In Vitro and In Vivo Recording of Local Field Potential Oscillations in Mouse Hippocampus
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- Abstract
- Table of Contents
- Materials
- Figures
- Literature Cited
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
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
Materials
Basic Protocol 1: Producing Hippocampal Slices
Materials
Basic Protocol 2: Pharmacological Induction of Gamma Oscillations
Materials
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
Materials
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Figures
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Figure 1. Hippocampal isolation and generation of transverse slices. (A ) The brain hemisphere (arrow) is placed on its frontal cortex and a spatula is used to support the medial dorsal cortex. (B ) A second spatula is used to gently peel away the brainstem and thalamus. (C ) The hemisphere following B. The exposed hippocampus is outlined in black. (D ) Isolate the hippocampus (outlined in black) by sliding a spatula between the extreme dorsal surface of the hippocampus and the surrounding cortex. (E ) The isolated hippocampus (arrow). (F ) Place the hippocampal isolate (arrow) into a shallow vessel containing ice‐cold cutting solution and gently bubble with carbogen. Repeat A through F on the second brain hemisphere. (G ) Use a large spatula to lift the hippocampus from the cutting solution. CA1/CA3 should be facing downwards and the dentate gyrus/subiculum facing vertically upwards. (H –I ) Position the spatula above the flat surface of an agar block. Rotate 180° and place the hippocampus onto the agar block with the dentate gyrus/subiculum facing downwards. (J ‐K ) Repeat H through I for the second hippocampal isolate. The hippocampus should be positioned on the block such that the extreme dorsal and ventral ends of the two hippocampi are side by side (arrow). Use a small piece of filter paper to remove excess cutting solution. (L ) Use a razor blade to make a vertical cut through the extreme ventral end of the hippocampi and agar block. (M ) Place a dab of superglue on the microtome stage. (N ) Glue the cut end of the hippocampi and agar block to the microtome stage. Try to avoid getting glue on the hippocampal tissue. Holding the stage vertically should help with this. (O ) Place the stage into the vibrating microtome and cover with ice cold cutting solution. View Image -
Figure 2. Kainate‐induced gamma oscillations in transverse hippocampal slices. (A ) Example spectrogram showing the development of gamma (30 to 100 Hz) oscillations in CA3 following the application of kainate (100 nM, red line) to a transverse hippocampal slice. (B ) Example of steady‐state gamma activity in (A) 80 min after kainate application. The raw trace has been filtered between 1 and 150 Hz. (C ) Pooled data from six transverse hipppocampal slices. The figure plots the time‐course of gamma oscillation generation after application of 100 nM kainate (arrow). Peak gamma band power (filled squares) and frequency (open circles) are plotted. View Image -
Figure 3. Spontaneous theta oscillations in the intact hippocampal isolate. (A ) Example of spontaneous theta (3 to 12 Hz) oscillations recorded in CA1 of the intact hippocampus. The raw trace has been filtered between 1 and 20 Hz. (B ) Spectrogram of steady‐state, spontaneous theta activity in CA1 over a 10‐min recording epoch. Note that in this example the peak frequency was at the lower end of the theta band as the hippocampal isolate was superfused with low K+ (3 mM) containing aCSF. As demonstrated by Goutagny et al. (), the frequency of spontaneous hippocampal theta activity increases with higher K+ concentration in the perfusate. (C ) Fourier generated power spectrum of the recording epoch in B. View Image -
Figure 4. Schematic of array assembly. (A ) Top‐down view of holes drilled in a 2‐mm thick Delrin platform, arranged according to stereotaxic coordinates; this example would target frontal cortex and hippocampus bilaterally. Lengths of 2‐mm of 23‐G cannulae (gray) are glued into the holes, and a connector appropriate for the headstage preamplifier is mounted in the center. (B ) Lengths of 30‐G cannulae (gray) are inserted and glued into the 23‐G holders, and (C ) lengths of nichrome wire loaded into the 30‐G and connected to the electrode interface (e.g., Neuralynx EIB‐18). After checking the electrical connection, the wire is glued in place at the top end of the 30‐G cannulae. (D ) Silver wire for the ground and reference connections is attached and nichrome electrode wire is then trimmed to the required lengths for implantation. View Image -
Figure 5. Overview of typical mouse LFP recording setup. (A ) Photograph showing recording arena (ra), fine‐wire tether (fwt) connected to pulleys (p) and held balanced by counterweights (cw) to allow free movement. Overhead camera (c) monitors behavior. (B ) Implanted adult mouse connected to Neuralynx recording hardware via EIB‐18 and HS18‐LED. View Image -
Figure 6. Examples of LFP data and spectral analysis. (A ) 2 sec of CA1 LFP recorded during active exploration of an open field environment. Top trace shows 0.1 to 475 Hz wideband LFP, with 5 to 10 Hz (theta, middle trace) and 60 to 100 Hz (gamma, lower trace) band‐pass filtered data shown below. Note characteristic correlation between gamma amplitude and theta phase. (B ) CA1 LFP power spectra from eight adult C57BL6 mice exploring a novel environment. Thin lines show spectra for individuals, thick line shows group median. (C ) Running speed over the course of a recording session from a single animal placed in a series of different environments at times shown by arrowheads. Speed is derived from LED‐based positional tracking; inset shows raw tracking data from a single oval open field environment. (D ) Spectrogram taken from same recording session as C, showing characteristic theta‐band power at 5 to 10 Hz. Note increases in theta power coinciding with increased running speed as mouse enters different environments. View Image
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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. |