Abstract
Neuronal network oscillations support interaction within and between brain regions and are implicated in cognitive functions including perception, memory, and spatial navigation. Recent developments of optogenetics and in vivo elecrophysiology made possible a high-precision control of network oscillations. Here, we describe an experimental approach established in our laboratory to optogenetically manipulate hippocampal theta (5–10 Hz) oscillations in behaving mice and thus to causally address their role in behavior. We provide detailed description of this preparation, describe its advantages and limitations and discuss further possible applications.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Salinas E, Sejnowski TJ (2001) Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci 2(8):539–550. doi:10.1038/35086012
Buzsaki G, Wang XJ (2012) Mechanisms of gamma oscillations. Annu Rev Neurosci 35:203. doi:10.1146/annurev-neuro-062111-150444
Cannon J, McCarthy MM, Lee S, Lee J, Borgers C, Whittington MA, Kopell N (2014) Neurosystems: brain rhythms and cognitive processing. Eur J Neurosci 39(5):705–719. doi:10.1111/ejn.12453
Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32:209–224. doi:10.1146/annurev.neuro.051508.135603
Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459(7247):663–667. doi:10.1038/nature08002
Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI (2009) Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462(7271):353–357, nature08573
Csicsvari J, Jamieson B, Wise KD, Buzsaki G (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37(2):311–322
Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci U S A 86(5):1698–1702
Lisman JE, Jensen O (2013) The theta-gamma neural code. Neuron 77(6):1002–1016, S0896-6273(13)00231-6
Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsaki G (2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60(4):683–697, S0896-6273(08)00762-9
Wang J, Hirschmann J, Elben S, Hartmann CJ, Vesper J, Wojtecki L, Schnitzler A (2014) High-frequency oscillations in Parkinson’s disease: spatial distribution and clinical relevance. Mov Disord 29(10):1265–1272. doi:10.1002/mds.25962
Hammond C, Bergman H, Brown P (2007) Pathological synchronization in Parkinson’s disease: networks, models and treatments. Trends Neurosci 30(7):357–364. doi:10.1016/j.tins.2007.05.004
Bragin A, Engel J Jr, Wilson CL, Fried I, Buzsaki G (1999) High-frequency oscillations in human brain. Hippocampus 9(2):137–142
Gulyas AI, Miles R, Sik A, Toth K, Tamamaki N, Freund TF (1993) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366(6456):683–687
Buhl EH, Han ZS, Lorinczi Z, Stezhka VV, Karnup SV, Somogyi P (1994) Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus. J Neurophysiol 71(4):1289–1307
Korotkova T, Fuchs EC, Ponomarenko A, von Engelhardt J, Monyer H (2010) NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 68(3):557–569, S0896-6273(10)00759-2
Wulff P, Ponomarenko AA, Bartos M, Korotkova TM, Fuchs EC, Bahner F, Both M, Tort AB, Kopell NJ, Wisden W, 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(9):3561–3566, 0813176106
Buhl DL, Harris KD, Hormuzdi SG, Monyer H, Buzsaki G (2003) Selective impairment of hippocampal gamma oscillations in connexin-36 knock-out mouse in vivo. J Neurosci 23(3):1013–1018
Racz A, Ponomarenko AA, Fuchs EC, Monyer H (2009) Augmented hippocampal ripple oscillations in mice with reduced fast excitation onto parvalbumin-positive cells. J Neurosci 29(8):2563–2568, 29/8/2563
Contreras D, Steriade M (1995) Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J Neurosci 15(1 Pt 2):604–622
Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336(6195):170–173
Steriade M, McCormick DA, Sejnowski TJ (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262(5134):679–685
Pita-Almenar JD, Yu D, Lu HC, Beierlein M (2014) Mechanisms underlying desynchronization of cholinergic-evoked thalamic network activity. J Neurosci 34(43):14463–14474. doi:10.1523/JNEUROSCI.2321-14.2014
Crandall SR, Cruikshank SJ, Connors BW (2015) A corticothalamic switch: controlling the thalamus with dynamic synapses. Neuron 86(3):768–782. doi:10.1016/j.neuron.2015.03.040
Bartho P, Slezia A, Matyas F, Faradzs-Zade L, Ulbert I, Harris KD, Acsady L (2014) Ongoing network state controls the length of sleep spindles via inhibitory activity. Neuron 82(6):1367–1379. doi:10.1016/j.neuron.2014.04.046
Beltramo R, D’Urso G, Dal Maschio M, Farisello P, Bovetti S, Clovis Y, Lassi G, Tucci V, De Pietri Tonelli D, Fellin T (2013) Layer-specific excitatory circuits differentially control recurrent network dynamics in the neocortex. Nat Neurosci 16(2):227–234. doi:10.1038/nn.3306
