Neurobiology of hippocampal interneurons: A workshop review
1996; Wiley; Volume: 6; Issue: 3 Linguagem: Inglês
10.1002/(sici)1098-1063(1996)6
ISSN1098-1063
AutoresPaul S. Buckmaster, Iván Soltész,
Tópico(s)Memory and Neural Mechanisms
ResumoHippocampusVolume 6, Issue 3 p. 330-339 Review Article Neurobiology of hippocampal interneurons: A workshop review Paul S. Buckmaster, Paul S. Buckmaster Department of Anatomy and Neurobiology, Colorado State University, Fort Collins, ColoradoSearch for more papers by this authorIvan Soltesz, Corresponding Author Ivan Soltesz Department of Anatomy and Neurobiology, University of California, College of Medicine, Irvine, CaliforniaDept. of Anatomy and Neurobiology, Univ. of California, College of Medicine, Irvine, CA 92717Search for more papers by this author Paul S. Buckmaster, Paul S. Buckmaster Department of Anatomy and Neurobiology, Colorado State University, Fort Collins, ColoradoSearch for more papers by this authorIvan Soltesz, Corresponding Author Ivan Soltesz Department of Anatomy and Neurobiology, University of California, College of Medicine, Irvine, CaliforniaDept. of Anatomy and Neurobiology, Univ. of California, College of Medicine, Irvine, CA 92717Search for more papers by this author First published: 1996 https://doi.org/10.1002/(SICI)1098-1063(1996)6:3 3.0.CO;2-QCitations: 18AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL References Gray CM, König P, Engel AK, Singer W, (1989) Oscillatory responses in cat visula cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338: 334– 337. Kaila K, Voipio J, (1987) Poststynaptic fall in intracellular pH induced by GABA-activated bicarbonate conductance. Nature 330: 163– 165. Kawa K, (1994) Distribution and functional properties of 5-HT3 receptors in the rat hippocampal dentate gyrus: a patch-chlamp study. J Neurophysiol 71: 1935– 1947. Marr D, (1971) Simple memory: a theory for archicortex. Proc Soc Lond [Biol] 262: 23– 81. Marty A, Liano I, (1995) Modulation of inhibitory synapses in teh mammalian brain. Curr Opin Neurobiol 5: 335– 341. McCormick DA, Connors BW, Lighhall JW, Prince DA, (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54: 782– 806. Rakic P, (1976) Local circuit neurons, p 161. Cambridge: MIT Press. Ramón y Cajal S, (1899) Comparative study of the sensory areas of the human cortex. In: Clark University 1889-1899 decennial celebration, pp 311– 382, Worcester, MA Sandler R, Smith AD, (1991) Coexistence of GABA and glutamate fin mossy fiber terminals of the primate hippocampus: an ultrastructural study. J Comp Neurol 303: 177– 192. Shepherd GM, (1990) The organization of the brain, Third edition, pp 237, 393. New York: Oxford University Press. Staley KJ, Soldo BL, Proctor WR, (1995) Ionic mechanisms of neuronal excitation by inhyibitory GABAA receptors. Science 269: 977– 981. Acsády L, Arabadzisz D, Freund TF, (1996) Correlated morphological and neurochemical features identify different subsets of VIP-immunoreactive interneurons in rat hippocampus. Neuroscience (in press). Acsády L, Görcs TJ, Freund TF, (1996) Different populations of VIP-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus. Neuroscience (in press). Aika Y, Ren JQ, Kosaka K, Kosaka T, (1994) Quantivtative analysis of GABA-like immunoreactivity and parvalbumin-containing neurons in the CA1 region of the rat hippocampus using a stereological method, the dissector. Exp Brain Res 99: 267– 276. Amaral DG, (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 182: 851– 914. Auerbach JM, Segal M, (1994) A novel cholinergic induction of long term potentiation in rat hippocampus. J Neurophysiol controlling depression and long