Subcellular patch-clamp techniques for single-bouton stimulation and simultaneous pre- and postsynaptic recording at cortical synapses

David Vandael, Yuji Okamoto, Carolina Borges-Merjane, Victor Vargas-Barroso, Benjamin A. Suter, Peter Jonas

Published: 2021-05-13 DOI: 10.1038/s41596-021-00526-0

patch-clamp

cortical synapses

presynaptic recording

postsynaptic recording

unitary synaptic events

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Reporting Summary

Supplementary Video 1

MFB–CA3 pyramidal neuron paired recording under experimental conditions.

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Subcellular patch-clamp techniques for single-bouton stimulation and simultaneous pre- and postsynaptic recording at cortical synapses

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Adler, E. M., Augustine, G. J., Duffy, S. N. & Charlton, M. P. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J. Neurosci. 11, 1496–1507 (1991).
Llinás, R. R. The Squid Giant Synapse: A Model for Chemical Transmission (Oxford University Press, 1999).
Forsythe, I. D. Direct patch recording from identified presynaptic terminals mediating glutamatergic EPSCs in the rat CNS, in vitro. J. Physiol. 479, 381–387 (1994).
von Gersdorff, H. & Borst, J. G. G. Short-term plasticity at the calyx of Held. Nat. Rev. Neurosci. 3, 53–64 (2002).
Neher, E. Some subtle lessons from the calyx of Held synapse. Biophys. J. 112, 215–223 (2017).
Borst, J. G. G. & Sakmann, B. Calcium influx and transmitter release in a fast CNS synapse. Nature 383, 431–434 (1996).
Vyleta, N. P. & Jonas, P. Loose coupling between Ca2+ channels and release sensors at a plastic hippocampal synapse. Science 343, 665–670 (2014).
Lindau, M. & Neher, E. Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflügers Arch. 411, 137–146 (1988).
von Gersdorff, H. & Mathews, G. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367, 735–739 (1994).
Hallermann, S., Pawlu, C., Jonas, P. & Heckmann, M. A large pool of releasable vesicles in a cortical glutamatergic synapse. Proc. Natl. Acad. Sci. USA 100, 8975–8980 (2003).
Delvendahl, I., Vyleta, N. P., von Gersdorff, H. & Hallermann, S. Fast, temperature-sensitive and clathrin-independent endocytosis at central synapses. Neuron 90, 492–498 (2016).
Nicoll, R. A. & Schmitz, D. Synaptic plasticity at hippocampal mossy fibre synapses. Nat. Rev. Neurosci. 6, 863–876 (2005).
Espinoza, C., Guzman, S. J., Zhang, X. & Jonas, P. Parvalbumin+ interneurons obey unique connectivity rules and establish a powerful lateral-inhibition microcircuit in dentate gyrus. Nat. Commun. 9, 4605 (2018).
Akaike, N., et al. Focal stimulation of single GABAergic presynaptic boutons on the rat hippocampal neuron. Neurosci. Res. 42, 187–195 (2002).
Vyleta, N. P., Borges-Merjane, C. & Jonas, P. Plasticity-dependent, full detonation at hippocampal mossy fiber-CA3 pyramidal neuron synapses. eLife 5, e17977 (2016).
Vandael, D., Borges-Merjane, C., Zhang, X. & Jonas, P. Short-term plasticity at hippocampal mossy fiber synapses is induced by natural activity patterns and associated with vesicle pool engram formation. Neuron 107, 509–521.e7 (2020).
Chicurel, M. E. & Harris, K. M. Three-dimensional analysis of the structure and composition of CA3 branched dendritic spines and their synaptic relationships with mossy fiber boutons in the rat hippocampus. J. Comp. Neurol. 325, 169–182 (1992).
