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Long-Term Plasticity at the Mitral and Tufted Cell to Granule Cell Synapse of the Olfactory Bulb Investigated with a Custom Multielectrode in Acute Brain Slice Preparations

  • Michael Lukas
  • Knut Holthoff
  • Veronica EggerEmail author
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1820)

Abstract

Single extracellular stimulation electrodes are a widespread means to locally activate synaptic inputs in acute brain slices. Here we describe the fabrication and application of a multielectrode stimulator that was developed for conditions under which independent stimulation of several nearby sites is desirable. For the construction of the multielectrode we have developed a method by which electrode wires can be spaced at minimal distances of 100 μm. This configuration increases the efficiency of stimulation paradigms, such as the comparison of proximal induced and control inputs for studies of synaptic plasticity.

In our case the multielectrode was used for acute olfactory bulb slices to independently excite individual nearby glomeruli; the technique allowed us to demonstrate homosynaptic bidirectional long-term plasticity at the mitral/tufted cell to granule cell synapse. We also describe the determinants for successful recordings of long-term plasticity at this synapse, with mechanical and electrophysiological recording stability being tantamount. Finally, we briefly discuss data analysis procedures.

Key words

Long-term plasticity Multielectrode Olfactory bulb Glomerulus Homosynaptic 

Notes

Acknowledgments

The construction technique of the microelectrode was established in close collaboration with the mechanical workshop at Ludwig-Maximilians-Universität München (Robert Waberer). We thank Günes Birdal for the electrode photographs in Fig. 1a, b. This work was supported by DFG grants (EG135/2, EG135/4) to V.E., the Priority Program 1665 of the German Research Foundation (HO 2156/3-1/2 to KH), the Collaborative Research Center/Transregio 166 of the German Research Foundation (B3 to KH), and the Research Group FO 1738 (WI 830/10-2 to KH).

