Subcellular Patch-clamp Recordings from the Somatodendritic Domain of Nigral Dopamine Neurons.

[en] Dendrites of dopaminergic neurons receive and convey synaptic input, support action potential back-propagation and neurotransmitter release. Understanding these fundamental functions will shed light on the information transfer in these neurons. Dendritic patch-clamp recordings provide the possibility to directly examine the electrical properties of dendrites and underlying voltage-gated ion channels. However, these fine structures are not easily accessible to patch pipettes because of their small diameter. This report describes a step-by-step procedure to collect stable and reliable recordings from the dendrites of dopaminergic neurons in acute slices. Electrophysiological measurements are combined with post hoc recovery of cell morphology. Successful experiments rely on improved preparation of slices, solutions and pipettes, adequate adjustment of the optics and stability of the pipette in contact with the recorded structure. Standard principles of somatic patch-clamp recording are applied to dendrites but with a gentler approach of the pipette. These versatile techniques can be implemented to address various questions concerning the excitable properties of dendrites.

Research Center/Unit :

Laboratory of Neurophysiology, GIGA-Neurosciences

Disciplines :

Life sciences: Multidisciplinary, general & others

Author, co-author :

Engel, Dominique ; Université de Liège > Département des sciences biomédicales et précliniques > Pharmacologie

Language :

English

Title :

Subcellular Patch-clamp Recordings from the Somatodendritic Domain of Nigral Dopamine Neurons.

Publication date :

02 November 2016

Journal title :

Journal of Visualized Experiments

eISSN :

1940-087X

Publisher :

MYJoVE Corporation, Boston, United States - Massachusetts

Volume :

117

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique

Funding text :

This work was supported by grants from the Belgian F.R.S. - FNRS (U.N002.13 and T.N0015.13) and published with the support of the Belgian University Foundation (Publié avec le concours de la Fondation Universitaire de Belgique).

Available on ORBi :

since 31 May 2017

Statistics

Number of views

66 (3 by ULiège)