term potentiation in the rat hippocampus. J Physiol (Lond) 492: 497– 493. Bergles DE, Doze VA, Madison DA, Smith SJ, (1996) Excitatory actions of norepinephrine on multiple calsses of hippocampal CA1 interneurons. J Neurosci 16: 572– 585. Bijak M, Misgeld U, (1995) Adrenergic modulation of hilar neuron activity and granule cell inhibition in the guinea-pig hippicampal slice. Neuroscience 67: 541– 550. Blasco-Ibanez JM, Freund TF, (1995) Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CA1 subfield: structural basis of feed-back activation. Eur J Neurosci 7: 2170– 2180. Bochet P, Audinat E, Lambolez B, Crepel F, Rossier J, Iino M, Tsuzuke K, Ozawa S, (1994) Subunit composition at the single cell level explains functional properties of a glutamate-gated channel. Neuron 12: 383– 388. Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsáki G, (1995) Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15: 47– 60. Brunner H, Misgelld U, (1994) Muscarinic amplification of fast excitation in hilar neurones and inhibition in granule cells in the guineapig hippocampus. J Physiol (Lond) 480: 513– 526. Buckmaster PS, Schwartzkroin PA, (1995) Interneurons and inhibition in the dentate gyrus of the rat in vivo. J Neurosci 15: 774– 789. Buckmaster PS, Schwartzkroin PA, (1995) Physiological and morphological heterogeneity of dentate gyrus-hilus interneurons in the gerbil hippocampus in vivo. Eur J Neurosci 7: 1393– 1402. Buckmaster PS, HJ Wenzel, DD Kunkel, PA Schwartzkroin, (1996) Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo. J Comp Neurol 366: 270– 292. Buhl EH, Cobb SR, Halasy K, Somogyi P, (1995) Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. Eur J Neurosci 7: 1989– 2004. Buhl EH, Otis TS, Mody I, (1996) Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science 271: 369– 373. Buzsáki G, Chrobak JJ, (1995) Temporal structure in spatially organized neuronal ensembles: a role for interneuron networks. Curr Opin Neurobiol 5: 504– 510. Catania MV, Tolle TR, Monyer H, (1995) Differential expression of AMPA receptor subunits in NOS-positive neurons of cortex, striatum, and hippocampus. J Neurosci 15: 7046– 7061. Cobb SR, Buhl EH, Halasy K, Paulsen P, Somogyi P, (1995) Synchronisation of neuronal activity in hippocmpus by individual GABAergic interneurones. Nature 378: 75– 78. Choen GA, Doze VA, Madison DV, (1992) Opioid inhibition of GABA release from presynaptic terminals of rat hippocampal interneurons. Neuron 9: 325– 335. Czeh B, Czurko A, Seress L, (1996) Distribution of NADPH-d positive cells in the hippocampus following neonatal X-ray irradiation induced granule cell loss. Eur J Neurosci [Suppl 8]: 1. Deller T, Nitsch R, Frotscher M, (1994) Associational and commissural afferents of parvalvumin-immunoreactive neurons in the rat hippocampus: a combined immunocytochemical and PHA-L study. J Comp Neurol 350: 612– 622. Desai MA, McBain CJ, Kauer JA, Conn PJ, (1994) Metabotropic glutamate receptor-induced disinhibition is mediated by reduced transmission at excitatory synapses onto interneurons and inhibitory synapses onto pyramidal cells. Neurosci Lett 181: 78– 82. Doze VA, Cohen GA, Madison DV, (1991) Synaptic localization of adrenergic disinhibition in the rat hippocampus. Neuron 6: 889– 900. Doze VA, Cohen GA, Madison DV, (1995) Calcium channel involvement in GABAB receptor-mediated inhibition of GABA release in area CA1 of the rat hippocampus. J Neurophysiol 74: 43– 53. Du J, Zhang L, Weiser M, Rudy B, McBain CJ, (1996) Developmental expression and functional characterization of the potassium channel subunit Kv3. 