Rollenhagen, A. et al. Structural determinants of transmission at large hippocampal mossy fiber synapses. J. Neurosci. 27, 10434–10444 (2007).
Borges-Merjane, C., Kim, O. & Jonas, P. Functional electron microscopy, ‘flash and freeze,’ of identified cortical synapses in acute brain slices. Neuron 105, 992–1006 (2020).
Rancz, E. A. et al. High-fidelity transmission of sensory information by single cerebellar mossy fibre boutons. Nature 450, 1245–1248 (2007).
Ritzau-Jost, A. et al. Ultrafast action potentials mediate kilohertz signaling at a central synapse. Neuron 84, 152–163 (2014).
Vivekananda, U. et al. Kv1.1 channelopathy abolishes presynaptic spike width modulation by subthreshold somatic depolarization. Proc. Natl. Acad. Sci. USA 114, 2395–2400 (2017).
Kawaguchi, S. Y. & Sakaba, T. Fast Ca2+ buffer-dependent reliable but plastic transmission at small CNS synapses revealed by direct bouton recording. Cell Rep. 21, 3338–3345 (2017).
Ritzau-Jost, A. et al. Large, stable spikes exhibit differential broadening in excitatory and inhibitory neocortical boutons. Cell Rep. 34, 108612 (2021).
Geiger, J. R. P. & Jonas, P. Dynamic control of presynaptic Ca2+ inflow by fast-inactivating K+ channels in hippocampal mossy fiber boutons. Neuron 28, 927–939 (2000).
Bischofberger, J., et al. Patch-clamp recording from mossy fiber terminals in hippocampal slices. Nat. Protoc. 1, 2075–2081 (2006).
Perkins, K. L. Cell-attached voltage-clamp and current-clamp recording and stimulation techniques in brain slices. J. Neurosci. Methods 154, 1–18 (2006).
Alcami, P., Franconville, R., Llano, I. & Marty, A. Measuring the firing rate of high-resistance neurons with cell-attached recording. J. Neurosci. 32, 3118–3130 (2012).
Engel, D. & Jonas, P. Presynaptic action potential amplification by voltage-gated Na+ channels in hippocampal mossy fiber boutons. Neuron 45, 405–417 (2005).
Dodt, H. U. & Zieglgänsberger, W. Infrared videomicroscopy: a new look at neuronal structure and function. Trends Neurosci. 17, 453–458 (1994).
Jonas, P., Major, G. & Sakmann, B. Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J. Physiol. 472, 615–663 (1993).
Lawrence, J. J., Grinspan, Z. M. & McBain, C. J. Quantal transmission at mossy fibre targets in the CA3 region of the rat hippocampus. J. Physiol. 554, 175–193 (2004).
Kamiya, H., Shinozaki, H. & Yamamoto, C. Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses. J. Physiol. 493, 447–455 (1996).
Shigemoto, R. et al. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J. Neurosci. 17, 7503–7522 (1997).
Weisskopf, M. G. & Nicoll, R. A. Presynaptic changes during mossy fibre LTP revealed by NMDA receptor-mediated synaptic responses. Nature 376, 256–259 (1995).
Ben-Simon, Y. et al. A combined optogenetic-knockdown strategy reveals a major role of tomosyn in mossy fiber synaptic plasticity. Cell Rep. 12, 396–404 (2015).
Mori, M., Abegg, M. H., Gähwiler, B. H. & Gerber, U. A frequency-dependent switch from inhibition to excitation in a hippocampal unitary circuit. Nature 431, 453–456 (2004).
Bischofberger, J., Geiger, J. R. P. & Jonas, P. Timing and efficacy of Ca2+ channel activation in hippocampal mossy fiber boutons. J. Neurosci. 22, 10593–10602 (2002).
Martinello, K., et al. The subthreshold-active Kv7 current regulates neurotransmission by limiting spike-induced Ca2+ influx in hippocampal mossy fiber synaptic terminals. Commun. Biol. 2, 145 (2019).
