In Vitro and In Vivo Recording of Local Field Potential Oscillations in Mouse Hippocampus

L.H. Forsyth1, J. Witton2, J.T. Brown2, A.D. Randall2, M.W. Jones1

1 School of Physiology and Pharmacology, University of Bristol, Bristol, United Kingdom, 2 Pfizer Applied Neurophysiology Group, School of Physiology and Pharmacology, University of Bristol, Bristol, United Kingdom
Publication Name:  Current Protocols in Mouse Biology
Unit Number:   
DOI:  10.1002/9780470942390.mo120089
Online Posting Date:  September, 2012
GO TO THE FULL TEXT: PDF or HTML at Wiley Online Library

Abstract

Oscillations in hippocampal local field potentials (LFP) reflect the coordinated, rhythmic activity of constituent interneuronal and principal cell populations. Quantifying changes in oscillatory patterns and power therefore provides a powerful metric through which to infer mechanisms and functions of hippocampal network activity at the mesoscopic level, bridging single‐neuron studies to behavioral assays of hippocampal function. Here, complementary protocols that enable mechanistic analyses of oscillation generation in vitro (in slices and a whole hippocampal preparation) and functional analyses of hippocampal circuits in behaving mice are described. Used together, these protocols provide a comprehensive view of hippocampal phenotypes in mouse models, highlighting oscillatory biomarkers of hippocampal function and dysfunction. Curr. Protoc. Mouse Biol. 2:273‐294 © 2012 by John Wiley & Sons, Inc.

Keywords: theta rhythm; gamma rhythm; electrophysiology; LFP; slice; in vitro; in vivo

     
 
GO TO THE FULL PROTOCOL:
PDF or HTML at Wiley Online Library

Table of Contents

  • Introduction
  • Basic Protocol 1: Producing Hippocampal Slices
  • Basic Protocol 2: Pharmacological Induction of Gamma Oscillations
  • Support Protocol 1: Recording Spontaneous Theta Oscillations in an In Vitro Mouse Whole Hippocampus Preparation
  • Basic Protocol 3: Recording of Local Field Potentials in Mouse Hippocampus In Vivo
  • Reagents and Solutions
  • Commentary
  • Literature Cited
  • Figures
     
 
GO TO THE FULL PROTOCOL:
PDF or HTML at Wiley Online Library

Materials

Basic Protocol 1: Producing Hippocampal Slices

  Materials
  • Mice
  • High‐sucrose cutting solution (see recipe), ice‐cold
  • Carbogen (95% O 2/5% CO 2) source
  • Quick drying superglue (cryanoacylate)
  • aCSF (see recipe)
  • Agar block (∼15 × 15 × 10–mm)
  • Large surgical scissors
  • Scalpel with no. 11 blade
  • Vannas micro scissors/small surgical scissors
  • Dumont no. 7 forceps
  • Small spatulas
  • Small teaspoon
  • Filter paper
  • 10‐cm diameter Petri dishes
  • Medium spatula
  • Vibrating microtome
  • Pasteur pipet
  • Slice incubation chamber
  • Razor blades

Basic Protocol 2: Pharmacological Induction of Gamma Oscillations

  Materials
  • Reservoir of carbogenated aCSF (see recipe)
  • Carbogen (95% O 2/5% CO 2) source
  • Hippocampal slices (see protocol 1)
  • Kainate stock (e.g., 1 mM)
  • Slice recording chamber fixed on an air‐table and surrounded by a grounded Faraday cage
  • Perfusion pump
  • Dissection microscope
  • Soft bristled no. 5 sable hair brush, optional
  • Small pieces of lens cleaning tissue (∼1‐mm square; interface recording chamber only)
  • Slice weights (e.g., short pieces (2‐ to 3‐mm long) of twisted silver wire; submerged recording chamber only), optional
  • Pasteur pipet
  • Glass microelectrodes (pulled from borosilicate glass capillaries, <1‐mm diameter, to a resistance of 2 to 5 mΩ)
  • Microfil and 1‐ml syringe
  • Sliver wire recording electrode connected to a headstage pre‐amplifier
  • Micromanipulator
  • Water bath
  • Amplifier
  • Hum Bug noise eliminator
  • Analog‐to‐digital signal converter
  • Personal computer with electrophysiology data acquisition software

Support Protocol 1: Recording Spontaneous Theta Oscillations in an In Vitro Mouse Whole Hippocampus Preparation

  • Hippocampal isolates (see protocol 1)

Basic Protocol 3: Recording of Local Field Potentials in Mouse Hippocampus In Vivo

