Talk:Dynamic clamp

From Scholarpedia
Jump to: navigation, search

    All candidates would do an excellent job of writing on the subject. Dr. Sharp may present an interesting historical account of the development of the procedure.

    It looks like Boston and Atlanta are the only two places where this research is active!

    No! There are lots of additional places: Bordeaux, Marseille, San Diego, New York, Chicago, etc etc.


    Reviewer B:

    This is a nice overview of the dynamic-clamp technique. I have several remarks about points that need improvement.

    The first remark is that the paper should give a more detailed historical description of the dynamic-clamp. Below I quote references that should be mentioned, based on the introduction chapter by Piwkowska et al. in the "Dynamic-clamp" book edited by Destexhe & Bal (Springer, 2009). An early form of the dynamic-clamp technique, called the "Ersatz Nexus", has been described in cardiac physiology as early as 1979, in a PhD thesis studying the impact of electrical synapses (gap junctions) on the synchronization of clusters of cardiomyocytes in the chicken (Scott 1979). Note that I have myself a copy of this thesis and I do confirm that this is the very first published report of a technique which is essentially the same as the dynamic-clamp. Later studies of cardiac tissue re-introduced a technique named "coupling clamp" (Tan and Joyner 1990) for bi-directionally connecting two isolated myocytes by a virtual gap junction of chosen conductance. The injected current flowing through the virtual gap junction is calculated according to a driving force determined in real time and equal to the difference of membrane potential between the two cells (see Verheijck et al. 1998 for an example of application exploring the synchronization between two spontaneously active rabbit cardiac cells). An extension of this technique, named the model clamp by the authors, consists in coupling, through such a virtual gap junction, a real myocyte and a model myocyte simulated in real time (Wilders et al., 1996).

    In neuroscience, the dynamic-clamp technique in its general form, with the general purpose of inserting into the membrane of a neuron any conductance the experimentalist might be interested in, has been introduced independently by Hugh Robinson (Robinson and Kawai 1993) and by a team led by Eve Marder and Larry Abbott, based on a collaboration with Gwendal Le Masson (Le Masson et al. 1992; Sharp et al. 1993; see also Le Masson, Le Masson and Moulins 1995). From the onset, based on the same principle of injecting a V$_m$-dependent current into a neuron, different implementations and applications were explored by the different groups: using digital systems, Robinson and Kawai injected synaptic inputs into cultured hippocampal neurons of the vertebrate CNS, while Sharp and colleagues studied various conductances and artificial networks in the stomato-gastric ganglion (STG) of decapod crustaceans (lobsters and crabs) nervous system. Le Masson and colleagues (Le Masson, Le Masson and Moulins 1995) developed an analog and a digital approach simultaneously for studies of the invertebrate preparation (and subsequently combined both approaches in a single study of mammalian thalamus networks, see Le Masson et al. 2002). Since this time, dynamic-clamp has been widely used in both vertebrate and invertebrate preparations.

    The review should give more credit to Gwen Le Masson from Bordeaux - he was first author on the SFN abstract on dynamic-clamp in 1992 by the Marder-Abbott group, and I believe this is the very first publication of the technique in neuroscience. He was also first author of a Nature paper in 2000 based on the dynamic-clamp technique, which is certainly worth mentioning in the review.

    Another remark is that the list of available systems should describe the "RT-Neuron", which enables running dynamic-clamp experiments from the Neuron simulator. This system is described in a chapter by Sadoc et al. in the 2009 dynamic-clamp book. Mike Hines (the author of Neuron) plans to include the RT module in the public distribution of Neuron, as an option. At the moment, this program runs only on the Windows operating system (Microsoft corp.), while the real-time is either given by a DSP acquisition board, or using commercial software to run real-time applications under Windows (see details in the Sadoc et al. chapter, and in particular in its appendix). A preliminary version of the RT-Neuron system was also described in a SFN abstract by LeFranc et al. This system was also developed by Gwen LeMasson.

    Finally, the part on injection of "synaptic noise" in neurons missed a lot of references. A large number of studies studied this paradigm in different brain regions and using different methods. The conductance waveforms were generated either by the convolution of pre-synaptic spike trains with unitary synaptic conductances (Reyes et al., 1996; Jaeger and Bower 1999; Harsch and Robinson 2000; Gauck and Jaeger 2000; Chance et al., 2002; Suter and Jaeger 2004; de Polavieja et al. 2005; Zsiros and Hestrin, 2005; Dorval and White 2006; Tateno and Robinson 2006; Morita et al., 2008), or by effective stochastic models of synaptic bombardment or synaptic noise, without explicit representation of the pre-synaptic spike trains (Destexhe et al. 2001; Shu et al. 2003; McCormick et al. 2003; Fellous et al. 2003a, Fellous et al. 2003b; Wolfart et al. 2005; Hasenstaub et al. 2005; Shu et al. 2006; Desai and Walcott 2006; Piwkowska et al. 2008). The latter method's main advantage is to allow independent control of the mean and variance of conductances, which cannot be done using convoluted spike trains.

