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Initiation of Sodium Spikelets in Basal Dendrites of Neocortical Pyramidal Neurons

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Abstract

Cortical information processing relies critically on the processing of electrical signals in pyramidal neurons. Electrical transients mainly arise when excitatory synaptic inputs impinge upon distal dendritic regions. To study the dendritic aspect of synaptic integration one must record electrical signals in distal dendrites. Since thin dendritic branches, such as oblique and basal dendrites, do not support routine glass electrode measurements, we turned our effort towards voltage-sensitive dye recordings. Using the optical imaging approach we found and reported previously that basal dendrites of neocortical pyramidal neurons show an elaborate repertoire of electrical signals, including backpropagating action potentials and glutamate-evoked plateau potentials. Here we report a novel form of electrical signal, qualitatively and quantitatively different from backpropagating action potentials and dendritic plateau potentials. Strong glutamatergic stimulation of an individual basal dendrite is capable of triggering a fast spike, which precedes the dendritic plateau potential. The amplitude of the fast initial spikelet was actually smaller that the amplitude of the backpropagating action potential in the same dendritic segment. Therefore, the fast initial spike was dubbed “spikelet”. Both the basal spikelet and plateau potential propagate decrementally towards the cell body, where they are reflected in the somatic whole-cell recordings. The low incidence of basal spikelets in the somatic intracellular recordings and the impact of basal spikelets on soma-axon action potential initiation are discussed.

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References

  • Antic S.D. 2003. Action potentials in basal and oblique dendrites of rat neocortical pyramidal neurons. J. Physiol. 550:35–50

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Antic S., Wuskell J.P., Loew L., Zecevic D. 2000. Functional profile of the giant metacerebral neuron of Helix aspersa: temporal and spatial dynamics of electrical activity in situ. J. Physiol. 1:55–69

    Article  Google Scholar 

  • Antic S., Zecevic D. 1995. Optical signals from neurons with internally applied voltage-sensitive dyes. J. Neurosci. 15:1392–405

    CAS  PubMed  Google Scholar 

  • Antic S.D., Radojicic M.S., Milojkovic B.A., Goldman-Rakic, P.S. 2003. Ionic basis of glutamate evoked spikes in basal dendrites of pyramidal neurons in prefrontal cortex. Soc. Neurosci. Abstr.:476.10

  • Archie K.A., Mel B.W. 2000. A model for intradendritic computation of binocular disparity. Nat. Neurosci. 3:54–63

    Article  CAS  PubMed  Google Scholar 

  • Ariav G., Polsky A., Schiller J. 2003. Submillisecond precision of the input-output transformation function mediated by fast sodium dendritic spikes in basal dendrites of CA1 pyramidal neurons. J. Neurosci 23:7750–7758

    CAS  PubMed  Google Scholar 

  • Bekkers J.M. 2000. Distribution and activation of voltage-gated potassium channels in cell-attached and outside-out patches from large layer 5 cortical pyramidal neurons of the rat. J. Physiol. 3:611–620

    Article  Google Scholar 

  • Chen W.R., Midtgaard J., Shepherd G.M. 1997. Forward and backward propagation of dendritic impulses and their synaptic control in mitral cells. Science 278:463–467

    Article  CAS  PubMed  Google Scholar 

  • Clements J.D. 1996. Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci. 19:163–71

    Article  CAS  PubMed  Google Scholar 

  • Davila H.V., Cohen L.B., Salzberg B.M., Shrivastav B.B. 1974. Changes in ANS and TNS fluorescence in giant axons from Loligo. J. Membrane. Biol. 15:29–46

    Article  CAS  Google Scholar 

  • deCharms R.C., Zador A. 2000. Neural representation and the cortical code. Annu. Rev. Neurosci. 23:613–647

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Elston G.N. 2003. Cortex, cognition and the cell: New insights into the pyramidal neuron and prefrontal function. Cereb. Cortex. 13:1124–1138

    Article  PubMed  Google Scholar 

  • Feldmeyer D., Lubke J., Silver R.A., 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 signalling within a cortical column. J. Physiol. 538:803–822