  Materials
  • Cyanoacrylate glue (quick drying superglue)
  • Gold plating solution (e.g., non‐cyanide, SIFCO Applied Surface Concepts), optional
  • Dental acrylic (e.g., Simplex Rapid liquid and powder, Kemdent), optional
  • 70% ethanol
  • Mice
  • Isofluorane
  • Oxygen
  • Surgical eye lubricant (e.g., Lacri‐lube, Allergan)
  • Lidocaine
  • Analgesic (e.g., buprenorphine, Buprenex)
  • 0.9% sterile saline
  • Dental adhesive cement (e.g., Super‐bond C&B, Sun Medical Ltd)
  • Silver conductive paint (e.g., Electrolube)
  • Gentamicin dental acrylic (e.g., DePuy International Ltd)
  • Delrin plastic sheet (2‐mm thickness, e.g., Gilbert Curry Industrial Plastics)
  • Vice clamp holder (or other suitable holder for electrode array building)
  • Mouse stereotaxic frame
  • Drill press (with XYZ measuring function to ± 0.01 mm)
  • 23‐G guide cannula holders (e.g., Cooper Needle Works)
  • 30‐G stainless steel cannulae (e.g., Cooper Needle Works)
  • Electrode interface board (EIB; or suitable alternative)
  • 60‐µm Formvar‐insulated nichrome wire (e.g., A‐M Systems)
  • Gold pins (or other suitable method of fixing wires to selected connector chip)
  • Silver wire (∼200‐µm diameter; e.g., World Precision Instruments)
  • Sharp, fine scissors
  • Anesthesia chamber
  • Stereotaxic gas anesthesia mask
  • Homeothermic blanket and temperature probe
  • Fur shaver
  • Scalpel
  • Fine forceps
  • Surgical drill
  • Stainless steel skull screws (thread diameter approximately 0.75 mm; jeweller's screws may suffice)
  • Hypodermic needles
  • Sutures
  • Recording equipment: headstage pre‐amplifier and fine wire tether cable
  • Computer with data acquisition software
  • Impedance meter (e.g., Bak Electronics IMP‐2)
GO TO THE FULL PROTOCOL:
PDF or HTML at Wiley Online Library

