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In Vivo Dynamic-Clamp Manipulation of Extrinsic and Intrinsic Conductances: Functional Roles of Shunting Inhibition and I BK in Rat and Cat Cortex

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Dynamic-Clamp

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 1))

Abstract

We present in vivo dynamic-clamp electrophysiological recordings to characterize the influences of shunting inhibition and the potassium current I BK on the input–output (I/O) transfer function of cortical neurons, in response to both artificial (injected current or conductance) and functional visual stimuli. In comparison to previous experimental and theoretical studies, we find that realistic levels of shunting inhibition have a significant divisive effect on the firing gain. We also quantitatively characterize the effect of shunting inhibition on threshold and saturation. Shunting inhibition applied by dynamic-clamp also has a non-linear effect on visual responses, not only reducing the response but also significantly changing the timing of the response. We confirm predictions that I BK facilitates spike firing, despite this being a hyperpolarizing current. This effect is demonstrated by an increase in both the gain of the I/O transfer function, e.g. the f/I curve, and visual responses.

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References

  • Anderson J, Carandini M, Ferster D (2000) Orientation tuning of input conductance, excitation and inhibition in cat primary visual cortex. J Neurophysiol 84:909–26.

    PubMed  CAS  Google Scholar 

  • Anderson J, Lampl I, Gillespie D, Ferster D (2001) Membrane potential and conductance changes underlying length tuning of cells in cat primary visual cortex. J Neurosci 21:2104–12.

    PubMed  CAS  Google Scholar 

  • Bernander O, Douglas RJ, Martin KAC, Koch C (1991) Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc Natl Acad Sci USA 88:11569–73.

    Article  PubMed  CAS  Google Scholar 

  • Borg-Graham LJ (1987) Modelling the somatic electrical behaviour of hippocampal pyramidal neurons. MSEE Thesis, Massachusetts Institute of Technology.

    Google Scholar 

  • Borg-Graham L, Monier C, Frégnac Y (1998) Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 389:369–73.

    Google Scholar 

  • Borg-Graham LJ (1999) Interpretations of data and mechanisms for hippocampal pyramidal cell models. In Cerebral cortex, eds. Ulinski PS, Jones EG, & Peters A, pp. 19–138. Kluwer Academic/Plenum Publishers, New York.

    Chapter  Google Scholar 

  • Brizzi L, Meunier C, Zytnicki D, Donnet M, Hansel D, LaMotte D’Incamps B, Van Vreeswijk C (2004) How shunting inhibition affects the discharge of lumbar motoneurones. A dynamic clamp study in anaesthetised cats. J Physiol 558(Pt 2):671–83.

    Article  PubMed  CAS  Google Scholar 

  • Capaday C, Van Vreeswijk C (2006) Direct control of firing rate gain by dendritic shunting inhibition. J Integr Neurosci 5:199–222.

    Article  PubMed  Google Scholar 

  • Chance FS, Abbott LF, Reyes AD (2002) Gain modulation from background synaptic input. Neuron v35, 773–82.

    Article  Google Scholar 

  • Destexhe A, Paré D (1999) Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol 81:1531–47.

    PubMed  CAS  Google Scholar 

  • Fellous J-M, Rudolph M, Destexhe A, Sejnowski TJ (2003) Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity. Neuroscience 122:811–29.

    Article  PubMed  CAS  Google Scholar 

  • Graham L, Kado R (2002) The neuron’s biophysical mosaic and its computational relevance. In the Handbook for Brain Theory and Neural Networks, ed. Arbib M, 2nd edition, pp. 170–175. MIT Press.

    Google Scholar 

  • Graham LJ (2006) Not what you’d expect: Paradoxical roles of Na+ and K+ currents on excitability. Paper presented at the Modelling the Brain’s Labyrinth Meeting, Hieraklion, Greece.

    Google Scholar 

  • Graham LJ (2007) Not what you'd expect: Paradoxical roles of Na+ and K+ currents on excitability. Paper presented at the Quantitative Neuron Modeling Meeting, EPFL, Lausanne, Switzerland.

    Google Scholar 

  • Graham LJ, Schramm A, Gener T (2007) The modulation of firing gain and threshold by shunting inhibition in cortical neurons in vivo, Society for Neuroscience Annual Meeting Abstracts, San Diego, USA.