    Article  CAS  PubMed  Google Scholar 

  • Frick A., Magee J., Koester H.J., Migliore M., Johnston D. 2003. Normalization of Ca2+ signals by small oblique dendrites of CA1 pyramidal neurons. J. Neuro sci 23:3243–3250

    Google Scholar 

  • Golding N.L., Spruston N. 1998. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CAl pyramidal neurons. Neuron 21:1189–1200

    Article  CAS  PubMed  Google Scholar 

  • Golding N.L., Staff N.P., Spruston N. 2002. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418:326–331

    Article  CAS  PubMed  Google Scholar 

  • Goldstein S.S., Rail W. 1974. Changes of action potential shape and velocity for changing core conductor geometry. Biophys. J. 14:731–757

    CAS  PubMed  Google Scholar 

  • Grinvald A., Salzberg B.M., Lev-Ram V., Hildesheim R. 1987. Optical recording of synaptic potentials from processes of single neurons using intracellular potentiometric dyes. Biophys. J. 51:643–651

    Article  CAS  PubMed  Google Scholar 

  • Gulledge A.T., Kampa B.M., Stuart G.J. 2005. Synaptic integration in dendritic trees. J. Neurobiol. 64:75–90

    Article  CAS  PubMed  Google Scholar 

  • Hassner, A., Birnbaum, D., L.M. 1984. Chargeshift probes of membrane potential. Synthesis. J. Org. Chem. 49:2546–2551

  • Hausser M., Major G., Stuart G.J. 2001. Differential shunting of EPSPs by action potentials. Science 291:138–141

    Article  CAS  PubMed  Google Scholar 

  • Hausser M., Spruston N., Stuart G.J. 2000. Diversity and dynamics of dendritic signaling. Science 290:739–744

    Article  CAS  PubMed  Google Scholar 

  • Hossain W.A., Antic S.D., Yang Y., Rasband M.N., Merest O.K. 2005. Where is the spike generator of the cochlear nerve? Voltage-gated sodium channels in the mouse cochlea. J. Neurosci. 25:6857–6866

    Article  CAS  PubMed  Google Scholar 

  • Konig P., Engel A.K., Singer W. 1996. Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci. 19:130–137

    Article  CAS  PubMed  Google Scholar 

  • Larkman A.U. 1991. Dendritic morphology of pyramidal neurones of the visual cortex of the rat: III. Spine distributions. J. Comp. Neurol. 306:332–343

    Article  CAS  PubMed  Google Scholar 

  • Larkum M.E., Launey T., Dityatev A., Luscher H.R. 1998. Integration of excitatory postsynaptic potentials in dendrites of motoneurons of rat spinal cord slice cultures. J. Neurophysiol. 80:924–935

    CAS  PubMed  Google Scholar 

  • Larkum M.E., Zhu J.J., Sakmann B. 2001. Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons. J. Physiol. 533:447–466

    Article  CAS  PubMed  Google Scholar 

  • Lewis B.L., O’Donnell P. 2000. Ventral tegmental area afferents to the prefrontal cortex maintain membrane potential ‘up’ states in pyramidal neurons via D(l) dopamine receptors. Cereb. Cortex 10:1168–1175

    Article  CAS  PubMed  Google Scholar 

  • Loew L.M., Cohen L.B., Dix J., Fluhler E.N., Montana V., Salama G., Wu J.Y. 1992. A naphthyl analog of the aminostyryl pyridinium class of potentiometric membrane dyes shows consistent sensitivity in a variety of tissue, cell, and model membrane preparations. J. Membrane. Biol. 130:1–10

    Article  CAS  Google Scholar 

  • London M., Hausser M. 2005. Dendritic computation. Annu. Rev. Neurosci. 28:503–532

    Article  CAS  PubMed  Google Scholar 

  • Mackenzie P.J., Murphy T.H. 1998. High safety factor for action potential conduction along axons but not dendrites of cultured hippocampal and cortical neurons. J. Neurophysiol. 80:2089–2101

    CAS  PubMed  Google Scholar 

  • Magee J.C. 2000. Dendritic integration of excitatory synaptic input. Nat. Rev. Neurosci. 1:181–190

    Article  CAS  PubMed  Google Scholar 

  • Magee J.C., Johnston D. 1995. Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. J. Physiol. 487:67–90