Figures

Videos

Literature Cited

Literature Cited
   Adhikari, A., Sigurdsson, T., Topiwala, M.A., and Gordon, J.A. 2010. Cross‐correlation of instantaneous amplitudes of field potential oscillations: A straightforward method to estimate the directionality and lag between brain areas. J. Neurosci. Methods 191:191‐200.
   Anderson, K.L., Rajagovindan, R., Ghacibeh, G.A., Meador, K.J., and Ding, M. 2010. Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. Cereb. Cortex 20:1604‐1612.
   Arguello, P.A. and Gogos, J.A. 2006. Modeling madness in mice: One piece at a time. Neuron 52:179‐196.
   Atallah, B.V. and Scanziani, M. 2009. Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition. Neuron 62:566‐577.
   Battaglia, F.P., Kalenscher, T., Cabral, H., Winkel, J., Bos, J., Manuputy, R., van Lieshout, T., Pinkse, F., Beukers, H., and Pennartz, C. 2009. The Lantern: An ultra‐light micro‐drive for multi‐tetrode recordings in mice and other small animals. J. Neurosci. Methods 178:291‐300.
   Bokil, H., Purpura, K., Schoffelen, J.M., Thomson, D., and Mitra, P. 2007. Comparing spectra and coherences for groups of unequal size. J. Neurosci. Methods 159:337‐345.
   Bokil, H., Andrews, P., Kulkarni, J.E., Mehta, S., and Mitra, P.P. 2010. Chronux: A platform for analyzing neural signals. J. Neurosci. Methods 192:146‐151.
   Brown, J.T., Teriakidis, A., and Randall, A.D. 2006. A pharmacological investigation of the role of GLUK5‐containing receptors in kainate‐driven hippocampal gamma band oscillations. Neuropharmacology 50:47‐56.
   Brown, J.T., Davies, C.H., and Randall, A.D. 2007. Synaptic activation of GABAB receptors regulates neuronal network activity and entrainment. Eur. J. Neurosci. 25:2982‐2990.
   Buhl, E.H., Tamás, G., and Fisahn, A. 1998. Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J. Physiol. 513:117‐126.
   Buzsáki, G. 1989. Two‐stage model of memory trace formation: A role for “noisy” brain states. Neuroscience 31:551‐570.
   Buzsáki, G. 2002. Theta oscillations in the hippocampus. Neuron 33:325‐340.
   Buzsáki, G., Buhl, D.L., Harris, K.D., Csicsvari, J., Czeh, B., and Morozov, A. 2003. Hippocampal network patterns of activity in the mouse. Neuroscience 116:201‐211.
   Cadotte, A.J., DeMarse, T.B., He, P., and Ding, M. 2008. Causal measures of structure and plasticity in simulated and living neural networks. PloS One 3:e3355.
   Denker, M., Roux, S., Linden, H., Diesmann, M., Riehle, A., and Grun, S. 2011. The local field potential reflects surplus spike synchrony. Cereb. Cortex 21:2681‐2695.
   Duzel, E., Penny, W.D., and Burgess, N. 2010. Brain oscillations and memory. Curr. Opin. Neurobiol. 20:143‐149.
   Fan, D., Rich, D., Holtzman, T., Ruther, P., Dalley, J.W., Lopez, A., Rossi, M.A., Barter, J.W., Salas‐Meza, D., Herwik, S., Holzhammer, T., Morizio, J., and Yin, H.H. 2011. A wireless multi‐channel recording system for freely behaving mice and rats. PloS One 6:e22033.
   Fisahn, A. 2005. Kainate receptors and rhythmic activity in neuronal networks: Hippocampal gamma oscillations as a tool. J. Physiol. 562:65‐72.
   Fisahn, A., Pike, F.G., Buhl, E.H., and Paulsen, O. 1998. Cholinergic induction of network oscillations at 40[thinsp]Hz in the hippocampus in vitro. Nature 394:186‐189.
   Fisahn, A., Contractor, A., Traub, R.D., Buhl, E.H., Heinemann, S.F., and McBain, C.J. 2004. Distinct roles for the kainate receptor subunits GluR5 and GluR6 in kainate‐induced hippocampal gamma oscillations. J. Neurosci. 24:9658‐9668.
   Gloveli, T., Dugladze, T., Rotstein, H.G., Traub, R.D., Monyer, H., Heinemann, U., Whittington, M.A., and Kopell, N.J. 2005. Orthogonal arrangement of rhythm‐generating microcircuits in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 102:13295‐13300.
   Goutagny, R., Jackson, J., and Williams, S. 2009. Self‐generated theta oscillations in the hippocampus. Nat. Neurosci. 12:1491‐1493.
   Hajos, N., Ellender, T.J., Zemankovics, R., Mann, E.O., Exley, R., Cragg, S.J., Freund, T.F., and Paulsen, O. 2009. Maintaining network activity in submerged hippocampal slices: Importance of oxygen supply. Eur. J. Neurosci. 29:319‐327.
   Huxter, J.R., Zinyuk, L.E., Roloff, E.L., Clarke, V.R., Dolman, N.P., More, J.C., Jane, D.E., Collingridge, G.L., and Muller, R.U. 2007. Inhibition of kainate receptors reduces the frequency of hippocampal theta oscillations. J. Neurosci. 27:2212‐2223.
   Javedan, S.P., Fisher, R.S., Eder, H.G., Smith, K., and Wu, J. 2002. Cooling abolishes neuronal network synchronization in rat hippocampal slices. Epilepsia 43:574‐580.
   Jones, M.W. and Wilson, M.A. 2005. Theta rhythms coordinate hippocampal‐prefrontal interactions in a spatial memory task. PLoS Biol. 3:e402.
