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H-Type Membrane Current Shapes the Local Field Potential (LFP) From This Accepted Manuscript has not been copyedited and formatted. The final version may differ from this version. Research Articles: Systems/Circuits h-type membrane current shapes the local field potential (LFP) from populations of pyramidal neurons Torbjørn V Ness, Michiel W H Remme and Gaute T Einevoll Torbjørn V Ness, Faculty of Science and Technology, Norwegian University of Life Sciences, 1432 Ås, Norway. Michiel W H Remme, Institute for Theoretical Biology, Humboldt University Berlin, 10115 Berlin, Germany. Gaute T Einevoll, Faculty of Science and Technology, Norwegian University of Life Sciences, 1432 Ås, Norway; Department of Physics, University of Oslo, 0316 Oslo, Norway. DOI: 10.1523/JNEUROSCI.3278-17.2018 Received: 18 November 2017 Revised: 17 April 2018 Accepted: 1 May 2018 Published: 6 June 2018 Author contributions: T.V.N., M.W.H.R., and G.T.E. designed research; T.V.N. performed research; T.V.N. analyzed data; T.V.N., M.W.H.R., and G.T.E. wrote the paper. Conflict of Interest: The authors declare no competing financial interests. This research has received funding from the European Union's Horizon 2020 Framework Programme for Research and Innovation under the Specific Grant Agreement No. 720270 (Human Brain Project SGA1) and No. 785907 (Human Brain Project SGA2) (TVN, GTE), the Research Council of Norway (Notur, nn4661k) (TVN, GTE), the Einstein Foundation Berlin (MWHR), and we want to thank Susanne Schreiber for her funding of MWHR through the Bundesministerium für Bildung und Forschung (www.bmbf.de; grant number 01GQ0901). Corresponding author: Gaute T Einevoll, Faculty of Science and Technology, Norwegian University of Life Sciences, 1432 Ås, Norway; [email protected] Cite as: J. Neurosci ; 10.1523/JNEUROSCI.3278-17.2018 Alerts: Sign up at www.jneurosci.org/cgi/alerts to receive customized email alerts when the fully formatted version of this article is published. Accepted manuscripts are peer-reviewed but have not been through the copyediting, formatting, or proofreading process. Copyright © 2018 the authors 1 Title: 2 h-type membrane current shapes the local field potential (LFP) from populations of pyramidal 3 neurons 4 5 Abbreviated title: 6 h-type current shapes the LFP 7 8 Author names and affiliation: 9 1) Torbjørn V Ness, Faculty of Science and Technology, Norwegian University of Life Sciences, 10 1432 Ås, Norway. 11 2) Michiel W H Remme, Institute for Theoretical Biology, Humboldt University Berlin, 10115 12 Berlin, Germany. 13 3) Gaute T Einevoll, Faculty of Science and Technology, Norwegian University of Life Sciences, 14 1432 Ås, Norway; Department of Physics, University of Oslo, 0316 Oslo, Norway. 15 16 Corresponding author: 17 Gaute T Einevoll, Faculty of Science and Technology, Norwegian University of Life Sciences, 1432 18 Ås, Norway; [email protected] 19 20 Number of pages: 23 21 Number of figures: 9 22 Number of tables: 0 23 Number of multimedia: 0 24 Number of 3D models: 0 25 26 Number of words for Abstract: 248 27 Number of words for Introduction: 684 28 Number of words for Discussion: 1654 29 30 Conflict of Interest: 31 The authors declare no competing financial interests. 32 33 Acknowledgements: 34 This research has received funding from the European Union’s Horizon 2020 Framework 35 Programme for Research and Innovation under the Specific Grant Agreement No. 720270 (Human 36 Brain Project SGA1) and No. 785907 (Human Brain Project SGA2) (TVN, GTE), the Research 37 Council of Norway (Notur, nn4661k) (TVN, GTE), the Einstein Foundation Berlin (MWHR), and 38 we want to thank Susanne Schreiber for her funding of MWHR through the Bundesministerium für 39 Bildung und Forschung (www.bmbf.de; grant number 01GQ0901). 1 40 h-type membrane current shapes the local field 41 potential (LFP) from populations of pyramidal neurons 42 Abstract 43 In cortex the local field potential (LFP) is thought to mainly stem from correlated synaptic input to 44 populations of geometrically aligned neurons. Computer models of single cortical pyramidal neurons 45 showed that subthreshold voltage-dependent membrane conductances can also shape the LFP 46 signal, in particular the h-type current, Ih. This ion-channel is prominent in various types of pyramidal 47 neurons, typically showing an increasing density gradient along the apical dendrites. Here, we 48 investigate how Ih affects the LFP generated by a model of a population of cortical pyramidal 49 neurons. We find that the LFP from populations of neurons that receive uncorrelated synaptic input 50 can be well predicted by the LFP from single neurons. In this case, when input impinges on the distal 51 dendrites where most h-type channels are located, a strong resonance in the LFP was measured 52 near the soma, whereas the opposite configuration does not reveal an Ih-contribution to the LFP. 53 Introducing correlations in the synaptic inputs to the pyramidal cells strongly amplifies the LFP, while 54 maintaining the differential effects of Ih for distal dendritic versus perisomatic input. Previous 55 theoretical work showed that input correlations do not amplify LFP power when neurons receive 56 synaptic input uniformly across the cell. We find that this crucially depends on the membrane 57 conductance distribution: asymmetric distribution of Ih results in a strong amplification of the LFP 58 when synaptic inputs to the cell population are correlated. In conclusion we find that the h-type 59 current is particularly suited to shape the LFP signal in cortical populations. 