    CAS  PubMed  Google Scholar 

  • Migliore M., Shepherd G.M. 2002. Emerging rules for the distributions of active dendritic conductances. Nat. Rev. Neurosci. 3:362–370

    Article  CAS  PubMed  Google Scholar 

  • Milojkovic B.A., Radojicic M.S., Antic S.D. 2005. A strict correlation between dendritic and somatic plateau depolarizations in the rat prefrontal cortex pyramidal neurons. J. Neurosci. 25:3940–3951

    Article  CAS  PubMed  Google Scholar 

  • Milojkovic B.A., Radojicic M.S., Goldman-Rakic P.S., Antic S.D. 2004. Burst generation in rat pyramidal neurones by regenerative potentials elicited in a restricted part of the basilar dendritic tree. J. Physiol. 558:193–211

    Article  CAS  PubMed  Google Scholar 

  • Nunez A., Amzica F., Steriade M. 1993. Electrophysiology of cat association cortical cells in vivo: intrinsic properties and synaptic responses. J. Neurophysiol. 70:418–430

    CAS  PubMed  Google Scholar 

  • Oakley J.C., Schwindt P.C., Grill W.E. 2001a. Dendritic calcium spikes in layer 5 pyramidal neurons amplify and limit transmission of ligand-gated dendritic current to soma. J. Neurophysiol. 86:514–527

    CAS  Google Scholar 

  • Oakley J.C., Schwindt P.C., Grill W.E. 2001b. Initiation and propagation of regenerative Ca2+ dependent potentials in dendrites of layer 5 pyramidal neurons. J. Neurophysiol. 86:503–513

    CAS  Google Scholar 

  • Parnas I., Hochstein S., Parnas H. 1976. Theoretical analysis of parameters leading to frequency modulation along an inhomogeneous axon. J. Neurophysiol. 39:909–923

    CAS  PubMed  Google Scholar 

  • Poirazi P., Brannon T., Mel B.W. 2003. Pyramidal neuron as two-layer neural network. Neuron 37:989–999

    Article  CAS  PubMed  Google Scholar 

  • Poznanski R.R. 2002. Dendritic integration in a recurrent network. J. Integr. Neurosci. 1:69–99

    Article  PubMed  Google Scholar 

  • Ramon F., Joyner R.W., Moore J.W. 1975. Propagation of action potentials in inhomogeneous axon regions. Fed. Proc. 34:1357–1363

    CAS  PubMed  Google Scholar 

  • Rapp M., Yarom Y., Segev I. 1996. Modeling back propagating action potential in weakly excitable dendrites of neocortical pyramidal cells. Proc. Natl. Acad. Sci. USA 93:11985–11990

    Article  CAS  PubMed  Google Scholar 

  • Regehr W.G., Tank D.W. 1990. Postsynaptic NMDA receptor-mediated calcium accumulation in hippocampal CA1 pyramidal cell dendrites. Nature 345:807–810

    Article  CAS  PubMed  Google Scholar 

  • Salzberg B.M., Grinvald A., Cohen L.B., Davila H.V., Ross W.N. 1977. Optical recording of neuronal activity in an invertebrate central nervous system: simultaneous monitoring of several neurons. J. Neurophysiol. 40:1281–1291

    CAS  PubMed  Google Scholar 

  • Schiller J., Major G., Koester H.J., Schiller Y. 2000. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404:285–289

    Article  CAS  PubMed  Google Scholar 

  • Schmitz D., Schuchmann S., Fisahn A., Draguhn A., Buhl E.H., Petrasch-Parwez E., Dermietzel R., Heinemann U., Traub R.D. 2001. Axo-axonal coupling, a novel mechanism for ultrafast neuronal communication. Neuron 31: 831–840

    Article  CAS  PubMed  Google Scholar 

  • Shepherd G.M. 2004. The synaptic organization of the brain. Oxford Univ. Press, New York

    Google Scholar 

  • Shipp S., Zeki S. 2002. The functional organization of area V2, I: specialization across stripes and layers. Vis. Neurosci. 19:187–210

    Article  PubMed  Google Scholar 

  • Softky W. 1994. Sub-millisecond coincidence detection in active dendritic trees. Neuroscience 58:13–41

