Makarov , Valeri A. and Korovaichuk, A. and Makarova, J. and Benito, N. and Herreras, Óscar (2010) Minor Contribution of Principal Excitatory Pathways to Hippocampal LFPs in the Anesthetized Rat: A Combined Independent Component and Current Source Density Study. Journal of Neurophysiology, 104 (1 ). 484-497 . ISSN 0022-3077
Restricted to Repository staff only until 31 December 2020.
Official URL: http://jn.physiology.org/content/104/1/484.full.pdf+html
Korovaichuk A, Makarova J, Makarov VA, Benito N, Herreras O. Minor contribution of principal excitatory pathways to hippocampal LFPs in the anesthetized rat: A combined independent component and current source density study. J Neurophysiol 104: 484-497, 2010. First published May 12, 2010; doi:10.1152/jn.00297.2010. Analysis of local field potentials (LFPs) helps understand the function of the converging neuronal populations that produce the mixed synaptic activity in principal cells. Recently, using independent component analysis (ICA), we resolved ongoing hippocampal activity into several major contributions of stratified LFP-generators. Here, using pathway-specific LFP reconstruction, we isolated LFP-generators that describe the activity of Schaffer-CA1 and Perforant-Dentate excitatory inputs in the anesthetized rat. First, we applied ICA and current source density analysis to LFPs evoked by electrical subthreshold stimulation of the pathways. The results showed that pathway specific activity is selectively captured by individual components or LFP-generators. Each generator matches the known distribution of axonal terminal fields in the hippocampus and recovers the specific time course of their activation. Second, we use sparse weak electrical stimulation to prime ongoing LFPs with activity of a known origin. Decomposition of ongoing LFPs yields a few significant LFP-generators with distinct spatiotemporal characteristics for the Schaffer and Perforant inputs. Both pathways convey an irregular temporal pattern in bouts of population activity of varying amplitude. Importantly, the contribution of Schaffer and Perforant inputs to the power of raw LFPs in the hippocampus is minor (7 and 5%, respectively). The results support the hypothesis on a sparse population code used by excitatory populations in the entorhino-hippocampal system, and they validate the separation of LFP-generators as a powerful tool to explore the computational function of neuronal circuits in real time.
|Uncontrolled Keywords:||Pyramidal cells; Behaving rat; In-vivo; Potential oscillations; Spreading depression; Tissue resistivity; Entorhinal cortex; Evoked-potentials; Population spikes; Cortical-neurons|
|Subjects:||Medical sciences > Biology > Neurosciences|
Aika Y, Ren JQ, Kosaka K, Kosaka T. Quantitative analysis of GABA-likeimmunoreactive and parvalbumin-containing neurons in the CA1 region of the rat hippocampus using a stereological method, the dissector. Exp Brain Res 99: 267–276, 1994.
Alonso A, Llinás RR. Subthreshold Na-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342: 175–177, 1989.
Amari S, Cichocki A, Yang H. A new learning algorithm for blind source separation. Adv Neural Inform Process Syst 8: 757–763, 1996.
Andersen P, Bliss TVP, Skrede KK. Lamellar organization of hippocampal excitatory pathways. Exp Brain Res 13: 222–238, 1971.
Anderson JS, Carandini M, Ferster D. Orientation tuning of input conductance, excitation and inhibition in cat primary visual cortex. J Neurophysiol 84: 909–926, 2000.
Bédard C, Kröger H, Destexhe A. Modeling extracellular field potentials and the frequency-filtering properties of extracellular space. Biophys J 86: 1829–1842, 2004.
Bell A, Sejnowski T. An information-maximization approach to blind separation and blind deconvolution. Neural Comput 7: 1129–1159, 1995.
Borg-Graham LJ, Monier C, Frégnac Y. Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393: 369–373, 1998.
Bragin A, Jandó G, Nádasdy Z, van Landeghem M, Buzsáki G. Dentate EEG spikes and associated interneuronal population bursts in the hippocampal hilar region of the rat. J Neurophysiol 73: 1691–1705, 1995.