    Google Scholar 

  • Gu N, Vervaeke K, Storm JF (2007) BK potassium channels facilitate high-frequency firing and cause early spike frequency adaptation in rat CA1 hippocampal pyramidal cells. J Physiol 580(3):859–82.

    Article  PubMed  CAS  Google Scholar 

  • Haider B, Duque A, Hasenstaub A, McCormick D (2006) Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci 26:4535–45.

    Article  PubMed  CAS  Google Scholar 

  • Haider H, Duque A, Hasenstaub AR, Yu Y, McCormick DA (2007) Enhancement of visual responsiveness by spontaneous local network activity in vivo. J Neurophysiol 4186–202.

    Google Scholar 

  • Higley M, Contreras D (2006) Balanced excitation and inhibition determine spike timing during frequency adaptation. J Neurosci 26:448–57.

    Article  PubMed  CAS  Google Scholar 

  • Hirsch JA, Alonso JM, Reid RC, Martinez LM (1998) Synaptic integration in striate cortical simple cells. J Neurosci 18:9517–28.

    PubMed  CAS  Google Scholar 

  • Holt G.R, Koch C (1997) Shunting inhibition does not have a divisive effect on firing rates. Neural Comput 9:1001–13.

    Article  PubMed  CAS  Google Scholar 

  • Ingham NJ, McAlpine D (2005) GABAergic inhibition controls neural gain in inferior colliculus neurons sensitive to interaural time differences. J Neurosci 25(26):6187–98.

    Article  PubMed  CAS  Google Scholar 

  • Kullmann PHM, Wheeler DW, Beacom J, Horn JP (2004) Implementation of a fast 16-bit dynamic clamp using LabVIEW-RT. J Neurophysiol 91:542–54.

    Article  PubMed  Google Scholar 

  • Kreiner L, Jaeger D (2003) Synaptic shunting by a baseline of synaptic conductances modulates responses to inhibitory input volleys in cerebellar Purkinje cells. Cerebellum 3:112–25.

    Article  Google Scholar 

  • Manuel M, Meunier C, Donnet M, Zytnicki D (2005) How much afterhyperpolarization conductance is recruited by an action potential? A dynamic-clamp study in cat lumbar motoneurons. J Neurosci 25(39):8917–23.

    Article  PubMed  CAS  Google Scholar 

  • Marino J, Schummers J, Lyon D, Schwabe L, Beck O, Wiesing P, Obermayer K, Sur M (2005) Invariant computations in local cortical networks with balanced excitation and inhibition. Nat Neurosci 8:194–201.

    Article  PubMed  CAS  Google Scholar 

  • Marrion NV, Tavalin SJ (1998) Selective activation of Ca2+-activated K+ channels by co-localized Ca2+ channels in hippocampal neurons. Nature 395:900–5.

    Article  PubMed  CAS  Google Scholar 

  • McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny neurons of the neocortex. J Neurophysiol 54:782–806.

    PubMed  CAS  Google Scholar 

  • Mitchell SJ, Silver RA (2003) Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38:433–45.

    Article  PubMed  CAS  Google Scholar 

  • Monier C, Chavane F, Baudot P, Graham L, Frégnac Y (2003) Orientation and direction selectivity of excitatory and inhibitory inputs in visual cortical neurons: A diversity of combinations produces spike tuning. Neuron v37:663–80.

    Article  Google Scholar 

  • Prescott SA, De Koninck YD (2003) Gain control of firing rate by shunting inhibition: Roles of synaptic noise and dendritic saturation. Proc Natl Acad Sci USA 100(4):2076–81.

    Article  PubMed  CAS  Google Scholar 

  • Priebe N, Ferster D (2005) Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex. Neuron 45:133–45.

    Article  PubMed  CAS  Google Scholar 

  • Priebe N, Ferster D. (2006) Mechanisms underlying cross-orientation suppression in cat visual cortex. Nat Neurosci 9:552–61.

    Article  PubMed  CAS  Google Scholar 

  • Rapp M, Yarom Y, Segev I (1992) The impact of parallel fiber background activity on the cable properties of cerebellar Purkinje cells. Neural Comput 4:518–33.

    Article  Google Scholar 

  • Rudolph M, Destexhe A (2003) A fast-conducting, stochastic integrative mode for neocortical neurons in vivo. J Neurosci 23:2466–76.