    Article  CAS  PubMed  Google Scholar 

  • Spruston N., Schiller Y., Stuart G., Sakmann B. 1995. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268:297–300

    CAS  PubMed  Google Scholar 

  • Steriade M., Nunez A., Amzica F. 1993a. Intracellular analysis of relations between the slow (< 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J. Neurosci. 13:3266–3283

    CAS  Google Scholar 

  • Steriade M., Nunez A., Amzica F. 1993b. A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 13:3252–3265

    CAS  Google Scholar 

  • Stuart G., Schiller J., Sakmann B. 1997. Action potential initiation and propagation in rat neocortical pyramidal neurons. J. Physiol. 505:617–632

    Article  CAS  PubMed  Google Scholar 

  • Stuart G., Spruston N. 1998. Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J. Neurosci. 18:3501–3510

    CAS  PubMed  Google Scholar 

  • Stuart G., Sakmann B. 1994. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367:69–72

    Article  CAS  PubMed  Google Scholar 

  • Tauc L. 1962. Site of origin and propagation in spike in the giant neuron of Aplysia. J. Gen. Physiol. 45:1077–1097

    Article  CAS  PubMed  Google Scholar 

  • Thomson A.M., Deuchars L, West D.C. 1993. Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self- facilitation, mediated postsynaptically. J. Neurophysiol. 70:2354–2369

    CAS  PubMed  Google Scholar 

  • Timofeev I., Grenier F., Bazhenov M., Sejnowski T.J., Steriade M. 2000. Origin of slow cortical oscillations in deafferented cortical slabs. Cereb. Cortex 10:1185–1199

    Article  CAS  PubMed  Google Scholar 

  • Trettel J., Fortin D.A., Levine E.S. 2004. Endocannabinoid signalling selectively targets perisomatic inhibitory inputs to pyramidal neurones in juvenile mouse neocortex. J.Physiol. 556:95–107

    Article  CAS  PubMed  Google Scholar 

  • Trimmer J.S., Rhodes K.J. 2004. Localization of voltage-gated ion channels in mammalian brain. Annu. Rev. Physiol. 66:477–519

    Article  CAS  PubMed  Google Scholar 

  • Tsodyks M.V., Markram H. 1997. The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc. Natl. Acad. Sci. USA 94:719–723

    Article  CAS  PubMed  Google Scholar 

  • Vetter P., Roth A., Hausser M. 2001. Propagation of action potentials in dendrites depends on dendritic morphology. J. Neurophysiol. 85:926–937

    CAS  PubMed  Google Scholar 

  • Waters J., Helmchen F. 2004. Boosting of action potential backpropagation by neocortical network activity in vivo. J. Neurosci. 24:11127–11136

    Article  CAS  PubMed  Google Scholar 

  • Wei D.S., Mei Y.A., Bagal A., Kao J.P., Thompson S.M., Tang C.M. 2001. Compartmentalized and binary behavior of terminal dendrites in hippocampal pyramidal neurons. Science 293:2272–2275

    Article  CAS  PubMed  Google Scholar 

  • Zilberter Y. 2000. Dendritic release of glutamate suppresses synaptic inhibition of pyramidal neurons in rat neocortex. J. Physiol. 528:489–496

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

S.A. is grateful to Guy Major for helpful discussions. This work was supported by NIH grants EB001963 and MH063503.

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Authors and Affiliations

  1. Department of Neuroscience, Erasmus MC Dr. Molewaterplein 50, 3015 GE, Rotterdam, Netherlands

    B.A. Milojkovic

  2. Department of Cell Biology, UConn Health Center, 263 Farmington Ave., CT, 06030, USA

    J.P. Wuskell & L.M. Loew

  3. Department of Neuroscience, L-4000, UConn Health Center, 263 Farmington Ave., Farmington, CT, 06030-3401, USA

    S.D. Antic

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  1. B.A. Milojkovic
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  2. J.P. Wuskell
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  3. L.M. Loew
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Correspondence to S.D. Antic.

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Milojkovic, B., Wuskell, J., Loew, L. et al. Initiation of Sodium Spikelets in Basal Dendrites of Neocortical Pyramidal Neurons. J Membrane Biol 208, 155–169 (2005). https://doi.org/10.1007/s00232-005-0827-7

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