60 61 Significance statement 62 The local field potential (LFP), the low frequency part of extracellular potentials recorded in neural 63 tissue, is often used for probing neural circuit activity. While the cortical LFP is thought to mainly 64 reflect synaptic inputs onto pyramidal neurons, little is known about the role of subthreshold active 65 conductances in shaping the LFP. By means of biophysical modelling we obtain a comprehensive, 66 qualitative understanding of how LFPs generated by populations of cortical pyramidal neurons 67 depend on active subthreshold currents, and identify the key importance of the h-type channel. Our 68 results show that LFPs can give information about the active properties of neurons and that preferred 69 frequencies in the LFP can result from those cellular properties instead of, e.g., network dynamics. 70 2 71 Introduction 72 The Local Field Potential (LFP) is the low frequency part (below ~500 Hz) of the extracellular 73 potentials recorded in the brain. The LFP signal in the mammalian cortex reflects the activity of 74 thousands of neurons (Buzsáki et al., 2012; Einevoll et al., 2013) and is commonly used to study the 75 network dynamics underlying, e.g., sensory processing, motor planning, attention, memory and 76 perception (Roux et al., 2006; Szymanski et al., 2011; Liebe et al., 2012). The LFP signal has further 77 increased in importance in recent decades because of the development of high-density silicon-based 78 micro-electrodes, allowing simultaneous recording of the LFP at thousands of positions spanning 79 entire brain regions (Normann et al., 1999; Buzsáki, 2004; Frey et al., 2009; Lambacher et al., 2011). 80 Furthermore, the LFP shows promise for steering neuroprosthetic devices as it is easier and more 81 stably recorded in chronic settings than single-unit spiking activity (Andersen et al., 2004; Markowitz 82 et al., 2011; Jackson and Hall, 2017). 83 The biophysical origins of the LFP are the transmembrane currents of neurons in the vicinity of the 84 recording electrode (Nunez and Srinivasan, 2006). The extracellular potentials induced by the 85 transmembrane currents can be calculated using the well-established volume conductor theory (Rall 86 and Shepherd, 1968; Holt and Koch, 1999; Nunez and Srinivasan, 2006; Lindén et al., 2014). The 87 main contribution to the cortical LFP is thought to stem from synaptic inputs and the ensuing return 88 currents (Mitzdorf, 1985; Pettersen et al., 2008; Einevoll et al., 2013; Haider et al., 2016). However, 89 cortical neurons are known to express many voltage-dependent (or active) currents (Migliore and 90 Shepherd, 2002; Lai and Jan, 2006; Major et al., 2013) that may contribute to the LFP, either by 91 subthreshold processing of synaptic inputs, or through somatic and dendritic spikes. Reimann et al., 92 (2013) recently studied the combined effects of all active currents on the LFP in a large cortical 93 population model and found substantial effects of these currents. However, their approach did not 94 allow for an easy separation between the effects of spiking currents and the effect of subthreshold 95 active currents, hence, it is still debated to what extent such subthreshold active currents contribute 96 to the LFP. We recently investigated this using computational models of single neurons (Ness et al., 97 2016) and found that subthreshold active currents can strongly amplify or dampen the lowest 98 frequencies of the LFP power spectrum, in the latter case leading to a resonance in the LFP. We 99 identified the key importance of the hyperpolarization-activated inward current, Ih, and in particular, 100 we observed that for synaptic input which selectively targeted the apical dendrites of cortical layer 5 101 pyramidal cells, Ih caused a strong resonance peak in the LFP power spectrum. However, how the 102 observed effect of Ih on the LFP would transfer from a single cell to a neural population remained an 103 open question. 104 Using a modelling approach we here investigate the effect of subthreshold active conductances on 105 the LFP from cortical neural populations. The populations consisted of layer 5 pyramidal cells, as 106 these numerous, large and geometrically aligned cells are thought to be a main contributor to the 107 cortical LFP (Einevoll et al., 2013; Hagen et al., 2016). We demonstrated the key importance of Ih in 108 shaping the LFP from pyramidal cell populations and found that it does this in two fundamentally 109 different ways depending on the synaptic input.
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