1b in parvalbumin-containing interneurons in the rat hippocampus. J Neurosci 16: 506– 518. Dupuy ST, Houser CR, (1995) Early appearance and generation of a prominent population of GAD67 -containing neurons in the developminent rat hippocampal formation. Soc Neurosci Abstr 21: 306. Esclapez M, Houser CR, (1995) Somatostatin neurons are a subpopulation of GABA neurons in the rat dentate gyrus: evidence from co-localization of pre-prosomatostatin and glutamate decarboxylase mRNAs. Neuroscience 64: 339– 355. Gaiarsa JL, McLean HA, Congar P, Leinkugel X, Khazipov R, Tseeb V, Ben-Ari Y, (1995) Postnatal maturation of gamma-amminobutyric acidA and B-mediated inhibition in the CA3 hippocampal region of the rat. J Neurobiol 26: 339– 349. Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, Jonas P, Monyer H, (1995) Relative abundance of subunit mRNAs determines gating and CA2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15: 193– 204. Ghadimi BM, Jarolimek W, Misgeld U, (1994) Effects of serotonin on hilar neurons and granule cell inhibition in the guinea pig hippocampal slice. Brain Res 63: 27– 32. Gulyás AI, Miles R, Hájos N, Freund TF, (1993) Precision and variability in post-synaptic target selection of inhibitory cells in hippocampal CA3 region. Eur J Neurosci 5: 1729– 1751. Gulyás AI, Hájos N, Freund TF, (1996) Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci (in press). Hájos N, Acsády L, Freund TF, (1996) Target selectivity and neurochenmical charavteristics of VIP-immunoreactive interneurons in the rat dentate gyrus. Eur J Neurosci (in press). Han Z-S, Buhl EH, Lorinczi Z, Somogyi P, (1993) A high degree of spatial selectivity in the axonal and dendritic domains of physiologically identified local-circuit neurons in the dentate gyrus of rat hippocampus. Eur J Neurosci 5: 395– 410. Heimrich B, Papp EC, Freund TF, Frotscher, M, (1996) Regeneration of the GABAergic septhippocampal projection in vitro. Neuroscience 72: 409– 417. Houser CR, Esclapez M, (1994) Localization of mRNAs encoding two forms of glutamic acid decarboxylase in the rat hippocampal formation. Hippocampus 4: 530– 545. Iino M, Ozawa S, Tsuzuki K, (1990) Permeation of calcium through excitatory amino acid recetor channels in cultured rat hioppocampal neurones. J Physiol (Lond) 424: 151– 165. Isa T, Iion M, Itazawa S, Ozawa S, (1995) Spermine mediates inward rectification of CA2+ -permeable AMPA receptor channels. Neuroreport 6: 2045– 2048. Isa T, Itazawa S, Iion M, Tsuzuki K, Ozawa S, (1996) Distribution of neurones expressing inwardly rectifying and Ca2+ -permeable AMPA. receptors in rat hippocampal slices. J Phaysiol (Lond) 491: 719– 733. Isa T, Iion M, Ozawa S, (1996) Spermine blocks synaptic transmission mediated by Ca2+ -permeable AMPA receptors. Neuroreport 7: 689– 692. Jefferys, JGR, Traub Whittington MA, (1996) Neuronal networks for induced “40 Hz” rhythms. Trends Neurosci 19: 202– 208. Karsumaru H, Kosaka T, Heizmann CW, Hama K, (1988) Gap junctions on GAB Aergic neurons contaiing the calcium-binding protein parvalbumin in the rat hippocampus (CA1 region). Exp Brain Res 72: 363– 370. Khazipov R, Bregestovski P, Ben-Ari Y, (1993) Hippocampal inhibitory inter neurons are functionally fromexcitatory inputs by anoxia. J Neurophysiol 70: 2251– 2259. Knowles WD, Schwartzkrion PA, (1981) Local circuit intractions in hippocampal brain slices. J Neurosci 1: 318– 322. Kosaka T, Hama K, (1985) Gap junctions between non-pyramidalcell dendrites in the rat hippocampus (CA1 and CA3 regions): a combined Glogi-electron microscopy study. J Comp Neurol 231: 150– 161. Kunkel DD, Schwartzkroin PA, (1988) Ultrastructural charactrization and GAD co-localization of somatostatin-like immunoreactive neurons in CA1 of rabbit