Brankack J, Stewart M, Fox SE. Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators. Brain Res 615: 310–327, 1993.
Buzsáki G, Czopf J, Kondákor I, Kellényi L. Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: currentsource density analysis, effects of urethane and atropine. Brain Res 365: 125–137, 1986.
Buzsáki G, Leung LS, Vanderwolf CH. Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287: 139–171, 1983.
Canals S, López-Aguado L, Herreras O. Synaptically-recruited apical currents are required to initiate a jonal and apical spikes in hippocampal pyramidal cells: modulation by inhibition. J Neurophysiol 93: 909–918, 2005.
Castellanos NP, Makarov VA. Recovering EEG brain signals: artifact suppression with wavelet enhanced independent component analysis. J Neurosci Methods 158: 300–312, 2006.
Choi S, Cichocki A, Park HM, Lee SY. Blind source separation and independent component analysis: a review. Neural Inform Process Lett Rev 6: 1–57, 2005.
Chrobak JJ, Buzsaki G. Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. J Neurosci 14: 6160–6170, 1994.
Csicsvari J, Jamieson B, Wise KD, Buzsáki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37: 311–322, 2003.
Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single trial EEG dynamics including independent component analysis. J Neurosci Methods 134: 9–21, 2004.
Einevoll GT, Pettersen KH, Devor A, Ulbert I, Halgren E, Dale AM. Laminar population analysis: estimating firing rates and evoked synaptic activity from multielectrode recordings in rat barrel cortex. J Neurophysiol 97: 2174–2190, 2007.
Frank LM, Brown EN, Wilson MA. A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. J Neurophysiol 86: 2029–2040, 2001.
Freeman JA, Nicholson C. Experimental optimization of current source-density technique for anuran cerebellum. J Neurophysiol 38: 369–382, 1975.
Hajos N, Katona I, Naiem SS, MacKie K, Ledent C, Mody I, Freund TF. Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12: 3239–3249, 2000.
Herreras O. Propagating dendritic action potential mediates synaptic transmission in CA1 pyramidal cells in situ. J Neurophysiol 64: 1429–1441, 1990.
Herreras O, Solís JM, Herranz AS, Martín del Río R, Lerma J. Sensory modulation of hippocampal transmission. II. Evidence for a cholinergic locus of inhibition in the Schaffer-CA1 synapse. Brain Res 451: 303–313, 1988.
Herreras O, Solís JM, Martín del Río R, Lerma J. Characteristics of CA1 activation through the hippocampal trisynaptic pathway in the unanaesthetized rat. Brain Res 413: 75–86, 1987.
Hjorth-Simonsen A, Jeune B. Origin and termination of the hippocampal perforant path in the rat studied by silver impregnation. J Comp Neurol 144: 215–232, 1972.
Hyvärinen A, Oja E. Independent component analysis: algorithms and applications Neural Netw 13: 411–430, 2000.
Jarosiewicz B, Skaggs WE. Level of arousal during the small irregular activity state in the rat hippocampal EEG. J Neurophysiol 91: 2649–2657, 2004.
Jung KY, Kim JM, Kim DW, Chung CS. Independent component analysis of generalized spike-and-wave discharges: primary versus secondary bilateral synchrony. Clin Neurophysiol 116: 913–919, 2005.
Kandel ER, Spencer WA, Brinley FJ Jr. Electrophysiology of hippocampal neurons. I. Sequential invasion and synaptic organization. J Neurophysiol 24: 225–242, 1961.
Kocsis B, Bragin A, Buzsáki G. Interdependence of multiple theta generators in the hippocampus: a partial coherence analysis. J Neurosci 19: 6200– 6212, 1999.
Lee T, Girolomi M, Sejnowski T. Independent component analysis using an extended infomax algorithm for mixed subgaussian and supergaussian sources. Neural Comput 11: 417–441, 1999.
Leung LS, Roth L, Canning KJ. Entorhinal inputs to hippocampal CA1 and dentate gyrus in the rat: a current-source-density study. J Neurophysiol 73: 2392–2403, 1995.