References

  1. 1.
    Golovin RM, Broadie K (2016) Developmental experience-dependent plasticity in the first synapse of the drosophila olfactory circuit. J Neurophysiol 116(6):2730–2738.  https://doi.org/10.1152/jn.00616.2016 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Kato HK, Chu MW, Isaacson JS, Komiyama T (2012) Dynamic sensory representations in the olfactory bulb: modulation by wakefulness and experience. Neuron 76(5):962–975.  https://doi.org/10.1016/j.neuron.2012.09.037 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Locatelli FF, Fernandez PC, Villareal F, Muezzinoglu K, Huerta R, Galizia CG, Smith BH (2013) Nonassociative plasticity alters competitive interactions among mixture components in early olfactory processing. Eur J Neurosci 37(1):63–79.  https://doi.org/10.1111/ejn.12021 CrossRefPubMedGoogle Scholar
  4. 4.
    Yamada Y, Bhaukaurally K, Madarász TJ, Pouget A, Rodriguez I, Carleton A (2017) Context- and output layer-dependent long-term ensemble plasticity in a sensory circuit. Neuron 93(5):1198–1212.e1195.  https://doi.org/10.1016/j.neuron.2017.02.006 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Abraham NM, Egger V, Shimshek DR, Renden R, Fukunaga I, Sprengel R, Seeburg PH, Klugmann M, Margrie TW, Schaefer AT, Kuner T (2010) Synaptic inhibition in the olfactory bulb accelerates odor discrimination in mice. Neuron 65(3):399–411.  https://doi.org/10.1016/j.neuron.2010.01.009 CrossRefPubMedGoogle Scholar
  6. 6.
    Abraham NM, Spors H, Carleton A, Margrie TW, Kuner T, Schaefer AT (2004) Maintaining accuracy at the expense of speed: stimulus similarity defines odor discrimination time in mice. Neuron 44(5):865–876.  https://doi.org/10.1016/j.neuron.2004.11.017 CrossRefPubMedGoogle Scholar
  7. 7.
    Nunes D, Kuner T (2015) Disinhibition of olfactory bulb granule cells accelerates odour discrimination in mice. Nat Commun 6:8950.  https://doi.org/10.1038/ncomms9950 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Alonso M, Lepousez G, Wagner S, Bardy C, Gabellec M-M, Torquet N, Lledo P-M (2012) Activation of adult-born neurons facilitates learning and memory. Nat Neurosci 15(6):897–904. doi:  https://doi.org/10.1038/nn.3108 CrossRefPubMedGoogle Scholar
  9. 9.
    Alonso M, Viollet C, Gabellec M-M, Meas-Yedid V, Olivo-Marin J-C, Lledo P-M (2006) Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J Neurosci 26(41):10508–10513.  https://doi.org/10.1523/jneurosci.2633-06.2006 CrossRefPubMedGoogle Scholar
  10. 10.
    Sailor KA, Valley MT, Wiechert MT, Riecke H, Sun GJ, Adams W, Dennis JC, Sharafi S, Ming G-L, Song H, Lledo P-M (2016) Persistent structural plasticity optimizes sensory information processing in the olfactory bulb. Neuron 91(2):384–396. doi:  https://doi.org/10.1016/j.neuron.2016.06.004CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Geramita M, Urban NN (2016) Postnatal odor exposure increases the strength of interglomerular lateral inhibition onto olfactory bulb tufted cells. J Neurosci 36(49):12321–12327.  https://doi.org/10.1523/JNEUROSCI.1991-16.2016 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Ma T-F, Zhao X-L, Cai L, Zhang N, Ren S-Q, Ji F, Tian T, Lu W (2012) Regulation of spike timing-dependent plasticity of olfactory inputs in mitral cells in the rat olfactory bulb. PLoS One 7(4):e35001.  https://doi.org/10.1371/journal.pone.0035001 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Chatterjee M, Perez de los Cobos Pallares F, Loebel A, Lukas M, Egger V (2016) Sniff-like patterned input results in long-term plasticity at the rat olfactory bulb mitral and tufted cell to granule cell synapse. Neural Plast 2016:16.  https://doi.org/10.1155/2016/9124986 CrossRefGoogle Scholar
  14. 14.
    Aihara T, Tsukada M, Crair MC, Shinomoto S (1997) Stimulus-dependent induction of long-term potentiation in CA1 area of the hippocampus: experiment and model. Hippocampus 7(4):416–426.  https://doi.org/10.1002/(SICI)1098-1063(1997)7:4<416::AID-HIPO7>3.0.CO;2-G CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Sun Y-G, Rupprecht V, Zhou L, Dasgupta R, Seibt F, Beierlein M (2016) MGluR1 and mGluR5 synergistically control cholinergic synaptic transmission in the thalamic reticular nucleus. J Neurosci 36(30):7886–7896.  https://doi.org/10.1523/jneurosci.0409-16.2016 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Zolnik TA, Sha F, Johenning FW, Schreiter ER, Looger LL, Larkum ME, Sachdev RNS (2017) All-optical functional synaptic connectivity mapping in acute brain slices using the calcium integrator campari. J Physiol 595(5):1465–1477.  https://doi.org/10.1113/JP273116 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Stroh O, Freichel M, Kretz O, Birnbaumer L, Hartmann J, Egger V (2012) NMDA receptor-dependent synaptic activation of TRPC channels in olfactory bulb granule cells. J Neurosci 32(17):5737–5746.  https://doi.org/10.1523/jneurosci.3753-11.2012 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Numberger M, Draguhn A (1996) Patch-Clamp-Technik. Spektrum Akad, HeidelbergGoogle Scholar
  19. 19.
    Wiegert JS, Gee CE, Oertner TG (2017) Stimulating neurons with heterologously expressed light-gated ion channels. Cold Spring Harb Protoc 2017(2):pdb.top089714.  https://doi.org/10.1101/pdb.top089714 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Burton SD, Urban NN (2015) Rapid feedforward inhibition and asynchronous excitation regulate granule cell activity in the mammalian main olfactory bulb. J Neurosci 35(42):14103–14122.  https://doi.org/10.1523/jneurosci.0746-15.2015 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Dhawale AK, Hagiwara A, Bhalla US, Murthy VN, Albeanu DF (2010) Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse. Nat Neurosci 13(11):1404–1412. http://www.nature.com/neuro/journal/v13/n11/abs/nn.2673.html CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Li A, Gire DH, Bozza T, Restrepo D (2014) Precise detection of direct glomerular input duration by the olfactory bulb. J Neurosci 34(48):16058–16064.  https://doi.org/10.1523/jneurosci.3382-14.2014 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Larson J, Munkácsy E (2015) Theta-burst LTP. Brain Res 1621:38–50.  https://doi.org/10.1016/j.brainres.2014.10.034 CrossRefPubMedGoogle Scholar
  24. 24.
    Kay LM, Beshel J, Brea J, Martin C, Rojas-Líbano D, Kopell N (2009) Olfactory oscillations: the what, how and what for. Trends Neurosci 32(4):207–214.  https://doi.org/10.1016/j.tins.2008.11.008 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Egger V, Svoboda K, Mainen ZF (2005) Dendrodendritic synaptic signals in olfactory bulb granule cells: local spine boost and global low-threshold spike. J Neurosci 25(14):3521–3530.  https://doi.org/10.1523/JNEUROSCI.4746-04.2005 CrossRefPubMedGoogle Scholar
  26. 26.
    Micheva KD, Smith SJ (2005) Strong effects of subphysiological temperature on the function and plasticity of mammalian presynaptic terminals. J Neurosci 25(33):7481–7488.  https://doi.org/10.1523/jneurosci.1801-05.2005 CrossRefPubMedGoogle Scholar
  27. 27.
    Young C, Luo M-Z, Shen Y-Z, Gean P-W (2001) Dissociation between synaptic depression and block of long-term depression induced by raising the temperature in rat hippocampal slices. Synapse 40(1):27–34.  https://doi.org/10.1002/1098-2396(200104)40:1<27::AID-SYN1023>3.0.CO;2-3 CrossRefPubMedGoogle Scholar
  28. 28.
    Bywalez Wolfgang G, Patirniche D, Rupprecht V, Stemmler M, Herz Andreas VM, Pálfi D, Rózsa B, Egger V (2015) Local postsynaptic voltage-gated sodium channel activation in dendritic spines of olfactory bulb granule cells. Neuron 85(3):590–601.  https://doi.org/10.1016/j.neuron.2014.12.051 CrossRefPubMedGoogle Scholar
  29. 29.
    Egger V, Stroh O (2009) Calcium buffering in rodent olfactory bulb granule cells and mitral cells. J Physiol 587(18):4467–4479.  https://doi.org/10.1113/jphysiol.2009.174540 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Zoology and Regensburg Center of NeuroscienceRegensburg UniversityRegensburgGermany
  2. 2.Hans-Berger Department of NeurologyUniversity Hospital JenaJenaGermany

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