hippocampus. Synapse 2: 371– 381. Lacaille J-C, Kunkel DD, Schwartzkroin PA, (1989) Electrophysiological and morphological charactrization of hippocampalinterneurons. In: The hippocampus: newvistas ( Kohler C Chan-Play, eds) pp 287– 305. New York: AlanR. Liss Inc. Lamberr NA, Wilson WA, (1993) Heterogeneity in presynaptic regulation of GABA release from hippocampal inhibitory neurons. Neuron 11: 1057– 1067. Lambert NA, Wilson WA, (1996) High-threshold Ca2+ -currents in hippocampal inter neurones and their selective inhibition by activation of GABAB reseptors. J Physiol (Lond) 492: 115– 127. Leinkugel X, Ben-Ari Y, Bregestovski P, (1995) Synaptic GABAA activation induces calcium rise in pyramidal cells and interneurons from rat neoatalhippocampal slices. J Physiol 487: 319– 329. Leranth C, Nitsch R, (1994) Hypothalamic substance P-containing afferentscan filter the signal flow in the monkey hippocampal formation: morphological evidence for stimulation and feed-forword inhibitation of different populations of granule cells and indirect inhibition of CA3 pyramidal neurons. J Neurosci 14: 4079– 4094. Leranth C, Szeidemann Z, Hsu M, Buzsaki G, (1995) AMPA receptors in the rat and primate hippocampus: absence of GluR2subunits in most inter neurons. Neuroscience 70: 631– 652. Liu Y, Fujise N, Kosaka T, (1996) Distribution of calretinin immunoreactivity in the mouse dentate gyrus: I. General discription. Exp Brain Res 108: 389– 403. Maccaferri G, McBain CJ, (1995) Passive propagation of LTD to stratum oriens-alveusinhibitory neuronsmodulates the temporammonic input to the hippocampal CA1 region. 15: 137– 145. Madison DV, Nicoll RA, (1984) Enkephalm hyperpolarizes interneurons in the rat hippocampus. J Physiol (Lond) 354: 319– 331. McBain CJ, DiChiara, TJ, Kauer, JA, (1994) Activation of metabottopic glutamate receptors differentially affects two classes of hippocampal interneurons and potentiates excitatory synaptic trasmission. J Neurosci 14: 4433– 4445. McLean HA, Rovira C, Ben-Ari Y, Gaiarsa JL, (1995) NMDA-dependent GABAA-mediated polysynaptic potentials in the neonatal rat hippocampus. Eur J Neurosci 7: 1442– 1448. McLean HA, Caillard O, Khazipov R, Ben-Ari Y, Gaiarsa JL, (1996) Spontaneous release of GABAB receptors and controls network activity in the neonatal rat hippocampus. J Neurophysiol (in press). Michelson HB, Wong RKS, (1994) Synchronization of inhibitory neurones in the guinea-pighippocampus in vitro. J Physiol (Lond) 477: 35– 45. Miles R, Tóth K, Gulyás AI, Hájos N, Freund TF, (1996) Distinc functional roles for somatic and dendritic inhibition in the hippocampus. Neuron 16: 815– 823. Morin F, Beaulieu C, Lacaille J_C, (1996) Membrane properties and synaptic currents evoked in CA1 inter neuron subtypes in rat hippocampal slices. J Neurophysiol (in press). Nitsch R, Leranth C, (1994) Sprouting of intrinsic substance P-immunoreactive fibers in the monkey dentate gyrus following denervatuion from its substace P-cintaining hypothalamic afferents. Exp Brain Res 100: 522– 526. Nitsch R, Leranth C, (1996) GABAergic neurons in the rat dentate gyrus are innervatedby subcortical calretinin-containing afferents. J Comp Neuronl 364: 425– 438. Nitsch R, Soriano E, Frotscher M, (1990) The parvalbumin-containing nonpyramidal neurons in the rat hippocampus. Anat Embryol (Berl) 181: 413– 425. Otis TS, De Koninck Y, Mody I, (1994) Lasting potentiation of inhibition is associated with an increased number of gamma-aminobutyric acid type A receptors during miniture inhibitory postsynaptic currents. Proc Nat Acad Sci USA 91: 7698– 7702. Ouardouz M, Lacaille J_C, (1995) Mechanismsof selectivelong-term potentiation of