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.
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Agmon, A., and Connors, B. W., 1991, Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro, Neuroscience 41:365–379.
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.
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.
Ataka, K., and Pieribone, V. A., 2002, A genetically targetable fluorescent probe of channel gating with rapid kinetics, Biophys. J. 82:509–516.
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.
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.
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.
Bruno, R. M., and Simons, D. J., 2002, Feedforward mechanisms of excitatory and inhibitory cortical receptive fields, J. Neurosci. 22:10966–10975.
Buzsaki, G., 2004, Large-scale recording of neuronal ensembles, Nat. Neurosci. 7:446–451.
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.
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.
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.
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.
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.
Grinvald, A., and Hildesheim, R., 2004, VSDI: a new era in functional imaging of cortical dynamics, Nat. Rev. Neurosci. 5:874–885.
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.
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.
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.
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.
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.
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.
Neher, E., 1992, Ion channels for communication between and within cells, Science 256:498–502.
Neher, E., and Sakmann, B., 1976, Single-channel currents recorded from membrane of denervated frog muscle fibres, Nature 260:799–802.
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.
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.
Petersen, C. C. H., 2002, Short-term plasticity within the excitatory neuronal network of layer 4 barrel cortex, J. Neurophysiol. 87:2904–2914.
Petersen, C. C. H., 2003, The barrel cortex—integrating molecular, cellular and systems physiology, Pflügers Arch. 447:126–134.
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.
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.
Petersen, C. C. H., and Sakmann, B., 2000, The excitatory neuronal network of layer 4 barrel cortex, J. Neurosci. 20:7579–7586.
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.
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.
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.
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.
Sakmann, B., 1992, Elementary steps in synaptic transmission revealed by currents through single ion channels, Science 256:503–512.
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.
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.
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.
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.
Siegel, M. S., and Isacoff, E. Y., 1997, A genetically encoded optical probe of membrane voltage, Neuron 19:735–741.
Simons, D. J., 1978, Response properties of vibrissa units in rat SI somatosensory neocortex, J. Neurophysiol. 41:798–820.
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.
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.
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.
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.
Zecevic, D., 1996, Multiple spike-initiation zones in single neurons revealed by voltage-sensitive dyes, Nature 381:322–325.
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.
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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
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DOI: https://doi.org/10.1007/0-387-28942-9_14
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