    The review should mention these aspects

    For references, I copy below the reference list of Piwkowska et al. 2009:

    • Aradi I, Santhakumar V, Soltesz I (2004) Impact of heterogeneous perisomatic IPSC populations on pyramidal cell firing rates. J Neurophysiol 91:2849-2858.
    • Arsiero M, Luescher HR, Giugliano M (2005) The mean-field dynamic-clamp: linking single- neuron properties to network activity in in vitro preparations. In: Society for Neuroscience Meeting. 823.1.
    • Bedard C, Destexhe A (2008) A modified cable formalism for modeling neuronal membranes at high frequencies. Biophys J 94:1133-1143.
    • Ben-Ari Y (2002) Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3:728-739.
    • Berecki G, Zegers JG, Verkerk AO, Bhuiyan ZA, de Jonge B, Veldkamp MW, Wilders R, van Ginneken ACG (2005) HERG channel (dys)function revealed by dynamic action potential clamp technique. Biophys J 88:566578.
    • Bettencourt JC, Lillis KP, Stupin LR, White JA (2008) Effects of imperfect dynamic clamp: Computational and experimental results. J Neurosci Methods 169:282-289.
    • Brette R, Piwkowska Z, Monier C, Rudolph-Lilith M, Fournier J, Levy M, Fregnac Y, Bal T, Destexhe A (2008) High-resolution intracellular recordings using a real-time computational model of the electrode. Neuron 59:379-391.
    • Brizzi L, Meunier C, Zytnicki D, Donnet M, Hansel D, LaMotte D'Incamps B, Van Vreeswikj C (2004) How shunting inhibition affects the discharge of lumbar motoneurones. A dynamic clamp study in anaesthetised cats. J Physiol 558:671-83.
    • Chance FS, Abbott LF, Reyes AD (2002) Gain modulation from background synaptic input. Neuron 35:773-782.
    • Cohen I, Navarro V, Clemenceau S, Baulac M, Miles R (2002) On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298:1418-1421.
    • de Polavieja GG, Harsch A, Kleppe I, Robinson HP, Juusola M (2005) Stimulus history reliably shapes action potential waveforms of cortical neurons. J Neurosci 25:5657-5665.
    • Derjean D, Bertrand S, Le Masson G, Landry M, Morisset V, Nagy F (2003) Dynamic balance of metabotropic inputs causes dorsal horn neurons to switch functional states. Nat Neurosci 6:274-281.
    • Desai NS, Walcott EC (2006) Synaptic bombardment modulates muscarinic effects in forelimb motor cortex. J Neurosci 26:2215-2226.
    • Destexhe A, Pare D (1999) Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol 81:1531-1547.
    • Destexhe A, Rudolph M, Fellous JM, Sejnowski TJ (2001) Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons. Neuroscience 107:13-24.
    • Dorval AD, Christini DJ, White JA (2001) Real-Time linux dynamic clamp: a fast and flexible way to construct virtual ion channels in living cells. Ann Biomed Eng 29:897-907.
    • Dorval AD, Jr., White JA (2005) Channel noise is essential for perithreshold oscillations in entorhinal stellate neurons. J Neurosci 25:10025-10028.
    • Dorval AD, White JA (2006) Synaptic input statistics tune the variability and reproducibility of neuronal responses. Chaos 16:026105.
    • Fellous JM, 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 122:811-829.
    • Fellous JM, Sejnowski TJ (2003) Regulation of persistent activity by background inhibition in an in vitro model of a cortical microcircuit. Cereb Cortex 13:1232-1241.
    • Fernandez FR, White JA (2008) Artificial synaptic conductances reduce subthreshold oscillations and periodic firing in stellate cells of the entorhinal cortex. J Neurosci 28:3790-3803.
    • Foldy C, Aradi I, Howard A, Soltesz I (2004) Diversity beyond variance: modulation of firing rates and network coherence by GABAergic subpopulations. Eur J Neurosci 19:119-130.
    • Gauck V, Jaeger D (2000) The control of rate and timing of spikes in the deep cerebellar nuclei by inhibition. J Neurosci 20:3006-3016.
    • Gauck V, Jaeger D (2003) The contribution of NMDA and AMPA conductances to the control of spiking in neurons of the deep cerebellar nuclei. J Neurosci 23:8109-8118.
