Skip to main content

Advances in Understanding Cortical Function Through Combined Voltage-Sensitive Dye Imaging, Whole-Cell Recordings, and Analysis of Cellular Morphology

  • Chapter
Neuroanatomical Tract-Tracing 3

Abstract

Voltage-sensitive dyes can be used to image cortical network function with millisecond temporal resolution and with a horizontal spatial resolution of approximately 50 µm. This imaging technique can be combined with whole-cell patch-clamp measurement of membrane potential followed by the anatomical analysis of neuronal morphology. Together, such experiments reveal the relationship of activity recorded in individual identified neurons with the spatiotemporally resolved ensemble dynamics of a cortical region. Application of these techniques to the rodent barrel cortex has advanced our understanding of the synaptic mechanisms underlying sensory responses to simple whisker stimuli.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Agmon, A., and Connors, B. W., 1991, Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro, Neuroscience 41:365–379.

    Article  PubMed  CAS  Google Scholar 

  • Antic, S., Major, G., and Zecevic, D., 1999, Fast optical recordings of membrane potential changes from dendrites of pyramidal neurons, J. Neurophys. 82:1615–1621.

    CAS  Google Scholar 

  • Armstrong-James, M., Fox, K., and Das-Gupta, A., 1992, Flow of excitation within rat barrel cortex on striking a single vibrissa, J. Neurophysiol. 68:1345–1358.

    PubMed  CAS  Google Scholar 

  • Ataka, K., and Pieribone, V. A., 2002, A genetically targetable fluorescent probe of channel gating with rapid kinetics, Biophys. J. 82:509–516.

    Article  PubMed  CAS  Google Scholar 

  • Blanton, M. G., Lo Turco, J. J., and Kriegstein, A. R., 1989, Whole-cell recording from neurons in slices of reptilian and mammalian cerebral cortex, J. Neurosci. Methods 30:203–210.

    Article  PubMed  CAS  Google Scholar 

  • Brecht, M., Roth, A., and Sakmann, B., 2003, Dynamic receptive fields of reconstructed pyramidal cells in layers 3 and 2 of rat somatosensory barrel cortex, J. Physiol. 553:243–265.

    Article  PubMed  CAS  Google Scholar 

  • Brecht, M., and Sakmann, B., 2002, Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex, J. Physiol. 543:49–70.

    Article  PubMed  CAS  Google Scholar 

  • Bruno, R. M., and Simons, D. J., 2002, Feedforward mechanisms of excitatory and inhibitory cortical receptive fields, J. Neurosci. 22:10966–10975.

    PubMed  CAS  Google Scholar 

  • Buzsaki, G., 2004, Large-scale recording of neuronal ensembles, Nat. Neurosci. 7:446–451.

    Article  PubMed  CAS  Google Scholar 

  • Cacciatore, T. W., Brodfuehrer, P. D., Gonzalez, J. E., Jiang, T., Adams, S. R., Tsien, R. Y., Kristan, W. B., and Kleinfeld, D., 1999, Identification of neural circuits by imaging coherent electrical activity with FRET-based dyes, Neuron 23:449–459.

    Article  PubMed  CAS  Google Scholar 

  • Djurisic, M., Antic, S., Chen, W. R., and Zecevic, D., 2004, Voltage imaging from dendrites of mitral cells: EPSP attenuation and spike trigger zones, J. Neurosci. 24:6703–6714.

    Article  PubMed  CAS  Google Scholar 

  • Feldmeyer, D., Egger, V., Lubke, J., and Sakmann, B., 1999, Reliable synaptic connections between pairs of excitatory layer 4 neurons within a single “barrel” of developing rat somatosensory cortex, J. Physiol. 521:169–190.

    Article  PubMed  CAS  Google Scholar 

  • Feldmeyer, D., Silver, R. A., Lübke, J., and Sakmann, B., 2002, Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signaling within a cortical column, J. Physiol. 538: 803–822.

    Article  PubMed  CAS  Google Scholar 

  • Grinvald, A., Anglister, L., Freeman, J. A., Hildesheim, R., and Manker, A., 1984, Real-time optical imaging of naturally evoked electrical activity in intact frog brain, Nature 308:848–850.