Number of downloads

125 (2 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

London, M., & Häusser, M. Dendritic computation. Annu Rev Neurosci. 28, 503-532 (2005).
Stuart, G. J., & Spruston, N. Dendritic integration: 60 years of progress. Nat Neurosci. 18 (12), 1713-1721 (2015).
Sakmann, B., & Neher, E. Patch clamp techniques for studying ionic channels in excitable membranes. Annu Rev of Physiol. 46, 455-472 (1984).
Dodt, H. U., & Zieglgänsberger, W. Infrared videomicroscopy: a new look at neuronal structure and function. Trends Neurosci. 17 (11), 453-8 (1994).
Geiger, J., et al. Patch-clamp recording in brain slices with improved slicer technology. Pflug Arch. 443 (3), 491-501 (2002).
Nevian, T., Larkum, M. E., Polsky, A., & Schiller, J. Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study. Nat Neurosci. 10 (2), 206-214 (2007).
Delvendahl, I., Straub, I., & Hallermann, S. Dendritic patch-clamp recordings from cerebellar granule cells demonstrate electrotonic compactness. Front Cell Neurosci. 9, 93 (2015).
Stuart, G., & Spruston, N. Probing dendritic function with patch pipettes. Curr Opin Neurobiol. 5 (3), 389-394 (1995).
Stuart, G. J., & Sakmann, B. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature. 367 (6458), 69-72 (1994).
Magee, J. C. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci. 18 (19), 7613-7624 (1998).
Berger, T., Larkum, M. E., & Lüscher, H. R. High I(h) channel density in the distal apical dendrite of layer V pyramidal cells increases bidirectional attenuation of EPSPs. J Neurophysiol. 85 (2), 855-868 (2001).
Hoffman, D. a, Magee, J. C., Colbert, C. M., & Johnston, D. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature. 387 (6636), 869-875 (1997).
Engel, D., & Seutin, V. High dendritic expression of Ih in the proximity of the axon origin controls the integrative properties of nigral dopamine neurons. J Physiol. 593 (22), 4905-4922 (2015).
Hu, H., Martina, M., & Jonas, P. Dendritic mechanisms underlying rapid synaptic activation of fast-spiking hippocampal interneurons. Science. 327 (5961), 52-58 (2010).
Bischofberger, J., & Jonas, P. Action potential propagation into the presynaptic dendrites of rat mitral cells. J Physiol. 504 (2), 359-365 (1997).
Angelo, K., London, M., Christensen, S. R., & Hausser, M. Local and global effects of I(h) distribution in dendrites of mammalian neurons. J Neurosci. 27 (32), 8643-8653 (2007).
Stuart, G., Spruston, N., & Häusser, M. Dendrites. Oxford University Press: Oxford; New York, (2008).
Williams, S. R., & Stuart, G. J. Site independence of EPSP time course is mediated by dendritic I(h) in neocortical pyramidal neurons. J Neurophysiol. 83 (5), 3177-3182 (2000).
Williams, S. R., & Stuart, G. J. Action potential backpropagation and somato-dendritic distribution of ion channels in thalamocortical neurons. J Neurosci. 20 (4), 1307-1317 (2000).
Gasparini, S., & Magee, J. C. Phosphorylation-dependent differences in the activation properties of distal and proximal dendritic Na+ channels in rat CA1 hippocampal neurons. J Physiol. 541 (Pt 3), 665-672 (2002).
Martina, M., Vida, I., & Jonas, P. Distal initiation and active propagation of action potentials in interneuron dendrites. Science. 287 (5451), 295-300 (2000).
Kim, S., Guzman, S. J., Hu, H., & Jonas, P. Active dendrites support efficient initiation of dendritic spikes in hippocampal CA3 pyramidal neurons. Nature Neurosci. 15 (4), 600-606 (2012).
Lorincz, A., Notomi, T., Tamas, G., Shigemoto, R., & Nusser, Z. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci. 5 (11), 1185-1193 (2002).
Nusser, Z. Differential subcellular distribution of ion channels and the diversity of neuronal function. Curr Opin Neurobiol. 22 (3), 366-371 (2012).
Häusser, M., Stuart, G., Racca, C., & Sakmann, B. Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Neuron. 15 (3), 637-647 (1995).
Gentet, L. J., & Williams, S. R. Dopamine gates action potential backpropagation in midbrain dopaminergic neurons. J Neurosci. 27 (8), 1892-1901 (2007).
Stuart, G., Spruston, N., Sakmann, B., & Häusser, M. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 20 (3), 125-131 (1997).
Roth, A., & Häusser, M. Compartmental models of rat cerebellar Purkinje cells based on simultaneous somatic and dendritic patch-clamp recordings. J Physiol. 535 (Pt 2), 445-72 (2001).
Schmidt-Hieber, C., Jonas, P., & Bischofberger, J. Subthreshold dendritic signal processing and coincidence detection in dentate gyrus granule cells. J Neurosci. 27 (31), 8430-8441 (2007).