    • Goaillard JM, Marder E (2006) Dynamic clamp analyses of cardiac, endocrine, and neural function. Physiology (Bethesda) 21:197-207.
    • Goldman MS, Golowasch J, Marder E, Abbott LF (2001) Global structure, robustness, and modulation of neuronal models. J Neurosci 21:5229-5238.
    • Gulledge AT, Stuart GJ (2003) Excitatory actions of GABA in the cortex. Neuron 37:299-309.
    • Haider B, Duque A, Hasenstaub AR, Yu Y, McCormick DA (2007) Enhancement of visual responsiveness by spontaneous local network activity in vivo. J Neurophysiol 97:4186-4202.
    • Hanson JE, Jaeger D (2002) Short-term plasticity shapes the response to simulated normal and parkinsonian input patterns in the globus pallidus. J Neurosci 22:5164-5172.
    • Harsch A, Robinson HP (2000) Postsynaptic variability of firing in rat cortical neurons: the roles of input synchronization and synaptic NMDA receptor conductance. J Neurosci 20:6181-6192.
    • Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209.
    • Hughes SW, Cope DW, Crunelli V (1998) Dynamic clamp study of Ih modulation of burst firing and delta oscillations in thalamocortical neurons in vitro. Neuroscience 87:541-550.
    • Hughes SW, Cope DW, Toth TI, Williams SR, Crunelli V (1999) All thalamocortical
    • neurones possess a T-type Ca2+ 'window' current that enables the expression of bistability-mediated activities. J Physiol 517:805-815.
    • Hughes SW, Lorincz M, Cope DW, Crunelli V (2008) NeuReal: An interactive simulation system for implementing artificial dendrites and large hybrid networks. J Neurosci Methods 169:290-301.
    • Jaeger D, Bower JM (1999) Synaptic control of spiking in cerebellar Purkinje cells: dynamic current clamp based on model conductances. J Neurosci 19:6090-6101.
    • Kreiner L, Jaeger D (2004) Synaptic shunting by a baseline of synaptic conductances modulates responses to inhibitory input volleys in cerebellar Purkinje cells. Cerebellum 3:112-125.
    • Le Franc Y, Foutry B, Nagy F, Le Masson G (2001) Nociceptive signal transfer through the dorsal horn network: hybrid and dynamic clamp approaches using a real-time implementation of the Neuron simulation environment. In: Society for Neuroscience Meeting. 927.18
    • Le Masson G, Renaud-Le Masson S, Sharp AA, Marder E, Abbott LF (1992) Real-time interaction between a model neuron and the crustacean stomatogastric nervous system In: Society for Neuroscience Meeting. 18, 1055.
    • Le Masson G, Le Masson S, Moulins M (1995) From conductances to neural network properties: analysis of simple circuits using the hybrid network method. Prog Biophys Molec Biol 64:201-220.
    • Le Masson S, Laflaquiere A, Bal T, Le Masson G (1999) Analog circuits for modeling biological neural networks: design and applications. IEEE Trans Biomed Eng 46:638-645.
    • Le Masson G, Renaud-Le Masson S, Debay D, Bal T (2002) Feedback inhibition controls spike transfer in hybrid thalamic circuits. Nature 417:854-858.
    • Lien CC, Jonas P (2003) Kv3 potassium conductance is necessary and kinetically optimized
    • for high-frequency action potential generation in hippocampal interneurons. J Neurosci 23:2058-2068.
    • Manor Y, Nadim F (2001) Synaptic depression mediates bistability in neuronal networks with recurrent inhibitory connectivity. J Neurosci 21:9460-9470.
    • 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 25:8917-8923.
    • Manuel M, Meunier C, Donnet M, Zytnicki D (2006) The afterhyperpolarization conductance exerts the same control over the gain and variability of motoneurone firing in anaesthetized cats. J Physiol 576:873-886.
    • Manuel M, Meunier C, Donnet M, Zytnicki D (2007) Resonant or not, two amplification modes of proprioceptive inputs by persistent inward currents in spinal motoneurons. J Neurosci 27:12977-12988.
    • McCarren M, Alger BE (1985) Use-dependent depression of IPSPs in rat hippocampal pyramidal cells in vitro. J Neurophysiol 53:557-571.