   Kajikawa, Y. and Schroeder, C.E. 2011. How local is the local field potential. Neuron 72:847‐858.
   Katzner, S., Nauhaus, I., Benucci, A., Bonin, V., Ringach, D.L., and Carandini, M. 2009. Local origin of field potentials in visual cortex. Neuron 61:35‐41.
   Klausberger, T. and Somogyi, P. 2008. Neuronal diversity and temporal dynamics: The unity of hippocampal circuit operations. Science 321:53‐57.
   Korotkova, T., Fuchs, E.C., Ponomarenko, A., von Engelhardt, J., and Monyer, H. 2010. NMDA receptor ablation on parvalbumin‐positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 68:557‐569.
   Leão, R.N., Tan, H.M., and Fisahn, A. 2009. Kv7/KCNQ channels control action potential phasing of pyramidal neurons during hippocampal gamma oscillations in vitro. J. Neurosci. 29:13353‐13364.
   Linden, H., Tetzlaff, T., Potjans, T.C., Pettersen, K.H., Grun, S., Diesmann, M., and Einevoll, G.T. 2011. Modeling the spatial reach of the LFP. Neuron 72:859‐872.
   Lu, C.B., Jefferys, J.G.R., Toescu, E.C., and Vreugdenhil, M. 2011. In vitro hippocampal gamma oscillation power as an index of in vivo CA3 gamma oscillation strength and spatial reference memory. Neurobiol. Learn. Mem. 95:221‐230.
   Ludwig, K.A., Uram, J.D., Yang, J., Martin, D.C., and Kipke, D.R. 2006. Chronic neural recordings using silicon microelectrode arrays electrochemically deposited with a poly(3,4‐ethylenedioxythiophene) (PEDOT) film. J. Neur. Eng. 3:59‐70.
   Mann, E.O. and Paulsen, O. 2005. Mechanisms underlying gamma ([γ]40 Hz') network oscillations in the hippocampus—A mini‐review. Prog. Biophys. Mol. Biol. 87:67‐76.
   Mann, E.O. and Mody, I. 2010. Control of hippocampal gamma oscillation frequency by tonic inhibition and excitation of interneurons. Nat. Neurosci. 13:205‐212.
   Nakashiba, T., Buhl, D.L., McHugh, T.J., and Tonegawa, S. 2009. Hippocampal CA3 output is crucial for ripple‐associated reactivation and consolidation of memory. Neuron 62:781‐787.
   Nelson, M.J. and Pouget, P. 2010. Do electrode properties create a problem in interpreting local field potential recordings? J. Neurophysiol. 103:2315‐2317.
   O'Keefe, J. and Burgess, N. 2005. Dual phase and rate coding in hippocampal place cells: Theoretical significance and relationship to entorhinal grid cells. Hippocampus 15:853‐866.
   Onslow, A.C., Bogacz, R., and Jones, M.W. 2010. Quantifying phase‐amplitude coupling in neuronal network oscillations. Prog. Biophys. Mol. Biol. 105:49‐57.
   Oren, I., Mann, E.O., Paulsen, O., and Hájos, N. 2006. Synaptic currents in anatomically identified CA3 neurons during hippocampal gamma oscillations in vitro. J. Neurosci. 26:9923‐9934.
   Penny, W.D., Duzel, E., Miller, K.J., and Ojemann, J.G. 2008. Testing for nested oscillation. J. Neurosci. Methods 174:50‐61.
   Pesaran, B. 2009. Uncovering the mysterious origins of local field potentials. Neuron 61:1‐2.
   Pietersen, A.N., Patel, N., Jefferys, J.G., and Vreugdenhil, M. 2009. Comparison between spontaneous and kainate‐induced gamma oscillations in the mouse hippocampus in vitro. Eur. J. Neurosci. 29:2145‐2156.
   Reichinnek, S., Kunsting, T., Draguhn, A., and Both, M. 2010. Field potential signature of distinct multicellular activity patterns in the mouse hippocampus. J. Neurosci. 30:15441‐15449.
   Sadowski, J.H., Jones, M.W., and Mellor, J.R. 2011. Ripples make waves: Binding structured activity and plasticity in hippocampal networks. Neur. Plast. 2011:960389.
   Siapas, A.G., Lubenov, E.V., and Wilson, M.A. 2005. Prefrontal phase locking to hippocampal theta oscillations. Neuron 46:141‐151.
   Sigurdsson, T., Stark, K.L., Karayiorgou, M., Gogos, J.A., and Gordon, J.A. 2010. Impaired hippocampal‐prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 464:763‐767.
   Sirota, A., Montgomery, S., Fujisawa, S., Isomura, Y., Zugaro, M., and Buzsaki, G. 2008. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60:683‐697.
   Stewart, M. and Fox, S.E. 1990. Do septal neurons pace the hippocampal theta rhythm. Trends Neurosci. 13:163‐169.
   Vreugdenhil, M., Jefferys, J.G.R., Celio, M.R., and Schwaller, B. 2003. Parvalbumin‐deficiency facilitates repetitive IPSCs and gamma oscillations in the hippocampus. J. Neurophysiol. 89:1414‐1422.
   Vreugdenhil, M. and Toescu, E.C. 2005. Age‐dependent reduction of gamma oscillations in the mouse hippocampus in vitro. Neuroscience 132:1151‐1157.
   Wulff, P., Ponomarenko, A.A., Bartos, M., Korotkova, T.M., Fuchs, E.C., Bahner, F., Both, M., Tort, A.B., Kopell, N.J., Wisden, W., and Monyer, H. 2009. Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin‐positive interneurons. Proc. Natl. Acad. Sci. U.S.A. 106:3561‐3566.
GO TO THE FULL PROTOCOL:
PDF or HTML at Wiley Online Library