    PubMed  CAS  Google Scholar 

  • Schramm A, Graham LJ (2007) Touch ’n Zap: A new technique for blind whole-cell patch recordings, 8e Colloque de la Société des Neurosciences, Montpellier, France.

    Google Scholar 

  • Semyanov A, Walker MC, Kullmann DM, Silver RA (2004) Tonically active GABA A receptors: modulating gain and maintaining the tone. Trends Neurosci 27(5): 262–9.

    Article  PubMed  CAS  Google Scholar 

  • Shao LR, Halvorsrud R, Borg-Graham L, Storm JF (1999) The role of BK-type Ca2+-dependent K+ channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. J Physiol v521.1:135–46.

    Article  Google Scholar 

  • Stell BM, Brickley SG, Tang CY, Farrant M, Mody I (2003) Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by {delta} subunit-containing GABAA receptors. PNAS 100(24):1443.

    Article  Google Scholar 

  • Storm J F (1990). Potassium currents in hippocampal pyramidal cells. Prog Brain Res 83:161–87.

    Article  PubMed  CAS  Google Scholar 

  • Storm J, Borg-Graham L, Adams P (1987) A passive component of the afterdepolarization (ADP) in rat hippocampal cells. Biophys J 51:65a.

    Google Scholar 

  • Straw AD, Warrant EJ, O’Carroll DC (2006) A 'bright zone' in male hoverfly (Eristalis tenax) eyes and associated faster motion detection and increased contrast sensitivity. J Exp Biol 209(21):4339–54.

    Article  PubMed  Google Scholar 

  • Tan AY, Zhang LI, Merzenich MM, Schreiner CE. (2004) Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. J Neurophysiol 92:630–43.

    Article  PubMed  Google Scholar 

  • Ulrich D (2003) Differential arithmetic of shunting inhibition for voltage and spike rate in neocortical pyramidal cells. Eur J Neurosci 18:2159–65.

    Article  PubMed  Google Scholar 

  • Velumian AA, Carlen PL (1999) Differential control of three after-hyperpolarizations in rat hippocampal neurones by intracellular calcium buffering. J Physiol 517:201–16.

    Google Scholar 

  • Vergara C, Latorre R, Marrion NV, Adelman JP (1998) Calcium-activated potassium channels. Curr Opin Neurobiol 8:321–9.

    Article  PubMed  CAS  Google Scholar 

  • Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442–6.

    Article  PubMed  CAS  Google Scholar 

  • Wehr MS, Zador A (2005) Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47:325–7.

    Article  Google Scholar 

  • Wilent W, Contreras D (2004) Synaptic responses to whisker deflections in rat barrel cortex as a function of cortical layer and stimulus intensity. J Neurosci 24:3985–98.

    Article  PubMed  CAS  Google Scholar 

  • Wilent W, Contreras D (2005) Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat Neurosci 8:1364–70.

    Article  PubMed  CAS  Google Scholar 

  • Zhang LI, Tan AY, Schreiner CE, Merzenich MM (2003) Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 424:201–5.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by an HFSP grant (RGP0049/2002) and an Agence Nationale de Recherche grant (FUNVISYNIN) to Dr. Lyle J. Graham. We also gratefully acknowledge Thomas Gener for his help in developing the protocols and participating in early experiments. We also acknowledge the important contribution of the authors of the VisionEgg and the G-Clamp software packages.

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Authors and Affiliations

  1. Neurophysiology of Visual Computation Laboratory, Laboratory of Neurophysics and Physiology, CNRS UMR 8119, Université Paris Descartes, 45 rue des Saint-Pères, 75006 Paris, France

    Lyle J. Graham

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  1. Lyle J. Graham
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  2. Adrien Schramm
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Correspondence to Lyle J. Graham .

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    Graham, L.J., Schramm, A. (2009). In Vivo Dynamic-Clamp Manipulation of Extrinsic and Intrinsic Conductances: Functional Roles of Shunting Inhibition and I BK in Rat and Cat Cortex. In: Bal, T., Destexhe, A. (eds) Dynamic-Clamp. Springer Series in Computational Neuroscience, vol 1. Springer, New York, NY. https://doi.org/10.1007/978-0-387-89279-5_7

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