Nörenberg, A., Hu, H., Vida, I., Bartos, M., & Jonas, P. Distinct nonuniform cable properties optimize rapid and efficient activation of fast-spiking GABAergic interneurons. Proc Natl Acad Sci U S A. 107 (2), 894-9 (2010).
Pouille, F., & Scanziani, M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science. 293 (5532), 1159-1163 (2001).
Hornykiewicz, O. The discovery of dopamine deficiency in the parkinsonian brain. J Neural Transm. (70), 9-15 (2006).
Tepper, J. M., Sawyer, S. F., & Groves, P. M. Electrophysiologically identified nigral dopaminergic neurons intracellularly labeled with HRP: light-microscopic analysis. J Neurosci. 7 (9), 2794-806 (1987).
Cajal, S. R. Histologie du Système Nerveux de l'Homme et des Vertébrés. Tome premier.'Maloine Editeur. Paris Azoulay, L: Paris, (1909).
Cheramy, A., Leviel, V., & Glowinski, J. Dendritic release of dopamine in the substantia nigra. Nature. 289 (0028-0836 (Print)), 537-542 (1981).
Grace, A. A., & Bunney, B. S. The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci. 4 (11), 2877-2890 (1984).
Harnett, M. T., Bernier, B. E., Ahn, K.-C., & Morikawa, H. Burst-timing-dependent plasticity of NMDA receptor-mediated transmission in midbrain dopamine neurons. Neuron. 62 (6), 826-38 (2009).
Bischofberger, J., Engel, D., Li, L., Geiger, J. R., & Jonas, P. Patch-clamp recording from mossy fiber terminals in hippocampal slices. Nat Protoc. 1 (4), 2075-2081 (2006).
Sakmann, B., & Neher, E. Single-channel recording. Springer US: New York, (1995).
Davie, J. T., Kole, M. H. P., et al. Dendritic patch-clamp recording. Nat Protoc. 1 (3), 1235-1247 (2006).
Weng, J.-Y., Lin, Y.-C., & Lien, C.-C. Cell type-specific expression of acid-sensing ion channels in hippocampal interneurons. J Neurosci. 30 (19), 6548-6558 (2010).
Kole, M. H., Hallermann, S., & Stuart, G. J. Single Ih channels in pyramidal neuron dendrites: properties, distribution, and impact on action potential output. J Neurosci. 26 (6), 1677-1687 (2006).
Angelo, K., & Margrie, T. W. Population diversity and function of hyperpolarization-activated current in olfactory bulb mitral cells. Sci Rep. 1, 50 (2011).
Brown, A. L., Johnson, B. E., & Goodman, M. B. Making patch-pipettes and sharp electrodes with a programmable puller. J Vis Exp. (20), 1-2 (2008).
Gibb, A. J., & Edwards, F. a Patch clamp recording from cells in sliced tissues. Microelectrode techniques, The Plymouth workshop handbook. 255-274 (1994).
Edwards, F. A., & Konnerth, A. Patch-clamping cells in sliced tissue preparations. Method Enzymol. 207 (1980), 208-222 (1992).
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. Pflug Arch Eur J Phy. 423 (5-6), 511-518 (1993).
Castañeda-Castellanos, D. R., Flint, A. C., & Kriegstein, A. R. Blind patch clamp recordings in embryonic and adult mammalian brain slices. Nat Protoc. 1 (2), 532-542 (2006).
Dodt, H.-U., Becker, K., & Zieglgänsberger, W. Infrared video microscopy for visualizing neurons and neuronal excitation in brain slices. Cold Spring Harb Protoc. 2013 (12), 1149-52 (2013).
Dodt, H. U., & Zieglgansberger, W. Visualizing unstained neurons in living brain slices by infrared DIC-videomicroscopy. Brain Res. 537 (1-2), 333-336 (1990).
Stuart, G. Patch-pipet recording in brain slices. Curr Protoc Neurosci. Chapter 6, Unit 6.7 (2001).
Dodt, H. U., Frick, A., Kampe, K., & Zieglgänsberger, W. NMDA and AMPA receptors on neocortical neurons are differentially distributed. Eur J Neurosci. 10 (11), 3351-7 (1998).
Dodt, H.-U., Eder, M., Schierloh, A., & Zieglgänsberger, W. Infrared-guided laser stimulation of neurons in brain slices. Sci STKE. 2002 (120), pl2 (2002).
Warner Istruments, C. Techniques for Chloriding Silver Wires. (1999).
Stuart, G., & Sakmann, B. Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron. 15 (5), 1065-1076 (1995).
van Welie, I., van Hooft, J.A. & Wadman, W. J. Homeostatic scaling of neuronal excitability by synaptic modulation of somatic hyperpolarization-activated Ih channels. Proc Natl Acad Sci U S A. 101 (14), 5123-5128 (2004).
Berger, T., Larkum, M. E., & Luscher, H. R. High I(h) channel density in the distal apical dendrite of layer V pyramidal cells increases bidirectional attenuation of EPSPs. J Neurophysiol. 85 (2), 855-868 (2001).
Marx, M., Günter, R. H., Hucko, W., Radnikow, G., & Feldmeyer, D. Improved biocytin labeling and neuronal 3D reconstruction. Nat Protoc. 7 (2), 394-407 (2012).