    Article  PubMed  CAS  Google Scholar 

  • Grinvald, A., and Hildesheim, R., 2004, VSDI: a new era in functional imaging of cortical dynamics, Nat. Rev. Neurosci. 5:874–885.

    Article  PubMed  CAS  Google Scholar 

  • Gupta, A., Wang, Y., and Markram, H., 2000, Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex, Science 287:273–278.

    Article  PubMed  CAS  Google Scholar 

  • Hamill, O. P., Marty, A., Neheri, E., Sakmann, B., and Sigworth, F. J., 1981, Improved patchclamp techniques for high-resolution current recording from cells and cell-free membrane patches, Pflügers Arch. 391:85–100.

    Article  PubMed  CAS  Google Scholar 

  • Kuhn, B., Fromherz, P., and Denk, W., 2004, High sensitivity of stark-shift voltage-sensing dyes by one-or two-photon excitation near the red spectral edge, Biophys. J. 87:631–639.

    Article  PubMed  CAS  Google Scholar 

  • Lübke, J., Egger, V., Sakmann, B., and Feldmeyer, D., 2000, Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex, J. Neurosci. 20:5300–5311.

    PubMed  Google Scholar 

  • Margrie, T.W., Meyer, A. H., Caputi, A., Monyer, H., Hasan, M. T., Schaefer, A. T., Denk, W., and Brecht, M., 2003, Targeted whole-cell recordings in the mammalian brain in vivo, Neuron 39:911–918.

    Article  PubMed  CAS  Google Scholar 

  • Moore, C. I., and Nelson, S. B., 1998, Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex, J. Neurophysiol. 80: 2882–2892.

    PubMed  CAS  Google Scholar 

  • Neher, E., 1992, Ion channels for communication between and within cells, Science 256:498–502.

    Article  PubMed  CAS  Google Scholar 

  • Neher, E., and Sakmann, B., 1976, Single-channel currents recorded from membrane of denervated frog muscle fibres, Nature 260:799–802.

    Article  PubMed  CAS  Google Scholar 

  • Nicolelis, M. A., Dimitrov, D., Carmena, J. M., Crist, R., Lehew, G., Kralik, J. D., and Wise S. P., 2003, Chronic, multisite, multielectrode recordings in macaque monkeys, Proc. Natl. Acad. Sci. U.S.A. 100:11041–11046.

    Article  PubMed  CAS  Google Scholar 

  • Peterlin, Z. A., Kozloski, J., Mao, B. Q., Tsiola, A., and Yuste, R., 2000, Optical probing of neuronal circuits with calcium indicators, Proc. Natl. Acad. Sci. U.S.A. 97:3619–3624.

    Article  PubMed  CAS  Google Scholar 

  • Petersen, C. C. H., 2002, Short-term plasticity within the excitatory neuronal network of layer 4 barrel cortex, J. Neurophysiol. 87:2904–2914.

    PubMed  Google Scholar 

  • Petersen, C. C. H., 2003, The barrel cortex—integrating molecular, cellular and systems physiology, Pflügers Arch. 447:126–134.

    Article  PubMed  CAS  Google Scholar 

  • Petersen, C. C. H., Grinvald, A., and Sakmann, B., 2003a, Spatiotemporal dynamics of sensory responses in layer 2/3 of rat barrel cortex measured in vivo by voltage-sensitive dye imaging combined with whole-cell voltage recordings and anatomical reconstructions, J. Neurosci. 23:1298–1309.

    PubMed  CAS  Google Scholar 

  • Petersen, C. C. H., Hahn, T. T. G., Mehta, M., Grinvald, A., and Sakmann, B., 2003b, Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex, Proc. Natl. Acad. Sci. U.S.A. 100:13638–13643.

    Article  PubMed  CAS  Google Scholar 

  • Petersen, C. C. H., and Sakmann, B., 2000, The excitatory neuronal network of layer 4 barrel cortex, J. Neurosci. 20:7579–7586.

    PubMed  CAS  Google Scholar 

  • Petersen, C. C. H., and Sakmann, B., 2001, Functionally independent columns of rat somatosensory barrel cortex revealed with voltage-sensitive dye imaging, J. Neurosci. 21: 8435–8446.

    PubMed  CAS  Google Scholar 

  • Porter, J. T., Johnson, C. K., and Agmon, A., 2001, Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex, J. Neurosci. 21:2699–2710.