excitatory synapses in stratum oriens/alveus interneurons of rat hippocampalslices. J Neurophysiol 73: 810– 819. Ozawa S, Lino M, (1993) Two disticnt types of AMPA responces in cultured rat hippocampal neurons. Neurosci Lett. 155: 187– 190. Perez Y, Lacaille J-C, (1995) Changes in early and late IPSPs in CA1 pyramidal cells after high frequency stimulation of Schaffer collaterals. Soc Neurosci Abstr 21: 1100. Pierce RJ, Lewin GR, (1994) An ultrastructural size principle. Neuroscience 58: 441– 446. Ribak CE, (1992) Local circuitry of GABAergic basket cells in the dentategyrus. In: The dentate gyrus and its role in seizures ( CE Ribak, CM Gall, I Mody, eds) pp 29– 47 Amsterdom Elsevier. Ribak CE, Navetta MS, (1994) An immature mossy fiber innervation of hilar neurons may explain their resistance to kainate-induced cell death in 15-day-old rats. Dev Brain Res 79: 47– 62. Ribak CE, Seress L, (1983) Five types of basket cell in the hippocampal dentate gyrus. J Neurocytol 12: 577– 597. Rocamora N, Pascual M, Acsády L, Lecea L, Freund T, Soriano E, (1996) Hippocampal interneurons expressing NGF and NT3 are specific targets of the GABAergic septohippocampal pathway. J Neurosci (in press). Scharfman HE, (1992) Differentiation of rat dentate neurons by morphology and electrophysiology in hippocampal slices: granule cells, spiny hilar cells, and aspiny “fast-spiking” cells. In: The dentate gyrus and its role in seizures ( CE Ribak, CM Gall, I Mody, eds) pp 93– 109 Amsterdom: Elsevier. Scharfman HE, (1995) Electrophysiological diversity of pyramidal-shaped neurons at the granule cell layer/hilus border of the rat dentate gyrus recorded in vitro. Hippocampus 5: 287– 305. Schwartzkroin PA, Mathers LH, (1978) Physiological and morphological identification of a nonpyramidal hippocampal cell type. Brain Res 157: 1– 10. Seress L, Frotscher M, (1991) Basket cells in the fascia dentate: a Golgi/electron microscopic study. J Neurocytol 20: 915– 928. Seress L, Ribak CE, (1988) The development of GABAergic neurons in the rat hippocampal formation. An immunocytochemical study. Dev Brain Res 44: 197– 209. Seress L, Ribak CE, (1990) Postatal development of the light electron microscopic feature of basket cells in the hippocampal dentate gyrus of the rat. Anat Embrol (Berl) 181: 547– 565. Seress L, Frotscher M, Ribak CE, (1989) Local circuit neurons in both the detate gyrus and Ammon's horn establish synaptic connections with principal neurons in five day old rats: a morphological basis for inhibitation in early development. Exp Brain Res 78: 1– 9. Seress L, Nitsch R, Leranth C, (1993) Calretinin immunoreactivity in the monkey hippocampal formation. I. Light and electron microscopic characteristics and colocalization with other calcium binding proteins. Neuroscience 55: 775– 796. Silk A, Ylinen A, Penttonen M, Buzsaki G, (1994) Inhibitory CA1-CA3-hilar region feedback in the hippocampus. Science 264: 1722– 1724. Silk A, Penttonen M, Ylinen A, Buzsaki G, (1995) Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci 15: 6651– 6665. Sloviter RS, Brisman JL, (1995) Lateral inhibition and granule cell synchrony in the rat hippocampal dentate gyrus. J Neurosci 15: 811– 820. Sloviter RS, Sollas AL, Dean E, Dichter MA, (1995) Immunocytochemical localization of 65-kDa glutamic acid decarboxylase (CAD) and GABA-like immunoreactivities (LI) in the rat hippocampal formation: GAD67- and GABA-LI are rapidly induced by afferent stimulation, kainic acid, or pilocarpine. Soc Neurosci Abstr 21: 1968. Soltesz I, Deschenes, (1993) Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of thee rat hippocampus under ketamine-xylazine anesthesia. J Neurophysiol 