Lømo T. Patterns of activation in a monosynaptic cortical pathway: the perforant path input to the dentate area of the hippocampal formation. Exp Brain Res 12: 18–45, 1971.
López-Aguado L, Ibarz JM, Herreras O. Activity-dependent changes of tissue resistivity in the CA1 region in vivo are layer-specific: modulation of evoked potentials. Neuroscience 108: 249–262, 2001.
López-Aguado L, Ibarz JM, Varona P, Herreras O. Structural inhomogeneities differentially modulate action currents and population spikes initiated in the axon or dendrites. J Neurophysiol 88: 2809–2820, 2002.
Lorente de Nó R. Analysis of the distribution of action currents of nerves in volume conductors. In a study of nerve physiology. Stud Rockefeller Inst Med Res Repr 132: 384–477, 1947.
Makarov VA, Makarova J, Herreras O. Disentanglement of local field potential sources by independent component analysis. J Comput Neurosci In press.
Makarova J, Gómez-Galán M, Herreras O. Layer specific changes in tissue resistivity and spatial cancellation of transmembrane currents shape the voltage signal during spreading depression in the CA1 vivo. Eur J Neurosci 27: 444-456, 2008.
Makarova J, Makarov VA, Herreras O. A model of sustained field potentials based on gradients of polarization in single neurons. J Neurophysiol 103: 2446–2457, 2010.
Makeig S, Debener S, Onton J, Delorme A. Mining event-related brain dynamics. Trends Cogn Sci 8: 204–210, 2004.
Mann EO, Radcliffe CA, Paulsen O. Hippocampal gamma-frequency oscillations: from interneurones to pyramidal cells, and back. J Physiol 562: 55–63, 2005.
Miles R, Wong RK. Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J Physiol 388: 611–629, 1987.
Mitzdorf U. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev 65: 37–100, 1985.
Nunez PL, Srinivasan R. Electric Fields of the Brain: The Neurophysics of EEG (2nd ed.). New York: Oxford, 2006.
Oren I, Hajos N, Paulsen O. Identification of the current generator underlying cholinergically induced gamma frequency field potential oscillations in the hippocampal CA3 region. J Physiol 588: 785–797, 2010.
Ranck JB Jr. Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. Part 1. Behavioral correlates and firing repertoires. Exp Neurol 40: 462–531, 1973.
Rudolph M, Pelletier JG, Paré D, Destexhe A. Characterization of synaptic conductances and integrative properties during electrically induced EEGactivated states in neocortical neurons in vivo. J Neurophysiol 94: 2805-2821, 2005.
Soltesz I, Deschenes M. Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J Neurophysiol 70: 97– 116, 1993.
Somogyi P, Klausberger T. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J Physiol 562: 9–26, 2005.
Stone JV. Independent Component Analysis: A Tutorial Introduction. Cambridge, MA: MIT Press, 2004.
Tanskanen JM, Mikkonen JE, Penttonen M. Independent component analysis of neural populations from multielectrode field potential measurements. J Neurosci Methods 145: 213–232, 2005.
Thompson LT, Best PJ. Place cells and silent cells in the hippocampus of freely-behaving rats. J Neurosci 9: 2382–2390, 1989.
Varona P, Ibarz JM, López-Aguado L, Herreras O. Macroscopic and subcellular factors shaping CA1 population spikes. J Neurophysiol 83: 2192–2208, 2000.
Vigario R, Sarela J, Jousmaki V, Hamalainen M, Oja E. Independent component approach to the analysis of EEG and MEG recordings. IEEE Trans Biomed Eng 47: 589–593, 2000.
Whittington MA, Traub RD, Jefferys JGR. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373: 612–615, 1995.
Wu K, Canning KJ, Leung LS. Functional interconnections between CA3 and the dentate gyrus revealed by current source density analysis. Hippocampus 8: 217–230, 1998.
Ylinen A, Bragin A, Nádasdy Z, Jandó G, Szabó I, Sik A, Buzsáki G. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15: 30–46, 1995.
|Deposited On:||02 Oct 2012 08:20|
|Last Modified:||07 Feb 2014 09:32|
Repository Staff Only: item control page