Booker, S. A., Song, J., & Vida, I. Whole-cell Patch-clamp Recordings from Morphologically- and Neurochemically-identified Hippocampal Interneurons. J Vis Exp. (91), 1-11 (2014).
Schindelin, J., Arganda-Carreras, I., et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 9 (7), 676-682 (2012).
Myatt, D. R., Hadlington, T., Ascoli, G., & Nasuto, S. Neuromantic - from semi manual to semi automatic reconstruction of neuron morphology. Front Neuroinform. 6, 4 (2012).
Guzman, S. J., Schlögl, A., & Schmidt-Hieber, C. Stimfit: quantifying electrophysiological data with Python. Front Neuroinform. 8 (February), 1-10 (2014).
Schlögl, A., Jonas, P., Schmidt-Hieber, C., & Guzman, S. J. Stimfit: A Fast Visualization and Analysis Environment for Cellular Neurophysiology. BME/Biomed Tech (Berl). 58, 24-25 (2013).
Shu, Y., Hasenstaub, A., Duque, A., Yu, Y., & McCormick, D. A. Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential. Nature. 441 (7094), 761-765 (2006).
Masi, A., et al. Differential contribution of Ih to the integration of excitatory synaptic inputs in substantia nigra pars compacta and ventral tegmental area dopaminergic neurons. Eur J Neurosci. 42 (9), 2699-2706 (2015).
Franz, O., Liss, B., Neu, A., & Roeper, J. Single-cell mRNA expression of HCN1 correlates with a fast gating phenotype of hyperpolarization-activated cyclic nucleotide-gated ion channels (Ih) in central neurons. Eur J Neurosci. 12 (8), 2685-2693 (2000).
Thome, C., et al. Axon-carrying dendrites convey privileged synaptic input in hippocampal neurons. Neuron. 83 (6), 1418-1430 (2014).
Kuba, H., Ishii, T. M., & Ohmori, H. Axonal site of spike initiation enhances auditory coincidence detection. Nature. 444 (7122), 1069-1072 (2006).
Dugladze, T., Schmitz, D., Whittington, M. a., Vida, I., & Gloveli, T. Segregation of Axonal and Somatic Activity During Fast Network Oscillations. Science. 336 (6087), 1458-1461 (2012).
Zhang, L., et al. Whole-cell recording of the Ca(2+)-dependent slow afterhyperpolarization in hippocampal neurones: effects of internally applied anions. Pflug Arch Eur J Phy. 426 (3-4), 247-53 (1994).
Kaczorowski, C. C., Disterhoft, J., & Spruston, N. Stability and plasticity of intrinsic membrane properties in hippocampal CA1 pyramidal neurons: effects of internal anions. J Physiol. 578 (Pt 3), 799-818 (2007).
Velumian, A. A., Zhang, L., Pennefather, P., & Carlen, P. L. Reversible inhibition of IK, IAHP, Ih and ICa currents by internally applied gluconate in rat hippocampal pyramidal neurones. Pflug Arch Eur J Phy. 433 (3), 343-50 (1997).
Azene, E. M., Xue, T., & Li, R. a Molecular basis of the effect of potassium on heterologously expressed pacemaker (HCN) channels. J Physiol. 547 (Pt 2), 349-356 (2003).
Káradóttir, R., & Attwell, D. Combining patch-clamping of cells in brain slices with immunocytochemical labeling to define cell type and developmental stage. Nat Protoc. 1 (4), 1977-86 (2006).
Nair-Roberts, R. G., Chatelain-Badie, S. D., Benson, E., White-Cooper, H., Bolam, J. P., & Ungless, M. A. Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat. Neuroscience. 152 (4), 1024-1031 (2008).
Yasuda, R., et al. Imaging calcium concentration dynamics in small neuronal compartments. Sci STKE. 2004 (219), pl5 (2004).
Hsu, T.-T., Lee, C.-T., Tai, M.-H., & Lien, C.-C. Differential Recruitment of Dentate Gyrus Interneuron Types by Commissural Versus Perforant Pathways. Cereb cortex., 1-13 (2015).
Lin, J. Y., van Wyk, M., Bowala, T. K., Teo, M.-Y., & Lipski, J. Dendritic projections and dye-coupling in dopaminergic neurons of the substantia nigra examined in horizontal brain slices from young rats. J Neurophysiol. 90 (4), 2531-2535 (2003).
Henny, P., et al. Structural correlates of heterogeneous in vivo activity of midbrain dopaminergic neurons. Nat Neurosci. 15 (4), 613-619 (2012).
van Pelt, J., van Ooyen, A., & Uylings, H. B. M. Axonal and dendritic density field estimation from incomplete single-slice neuronal reconstructions. Front Neuroanat. 8 (June), 54 (2014).
Popovic, M., et al. Imaging submillisecond membrane potential changes from individual regions of single axons, dendrites and spines. Adv Exp Med Biol. 859, 57-101 (2015).
Sjostrom, P. J., Rancz, E. a, Roth, A., & Häusser, M. Dendritic Excitability and Synaptic Plasticity. Physiol Rev. 88 (2), 769-840 (2008).
Magee, J. C., & Johnston, D. Plasticity of dendritic function. Curr Opin Neurobiol. 15 (3), 334-342 (2005).