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J Physiol. 1994 Dec 1; 481(Pt 2): 395–405.
PMCID: PMC1155938

Excitatory synaptic connections onto rat hippocampal inhibitory cells may involve a single transmitter release site.


1. Whole-cell tight-seal records of excitatory postsynaptic currents (EPSCs) were made from inhibitory cells in the CA3 region of thin hippocampal slices. We tested the hypothesis that excitatory synaptic connections made on inhibitory cells involve few transmitter release sites. 2. EPSCs impinging on inhibitory cells had a time to peak of 0.4-3.8 ms and an amplitude of 8-90 pA at a holding potential of -60 mV. They were suppressed by the excitatory amino acid antagonists 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) and DL-2-amino-5-phosphonovaleric acid (APV). 3. Addition of tetrodotoxin (TTX) and Co2+ to the external solution reduced the frequency of EPSCs from 0.90 to 0.25 s-1 (n = 24 cells). In the majority of cells EPSC amplitude distributions were not significantly changed. 4. Increasing Ca2+ and reducing Mg2+ in the external solution, in order to enhance the probability of transmitter release, did not change EPSC amplitude distributions. In contrast, amplitude histograms for IPSCs recorded from pyramidal cells were shifted to higher mean values in this solution. 5. EPSCs were elicited in inhibitory cells by electrical stimulation via a glass pipette placed near to pyramidal cells in stratum pyramidale. EPSCs elicited by weak stimuli had similar amplitude distributions to excitatory synaptic events recorded in the presence of TTX and Co2+. 6. These findings suggest excitatory synaptic connections made with CA3 inhibitory cells involve few or possibly just one transmitter release site.