    • Milescu LS, Yamanishi T, Ptak K, Mogri MZ, Smith JC (2008) Real-time kinetic modeling of voltage-gated ion channels using dynamic clamp. Biophys J 95:66-87.
    • Mitchell SJ, Silver RA (2003) Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38:433-445.
    • Morita K, Kalra R, Aihara K, Robinson HP (2008) Recurrent synaptic input and the timing of gamma-frequency-modulated firing of pyramidal cells during neocortical "UP" states. J Neurosci 28:1871-1881.
    • Netoff TI, Banks MI, Dorval AD, Acker CD, Haas JS, Kopell N, White JA (2005) Synchronization in hybrid neuronal networks of the hippocampal formation. J Neurophysiol 93:1197-1208.
    • Nowotny T, Zhigulin VP, Selverston AI, Abarbanel HD, Rabinovich MI (2003) Enhancement of synchronization in a hybrid neural circuit by spike-timing dependent plasticity. J Neurosci 23:9776-9785.
    • Oprisan SA, Prinz AA, Canavier CC (2004) Phase resetting and phase locking in hybrid circuits of one model and one biological neuron. Biophys J 87:2283-2298.
    • Piwkowska Z, Pospischil M, Brette R, Sliwa J, Rudolph-Lilith M, Bal T, Destexhe A (2008)
    • Characterizing synaptic conductance fluctuations in cortical neurons and their influence on spike generation. J Neurosci Methods 169:302-322.
    • Pospischil M, Piwkowska Z, Rudolph M, Bal T, Destexhe A (2007) Calculating event-triggered average synaptic conductances from the membrane potential. J Neurophysiol 97:2544-2552.
    • Prescott SA, De Koninck Y (2003) Gain control of firing rate by shunting inhibition: roles of synaptic noise and dendritic saturation. Proc Natl Acad Sci U S A 100:2076-2081.
    • Prescott SA, Ratté S, De Koninck Y, Sejnowski TJ (2006) Nonlinear interaction between shunting and adaptation controls a switch between integration and coincidence detection in pyramidal neurons. J Neurosci 26: 9084-9097.
    • Prinz AA, Thirumalai V, Marder E (2003) The functional consequences of changes in the strength and duration of synaptic inputs to oscillatory neurons. J Neurosci 23:943-954.
    • Prinz AA, Abbott LF, Marder E (2004) The dynamic clamp comes of age. Trends Neurosci 27:218-224.
    • Prinz AA (2004) Neural networks: models and neurons show hybrid vigor in real time. Curr Biol 14:R661-662.
    • Reyes AD, Rubel EW, Spain WJ (1996) In vitro analysis of optimal stimuli for phase-locking and time-delayed modulation of firing in avian nucleus laminaris neurons. J Neurosci 16:993-1007.
    • Reyes AD (2003) Synchrony-dependent propagation of firing rate in iteratively constructed networks in vitro. Nat Neurosci 6:593-599.
    • Robinson HP, Kawai N (1993) Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons. J Neurosci Methods 49:157-165.
    • Robinson HP (2008) A scriptable DSP-based system for dynamic conductance injection. J Neurosci Methods 169:271-281.
    • Rudolph M, Piwkowska Z, Badoual M, Bal T, Destexhe A (2004) A method to estimate synaptic conductances from membrane potential fluctuations. J Neurophysiol 91:2884-2896.
    • Schreiber S, Fellous JM, Tiesinga P, Sejnowski TJ (2004) Influence of ionic conductances on spike timing reliability of cortical neurons for suprathreshold rhythmic inputs. J Neurophysiol 91:194-205.
    • Scott S (1979) Stimulation Simulations of Young Yet Cultured Beating Hearts. In. Buffalo, NY: State University of New York.
    • Sharp AA, O'Neil MB, Abbott LF, Marder E (1993) Dynamic clamp: computer-generated conductances in real neurons. J Neurophysiol 69:992-995.
    • Shu Y, Hasenstaub A, Badoual M, Bal T, McCormick DA (2003) Barrages of synaptic activity control the gain and sensitivity of cortical neurons. J Neurosci 23:10388-10401.
    • Siegelbaum SA, Koester J (2000) Ion channels. In: Principles of neural science, 4th Edition (Kandel ER, Schwartz JH, Jessell TM, eds). New York, NY: McGraw-Hill.
    • Sohal VS, Huguenard JR (2005) Inhibitory coupling specifically generates emergent gamma oscillations in diverse cell types. Proc Natl Acad Sci U S A 102:18638-18643.
