Haunso A, Celio MR, Bartsch U, Letiembre M, Celio MR, and Menoud PA. Morphology of perineuronal nets in tenascin-R and parvalbumin single and double knockout mice. Brain Res 864: 142-145, 2000.
27. Hefft S, Kraushaar U, Geiger JR, and Jonas P. Presynaptic short-term depression is maintained during regulation of transmitter release at a GABAergic synapse in rat hippocampus. J Physiol 539: 201-208, 2002.
28. 2+ buffers on evoked release and on facilitation in the crayfish neuromuscular junction. Neurosci Lett 125: 215-218, 1991.
29. Joho RH, Ho CS, and Marks GA. Increased γ- and decreased δ-oscillations in a mouse deficient for a potassium channel expressed in fast-spiking interneurons. J Neurophysiol 82: 1855-1864, 1999.
30. A receptor channel function in the nervous system. Prog Neurobiol 42: 489-537, 1994.
31. 2+ and short-term synaptic plasticity. Nature 371: 603-606, 1994.
32. Kamphuis W, Huisman E, Wadman WJ, Heizman CW, and Lopes da Silva FH. Kindling induced changes in parvalbumin immunoreactivity in rat hippocampus and its relation to long-term decrease in GABA immunoreactivity. Brain Res 479: 23-24, 1989.
33. A receptors in the hippocampus. J Neurosci 22: 2513-2521, 2002.
34. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419: 119-130, 1987.
35. Kosaka T, Kosaka K, Nakayama T, and Heizmann CW. Axons and axon terminals of cerebellar purkinje cells and basket cells have higher levels of parvalbumin immunoreactivity than somata and dendrites: quantitative analysis by immunogold labeling. Exp Brain Res 93: 483-491, 1993.
36. Lambert NA, Harrison NL, and Teyler TJ. Evidence for μ opiate receptors on inhibitory terminals in area CA1 of rat hippocampus. Neurosci Lett 124: 101-104, 1991.
37. Lambert NA and Wilson WA. Temporally distinct mechanisms of use-dependent depression at inhibitory synapses in the rat hippocampus in vitro. J Neurophysiol 72: 121-130, 1994.
38. 2+ transients of neuronal dendrites. J Physiol 525: 419-443, 2000.
39. Lüth H-J, Fischer J, and Celio MR. Soybean lectin binding neurons in the visual cortex of the rat contain parvalbumin and are covered by glial nets. J Neurocytol 21: 211-221, 1992.
40. Maccaferri G, Roberts JDB, Szucs P, Cottingham CA, and Somogyi P. Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurons in rat hippocampus in vitro. J Physiol 524: 91-116, 2000.
41. Medvedev A, Mackenzie L, Hiscock JJ, and Willoughby, JO. Kainic acid induces distinct types of epileptiform discharge with differential involvement of hippocampus and neocortex. Brain Res Bull 52: 89-98, 2000.
42. Miltner WHR, Braun C, Arnold M, Witte H, and Taub E. Coherence of gamma-band EEG activity as a basis for associative learning. Nature 397: 434-436, 1999.
43. Muller MM, Gruber T, and Keil A. Modulation of induced gamma band activity in the human EEG by attention and visual processing. Int J Psychophysiol 38: 283-299, 2000.
44. Nusser Z, Sieghart W, Benke D, Fritschy J-M, and Somogyi P. Differential synaptic localization of two major γ-aminobutyric acid type A receptor α subunits on hippocampal pyramidal cells. Proc Natl Acad Sci USA 93: 11939-11944, 1996.
45. A-mediated IPSCs in rat hippocampus. J Physiol 484: 425-435, 1995.
46. Penttonen M, Kamondi A, Acsady L, and Buzsáki G. Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur J Neurosci 10: 718-728, 1998.
47. Raymackers JM, Gailly P, Colson-Van Schoor M, Pette D, Schwaller B, Hunziker W, Celio MR, and Gillis JM. Tetanus relaxation of fast skeletal muscles of the mouse made parvalbumin-deficient by gene inactivation. J Physiol 527: 355-364, 2000.
48. Ribak CE, Nitsch R, and Seress L. Proportion of parvalbumin-positive basket cells in the GABAergic innervation of pyramidal and granule cells of the rat hippocampal formation. J Comp Neurol 300: 449-461, 1990.
49. Schwaller B, Dick J, Dhoot G, Carroll S, Vrbova G, Nicotera P, Pette D, Wyss A, Bluethmann H, Hunziker W, and Celio MR. Prolonged contraction-relaxation cycle of fast-twitch muscles in parvalbumin knockout mice. Am J Physiol Cell Physiol 276: C395-C403, 1999.
50. Sloviter RS, Sollas AL, Barbaro NM, and Laxer KD. Calcium-binding protein (calbindin-D28K) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus. J Comp Neurol 308: 381-396, 1991.
51. Stenkamp KJ. Matias Palva JM, Marylka Uusisaari M, Sebastian Schuchmann S, Schmitz D, Heinemann U, and Kai Kaila K. Enhanced temporal stability of cholinergic hippocampal gamma oscillations following respiratory alkalosis in vitro. J Neurophysiol 85: 2063-2069, 2001.
52. Tamas G, Buhl EH, Lörincz A, and Somogyi P. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat Neurosci 3: 366-371, 2000.
53. Tandon P, Villa A, Tetko IV, Silveira DC, Celio MR, and Schwaller B. Impairment of the inhibitory system in parvalbumin-deficient mice increases susceptibility towards epileptic seizures. Soc Neurosci Abstr 25: 843, 1999.
54. Thomson AM. Activity-dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro. J Physiol 502: 131-147, 1997.
55. Traub RD, Bibbig A, Fisahn A, LeBeau FEN, Whittington MA, and Buhl EH. A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro. Eur J Neurosci 12: 4093-4106, 2000.
56. Whittington MA, Traub RD, and Jefferys JGR. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373: 612-615, 1995.