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  • Bekkers JM, Richerson GB, Stevens CF. Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5359–5362. [PMC free article] [PubMed]
  • Brown AG, Fyffe RE. Direct observations on the contacts made between Ia afferent fibres and alpha-motoneurones in the cat's lumbosacral spinal cord. J Physiol. 1981;313:121–140. [PMC free article] [PubMed]
  • Busch C, Sakmann B. Synaptic transmission in hippocampal neurons: numerical reconstruction of quantal IPSCs. Cold Spring Harb Symp Quant Biol. 1990;55:69–80. [PubMed]
  • Edwards FA, Konnerth A, Sakmann B. Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch-clamp study. J Physiol. 1990 Nov;430:213–249. [PMC free article] [PubMed]
  • Edwards FA, Konnerth A, Sakmann B, Takahashi T. A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflugers Arch. 1989 Sep;414(5):600–612. [PubMed]
  • Faber DS, Young WS, Legendre P, Korn H. Intrinsic quantal variability due to stochastic properties of receptor-transmitter interactions. Science. 1992 Nov 27;258(5087):1494–1498. [PubMed]
  • Gulyás AI, Miles R, Hájos N, Freund TF. Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur J Neurosci. 1993 Dec 1;5(12):1729–1751. [PubMed]
  • Gulyás AI, Miles R, Sík A, Tóth K, Tamamaki N, Freund TF. Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature. 1993 Dec 16;366(6456):683–687. [PubMed]
  • Hestrin S. Activation and desensitization of glutamate-activated channels mediating fast excitatory synaptic currents in the visual cortex. Neuron. 1992 Nov;9(5):991–999. [PubMed]
  • Jack JJ, Redman SJ, Wong K. The components of synaptic potentials evoked in cat spinal motoneurones by impulses in single group Ia afferents. J Physiol. 1981 Dec;321:65–96. [PMC free article] [PubMed]
  • JENKINSON DH. The nature of the antagonism between calcium and magnesium ions at the neuromuscular junction. J Physiol. 1957 Oct 30;138(3):434–444. [PMC free article] [PubMed]
  • Kisvárday ZF, Martin KA, Whitteridge D, Somogyi P. Synaptic connections of intracellularly filled clutch cells: a type of small basket cell in the visual cortex of the cat. J Comp Neurol. 1985 Nov 8;241(2):111–137. [PubMed]
  • Korn H, Mallet A, Triller A, Faber DS. Transmission at a central inhibitory synapse. II. Quantal description of release, with a physical correlate for binomial n. J Neurophysiol. 1982 Sep;48(3):679–707. [PubMed]
  • Kuno M, Takahashi T. Effects of calcium and magnesium on transmitter release at Ia synapses of rat spinal motoneurones in vitro. J Physiol. 1986 Jul;376:543–553. [PMC free article] [PubMed]
  • Lisman JE, Harris KM. Quantal analysis and synaptic anatomy--integrating two views of hippocampal plasticity. Trends Neurosci. 1993 Apr;16(4):141–147. [PubMed]
  • Livsey CT, Vicini S. Slower spontaneous excitatory postsynaptic currents in spiny versus aspiny hilar neurons. Neuron. 1992 Apr;8(4):745–755. [PubMed]
  • Llano I, Gerschenfeld HM. Inhibitory synaptic currents in stellate cells of rat cerebellar slices. J Physiol. 1993 Aug;468:177–200. [PMC free article] [PubMed]
  • Llinas R, Bloedel JR, Hillman DE. Functional characterization of neuronal circuitry of frog cerebellar cortex. J Neurophysiol. 1969 Nov;32(6):847–870. [PubMed]
  • Llinás R, Nicholson C. Reversal properties of climbing fiber potential in cat Purkinje cells: an example of a distributed synapse. J Neurophysiol. 1976 Mar;39(2):311–323. [PubMed]
  • McBain C, Dingledine R. Dual-component miniature excitatory synaptic currents in rat hippocampal CA3 pyramidal neurons. J Neurophysiol. 1992 Jul;68(1):16–27. [PubMed]
  • McBain CJ, Dingledine R. Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. J Physiol. 1993 Mar;462:373–392. [PMC free article] [PubMed]
  • Malinow R. Transmission between pairs of hippocampal slice neurons: quantal levels, oscillations, and LTP. Science. 1991 May 3;252(5006):722–724. [PubMed]
  • Manabe T, Renner P, Nicoll RA. Postsynaptic contribution to long-term potentiation revealed by the analysis of miniature synaptic currents. Nature. 1992 Jan 2;355(6355):50–55. [PubMed]
  • Miles R. Variation in strength of inhibitory synapses in the CA3 region of guinea-pig hippocampus in vitro. J Physiol. 1990 Dec;431:659–676. [PMC free article] [PubMed]
  • Miles R, Wong RK. Excitatory synaptic interactions between CA3 neurones in the guinea-pig hippocampus. J Physiol. 1986 Apr;373:397–418. [PMC free article] [PubMed]
  • Raastad Morten, Storm Johan F, Andersen Per. Putative Single Quantum and Single Fibre Excitatory Postsynaptic Currents Show Similar Amplitude Range and Variability in Rat Hippocampal Slices. Eur J Neurosci. 1992 Oct;4(1):113–117. [PubMed]
  • Redman S. Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol Rev. 1990 Jan;70(1):165–198. [PubMed]
  • Ropert N, Miles R, Korn H. Characteristics of miniature inhibitory postsynaptic currents in CA1 pyramidal neurones of rat hippocampus. J Physiol. 1990 Sep;428:707–722. [PMC free article] [PubMed]
  • Sayer RJ, Friedlander MJ, Redman SJ. The time course and amplitude of EPSPs evoked at synapses between pairs of CA3/CA1 neurons in the hippocampal slice. J Neurosci. 1990 Mar;10(3):826–836. [PubMed]
  • Scanziani M, Capogna M, Gähwiler BH, Thompson SM. Presynaptic inhibition of miniature excitatory synaptic currents by baclofen and adenosine in the hippocampus. Neuron. 1992 Nov;9(5):919–927. [PubMed]
  • Silver RA, Traynelis SF, Cull-Candy SG. Rapid-time-course miniature and evoked excitatory currents at cerebellar synapses in situ. Nature. 1992 Jan 9;355(6356):163–166. [PubMed]
  • Somogyi P, Kisvárday ZF, Martin KA, Whitteridge D. Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience. 1983 Oct;10(2):261–294. [PubMed]
  • Somogyi P, Nunzi MG, Gorio A, Smith AD. A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells. Brain Res. 1983 Jan 17;259(1):137–142. [PubMed]
  • Tracey DJ, Walmsley B. Synaptic input from identified muscle afferents to neurones of the dorsal spinocerebellar tract in the cat. J Physiol. 1984 May;350:599–614. [PMC free article] [PubMed]
  • Van der Kloot W. The regulation of quantal size. Prog Neurobiol. 1991;36(2):93–130. [PubMed]
  • Wyllie DJ, Traynelis SF, Cull-Candy SG. Evidence for more than one type of non-NMDA receptor in outside-out patches from cerebellar granule cells of the rat. J Physiol. 1993 Apr;463:193–226. [PMC free article] [PubMed]

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