    • Sorensen M, DeWeerth S, Cymbalyuk G, Calabrese RL (2004) Using a hybrid neural system to reveal regulation of neuronal network activity by an intrinsic current. J Neurosci 24:5427-5438.
    • Stein V, Nicoll RA (2003) GABA generates excitement. Neuron 37:375-378.
    • Suter KJ, Jaeger D (2004) Reliable control of spike rate and spike timing by rapid input transients in cerebellar stellate cells. Neuroscience 124:305-317.
    • Swensen AM, Marder E (2001) Modulators with convergent cellular actions elicit distinct circuit outputs. J Neurosci 21:4050-4058.
    • Tan RC, Joyner RW (1990) Electrotonic influences on action potentials from isolated ventricular cells. Circ Res 67:1071-1081.
    • Tateno T, Robinson HP (2006) Rate coding and spike-time variability in cortical neurons with two types of threshold dynamics. J Neurophysiol 95:2650-2663.
    • Thompson SM, Gahwiler BH (1989) Activity-dependent disinhibition. I. Repetitive stimulation reduces IPSP driving force and conductance in the hippocampus in vitro. J Neurophysiol 61:501-511.
    • Thompson SM, Gahwiler BH (1989) Activity-dependent disinhibition. II. Effects of extracellular potassium, furosemide, and membrane potential on ECl- in hippocampal CA3 neurons. J Neurophysiol 61:512-523.
    • Tyzio R, Cossart R, Khalilov I, Minlebaev M, Hubner CA, Represa A, Ben-Ari Y, Khazipov R (2006) Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314:1788-1792.
    • Ulrich D, Huguenard JR (1996) Gamma-aminobutyric acid type B receptor-dependent burst-firing in thalamic neurons: a dynamic clamp study. Proc Natl Acad Sci U S A 93:13245-13249.
    • Ulrich D, Huguenard JR (1997) GABA(A)-receptor-mediated rebound burst firing and burst shunting in thalamus. J Neurophysiol 78:1748-1751.
    • Verheijck EE, Wilders R, Joyner RW, Golod DA, Kumar R, Jongsma HJ, Bouman LN, van Ginneken AC (1998) Pacemaker synchronization of electrically coupled rabbit sinoatrial node cells. J Gen Physiol 111:95-112.
    • Vervaeke K, Hu H, Graham LJ, Storm JF (2006) Contrasting effects of the persistent Na+ current on neuronal excitability and spike timing. Neuron 49:257-270.
    • Vida I, Bartos M, Jonas P (2006) Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 49:107-117.
    • Wilders R, Verheijck EE, Kumar R, Goolsby WN, van Ginneken AC, Joyner RW, Jongsma HJ (1996) Model clamp and its application to synchronization of rabbit sinoatrial node cells. Am J Physiol 271:H2168-2182.
    • Williams SR and Stuart GJ (2003) Voltage- and site-dependent control of the somatic impact of dendritic IPSPs. J Neurosci 23, 7358-7367.
    • Williams SR (2004) Spatial compartmentalization and functional impact of conductance in pyramidal neurons. Nat Neurosci 7:961-967.
    • Williams SR (2005) Encoding and decoding of dendritic excitation during active states in pyramidal neurons. J Neurosci 25:5894-5902.
    • Williams SR and Mitchell SJ (2008) Direct measurement of somatic voltage clamp errors in central neurons. Nature Neurosci 11:790-798.
    • Wolfart J, Debay D, Le Masson G, Destexhe A, Bal T (2005) Synaptic background activity controls spike transfer from thalamus to cortex. Nat Neurosci 8:1760-1767.
    • Yarom Y (1991) Rhythmogenesis in a hybrid system--interconnecting an olivary neuron to an analog network of coupled oscillators. Neuroscience 44:263-275.
    • Zosimovskii VA, Balaban PM, Zakharov IS, Sokolov EN (1980) [Study of monosynaptic excitatory connections using a biomathematical model of neuronal interaction] Neirofiziologiia 12(4):413-20. Russian.
    • Zosimovskii VA (1980) [Use of EC-1020 computers for experimental studies of synaptic interaction of mollusk neurons] Zh Vyssh Nerv Deiat Im I P Pavlova. 30(6):1306-11. Russian.
    • Zsiros V, Hestrin S (2005) Background synaptic conductance and precision of EPSP-spike coupling at pyramidal cells. J Neurophysiol 93:3248-3256.
    Personal tools
    Namespaces

    Variants
    Actions
    Navigation
    Focal areas
    Activity
    Tools