Alle, H. & Geiger, J. R. P. Combined analog and action potential coding in hippocampal mossy fibers. Science 311, 1290–1293 (2006).
Szabadics, J. & Soltesz, I. Functional specificity of mossy fiber innervation of GABAergic cells in the hippocampus. J. Neurosci. 29, 4239–4251 (2009).
Amaral, D. G. & Dent, J. A. Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J. Comp. Neurol. 195, 51–86 (1981).
Bazigou, E. et al. Genes regulating lymphangiogenesis control venous valve formation and maintenance in mice. J. Clin. Invest. 121, 2984–2992 (2011).
Geiger, J. R. P. et al. Patch-clamp recording in brain slices with improved slicer technology. Pflügers Arch. 443, 491–501 (2002).
Edwards, F. A., Konnerth, A., Sakmann, B. & Takahashi, T. A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflügers Arch. 414, 600–612 (1989).
Guzman, S. J., Schlögl, A. & Schmidt-Hieber, C. Stimfit: quantifying electrophysiological data with Python. Front. Neuroinform. 8, 16 (2014).
Williams, S. R. & Mitchell, S. J. Direct measurement of somatic voltage clamp errors in central neurons. Nat. Neurosci. 11, 790–798 (2008).
del Castillo, J. & Katz, B. Changes in end-plate activity produced by presynaptic polarization. J. Physiol. 124, 586–604 (1954).
Li, L., Bischofberger, J. & Jonas, P. Differential gating and recruitment of P/Q-, N-, and R-type Ca2+ channels in hippocampal mossy fiber boutons. J. Neurosci. 27, 13420–13429 (2007).
Pernía-Andrade, A. J. et al. A deconvolution-based method with high sensitivity and temporal resolution for detection of spontaneous synaptic currents in vitro and in vivo. Biophys. J. 103, 1429–1439 (2012).
Zhang, X., Schlögl, A., Vandael, D. & Jonas, P. MOD: a novel machine-learning optimal-filtering method for accurate and efficient detection of subthreshold synaptic events in vivo. J. Neurosci. Methods https://doi.org/10.1016/j.jneumeth.2021.109125 (2021).
Miyano, R., Miki, T. & Sakaba, T. Ca-dependence of synaptic vesicle exocytosis and endocytosis at the hippocampal mossy fibre terminal. J. Physiol. 597, 4373–4386 (2019).
Schneggenburger, R. & Neher, E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406, 889–893 (2000).
Bollmann, J. H., Sakmann, B. & Borst, J. G. G. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289, 953–957 (2000).
Midorikawa, M. & Sakaba, T. Kinetics of releasable synaptic vesicles and their plastic changes at hippocampal mossy fiber synapses. Neuron 96, 1033–1040 (2017).
Henze, D. A., McMahon, D. B., Harris, K. M. & Barrionuevo, G. Giant miniature EPSCs at the hippocampal mossy fiber to CA3 pyramidal cell synapse are monoquantal. J. Neurophysiol. 87, 15–29 (2002).
Salin, P. A., Scanziani, M., Malenka, R. C. & Nicoll, R. A. Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc. Natl. Acad. Sci. USA 93, 13304–13309 (1996).
Jackman, S. L., Turecek, J., Belinsky, J. E. & Regehr, W. G. The calcium sensor synaptotagmin 7 is required for synaptic facilitation. Nature 529, 88–91 (2016).
Griffith, W. H. Voltage-clamp analysis of posttetanic potentiation of the mossy fiber to CA3 synapse in hippocampus. J. Neurophysiol. 63, 491–501 (1990).
Toth, K., Suares, G., Lawrence, J. J., Philips-Tansey, E. & McBain, C. J. Differential mechanisms of transmission at three types of mossy fiber synapse. J. Neurosci. 20, 8279–8289 (2000).

Subcellular patch-clamp techniques for single-bouton stimulation and simultaneous pre- and postsynaptic recording at cortical synapses

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