70: 97– 116. Soltesz I, Mody I, (1994) Patch-clamp recordings reveal powerful GABAergic in inhibitation in dentate neurons. J Neuronsci 14: 2365– 2376. Soltesz I, Smetters DK, Mody I, (1995) Tonic inhibition originates from synapses close to the soma. Neuron 14: 1273– 1283. Soriano E, Frotscher M, (1993) GABAergic innervation of the rat fascia dentata: a novel type of interneuron in the granule cell layer with extensive axonal arborization in the molecular layer. J Comp Neurol 334: 385– 396. Soriano E, Nitsch R, Frotscher M, (1990) Axo-axonic chandelier cells in the rat fascia dentata: Golgi-electron microscopy and immunocytochamical studies. J Comp Neurol 293: 1– 25. Soriano E, Del Rio JA, Martinez A, Super H, (1994) The organization of the embryonic and early postnatal murine hippocampus. I. Immunocytochemical charactrization of neurol populations in the subplate and marginal zone. I Comp Neurol 342: 571– 595. Stelzer A, (1992) GABAA receptors control excitability of neuronal populations. Int Rev Neurobiol 33: 195– 287. Stelzer A, Shi H, (1994) Impairment of GABAA-receptors function by NMDA-mediated calcium influx in isolated CA1 pyramidal cells. Neuroscience 62: 813– 828. Stelzer A, Simon G, Kovacs G, Rai R, (1994) Synaptic disinhibition during maintenance of long-term potentiation in the CA1 hippocampal subfield. Proc Nat Acad Sci USA 91: 3058– 3062. Super H, Soriano E, (1994) The organization of the embryonic and early postnatal murine hippocampus. II. Development of entorhinal, commissural and septal connections studied with the lipophilic tracer Dil. J Comp Neurol 344: 101– 120. Traub RD, (1995) Model of synchronized population bursts in electrically coupled interneurons containing active dendritic conductances. J Comput Neurosci 2: 283– 289. Traub RD, Miles R, (1995) Pyramidal cell-to-inhibitory cell spike transduction explicable by active dendritic conductances in inhibitory cell. J Comput Neuroscience 2: 291– 298. Traub RD, Whittington MA, Colling SB, Buzsáki G, Jefferys JGR, (1996) Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. I Physiol (Lond)(in press). Wang XJ, (1993) Ionic basis for intrinsic-40Hzoscillations. Neuroreport 5: 221– 224. Wang X-J, Rinzel J, (1993) Spindle rhythmicity in the reticularis thalami nucleus synchronization among mutually inhibitory neurons. Neuroscience 53: 899– 904. Wang JH, Stelzer A, (1996) Shared calcium signalling pathways in the induction of long-term potentiation and synaptic dichibition in CA1 pyramidal cell dendrites. J Neurophsiol 75: 1687– 1702. Whittington MA, Traub RD, Jefferys JGR, (1995) Synchronized oscillations in interneurons networks driven by metabotropic glutamate receptors activation. Nature 373: 612– 615. Wilson MA, McNaughton BL, (1993) Dynamics of the hippocampal ensemble code for space. Science 261: 1055– 1058. Wilson MA, McNaughton BL, (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265: 676– 679. Xie CW, Lewis DV, (1995) Endogenous opioids regulate LTP of synaptic inhibition in the dentate gyrus of the rat. J Neurosci 15: 3788– 3795. Ylinen A, Soltez 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. Zhang L, McBain Cj (1995a) Voltage-grated potassium currents in stratum oriens-alveus inhibitory neurones of the rat CA1 hippocampus. J Physiol (Lond) 488: 647– 660. Zhang L, McBain Cj, (1995) Potassium conductances underlying action potential repolarization and afrerhyperpolarization in stratum oriens-alveus inhibitory neurones of the rat CA1 hippocampus. J Physiol (Lond) 488: 661– 672. Citing Literature Volume6, Issue31996Pages 330-339 ReferencesRelatedInformation
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