    PubMed  CAS  Google Scholar 

  • Reyes, A., and Sakmann, B., 1999, Developmental switch in the short-term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex, J. Neurosci. 19:3827–3835.

    PubMed  CAS  Google Scholar 

  • Sakai, R., Repunte-Canonigo, V., Raj, C. D., and Knopfel, T., 2001, Design and characterization of a DNA-encoded, voltage-sensitive fluorescent protein, Eur. J. Neurosci. 13:2314–2318.

    Article  PubMed  CAS  Google Scholar 

  • Sakmann, B., 1992, Elementary steps in synaptic transmission revealed by currents through single ion channels, Science 256:503–512.

    Article  PubMed  CAS  Google Scholar 

  • Salzberg, B. M., Davila, H.V., and Cohen, L. B., 1973, Optical recording of impulses in individual neurons of an invertebrate central nervous system, Nature 246:508–509.

    Article  PubMed  CAS  Google Scholar 

  • Schubert, D., Kotter, R., Zilles, K., Luhmann, H. J., and Staiger, J. F., 2003, Cell type-specific circuits of cortical layer 4 spiny neurons, J. Neurosci. 23:2961–2970.

    PubMed  CAS  Google Scholar 

  • Shepherd, G. M., Pologruto, T. A., and Svoboda, K., 2003, Circuit analysis of experiencedependent plasticity in the developing rat barrel cortex, Neuron 38:277–289.

    Article  PubMed  CAS  Google Scholar 

  • Shoham, D., Glaser, D. E., Arieli, A., Kenet, T., Wijnbergen, C., Toledo, Y., Hildesheim, R., and Grinvald, A., 1999, Imaging cortical dynamics at high spatial and temporal resolution with novel blue voltage-sensitive dyes, Neuron 24:791–802.

    Article  PubMed  CAS  Google Scholar 

  • Siegel, M. S., and Isacoff, E. Y., 1997, A genetically encoded optical probe of membrane voltage, Neuron 19:735–741.

    Article  PubMed  CAS  Google Scholar 

  • Simons, D. J., 1978, Response properties of vibrissa units in rat SI somatosensory neocortex, J. Neurophysiol. 41:798–820.

    PubMed  CAS  Google Scholar 

  • Stosiek, C., Garaschuk, O., Holthoff, K., and Konnerth, A., 2003, In vivo two-photon calcium imaging of neuronal networks, Proc. Natl. Acad. Sci. U.S.A. 100:7319–7324.

    Article  PubMed  CAS  Google Scholar 

  • Stuart, G. J., Dodt, H. U., and Sakmann, B., 1993, Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy, Pflügers Arch. 423:511–518.

    Article  PubMed  CAS  Google Scholar 

  • Tasaki, I., Watanabe, A., Sandlin, R., and Carnay, L., 1968, Changes in fluorescence, turbidity and birefringence associated with nerve excitation, Proc. Natl. Acad. Sci. U.S.A. 61:883–888.

    Article  PubMed  CAS  Google Scholar 

  • Woolsey, T. A., and Van der Loos, H., 1970, The structural organization of layer 4 in the somatosensory region (SI) of the mouse cerebral cortex: the description of a cortical field composed of discrete cytoarchitectonic units, Brain Res. 17:205–242.

    Article  PubMed  CAS  Google Scholar 

  • Zecevic, D., 1996, Multiple spike-initiation zones in single neurons revealed by voltage-sensitive dyes, Nature 381:322–325.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, J. J., and Connors, B. W., 1999, Intrinsic firing patterns and whiskers-evoked synaptic responses of neurons in the rat barrel cortex, J. Neurophysiol. 81:1171–1183.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer Science+Business Media, Inc.

About this chapter

Cite this chapter

Petersen, C.C.H. (2006). Advances in Understanding Cortical Function Through Combined Voltage-Sensitive Dye Imaging, Whole-Cell Recordings, and Analysis of Cellular Morphology. In: Zaborszky, L., Wouterlood, F.G., Lanciego, J.L. (eds) Neuroanatomical Tract-Tracing 3. Springer, Boston, MA . https://doi.org/10.1007/0-387-28942-9_14

Download citation

Publish with us

Policies and ethics