Giocomo LM, Hussaini SA, Zheng F, Kandel ER, Moser MB, Moser EI (2011) Grid cells use HCN1 channels for spatial scaling. Cell 147(5):1159–1170. doi:10.1016/j.cell.2011.08.051
Vertes RP, Hoover WB, Viana Di Prisco G (2004) Theta rhythm of the hippocampus: subcortical control and functional significance. Behav Cogn Neurosci Rev 3(3):173–200. doi:10.1177/1534582304273594
Buzsaki G, Moser EI (2013) Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16(2):130–138. doi:10.1038/nn.3304
Grass K, Prast H, Philippu A (1995) Ultradian rhythm in the delta and theta frequency bands of the EEG in the posterior hypothalamus of the rat. Neurosci Lett 191(3):161–164
Prast H, Grass K, Philippu A (1997) The ultradian EEG rhythm coincides temporally with the ultradian rhythm of histamine release in the posterior hypothalamus. Naunyn Schmiedebergs Arch Pharmacol 356(4):526–528
Grass K, Prast H, Philippu A (1998) Influence of catecholamine receptor agonists and antagonists on the ultradian rhythm of the EEG in the posterior hypothalamus. Naunyn Schmiedebergs Arch Pharmacol 357(2):169–175
Grass K, Prast H, Philippu A (1996) Influence of mediobasal hypothalamic lesion and catecholamine receptor antagonists on ultradian rhythm of EEG in the posterior hypothalamus of the rat. Neurosci Lett 207(2):93–96
Akam T, Oren I, Mantoan L, Ferenczi E, Kullmann DM (2012) Oscillatory dynamics in the hippocampus support dentate gyrus-CA3 coupling. Nat Neurosci 15(5):763–768. doi:10.1038/nn.3081
Mattis J, Brill J, Evans S, Lerner TN, Davidson TJ, Hyun M, Ramakrishnan C, Deisseroth K, Huguenard JR (2014) Frequency-dependent, cell type-divergent signaling in the hippocamposeptal projection. J Neurosci 34(35):11769–11780. doi:10.1523/JNEUROSCI.5188-13.2014
Schlingloff D, Kali S, Freund TF, Hajos N, Gulyas AI (2014) Mechanisms of sharp wave initiation and ripple generation. J Neurosci 34(34):11385–11398. doi:10.1523/JNEUROSCI.0867-14.2014
Craig MT, McBain CJ (2015) Fast gamma oscillations are generated intrinsically in CA1 without the involvement of fast-spiking basket cells. J Neurosci 35(8):3616–3624. doi:10.1523/JNEUROSCI.4166-14.2015
Vandecasteele M, Varga V, Berenyi A, Papp E, Bartho P, Venance L, Freund TF, Buzsaki G (2014) Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus. Proc Natl Acad Sci U S A 111(37):13535–13540. doi:10.1073/pnas.1411233111
Stark E, Eichler R, Roux L, Fujisawa S, Rotstein HG, Buzsaki G (2013) Inhibition-induced theta resonance in cortical circuits. Neuron 80(5):1263–1276. doi:10.1016/j.neuron.2013.09.033
Stark E, Roux L, Eichler R, Senzai Y, Royer S, Buzsaki G (2014) Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations. Neuron 83(2):467–480. doi:10.1016/j.neuron.2014.06.023
Pastoll H, Solanka L, van Rossum MC, Nolan MF (2013) Feedback inhibition enables theta-nested gamma oscillations and grid firing fields. Neuron 77(1):141–154. doi:10.1016/j.neuron.2012.11.032
Kim T, Thankachan S, McKenna JT, McNally JM, Yang C, Choi JH, Chen L, Kocsis B, Deisseroth K, Strecker RE, Basheer R, Brown RE, McCarley RW (2015) Cortically projecting basal forebrain parvalbumin neurons regulate cortical gamma band oscillations. Proc Natl Acad Sci U S A 112(11):3535–3540. doi:10.1073/pnas.1413625112
Sohal VS, Zhang F, Yizhar O, Deisseroth K (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459(7247):698–702. doi:10.1038/nature07991
Lepousez G, Lledo PM (2013) Odor discrimination requires proper olfactory fast oscillations in awake mice. Neuron 80(4):1010–1024. doi:10.1016/j.neuron.2013.07.025
Siegle JH, Pritchett DL, Moore CI (2014) Gamma-range synchronization of fast-spiking interneurons can enhance detection of tactile stimuli. Nat Neurosci 17(10):1371–1379. doi:10.1038/nn.3797
Yamamoto J, Suh J, Takeuchi D, Tonegawa S (2014) Successful execution of working memory linked to synchronized high-frequency gamma oscillations. Cell 157(4):845–857. doi:10.1016/j.cell.2014.04.009
Kim A, Latchoumane C, Lee S, Kim GB, Cheong E, Augustine GJ, Shin HS (2012) Optogenetically induced sleep spindle rhythms alter sleep architectures in mice. Proc Natl Acad Sci U S A 109(50):20673–20678. doi:10.1073/pnas.1217897109
Paz JT, Davidson TJ, Frechette ES, Delord B, Parada I, Peng K, Deisseroth K, Huguenard JR (2013) Closed-loop optogenetic control of thalamus as a tool for interrupting seizures after cortical injury. Nat Neurosci 16(1):64–70. doi:10.1038/nn.3269
Bender F, Gorbati M, Cadavieco MC, Denisova N, Gao X, Holman C, Korotkova T, Ponomarenko A (2015) Theta oscillations regulate the speed of locomotion via a hippocampus to lateral septum pathway. Nat Commun 6:8521. doi:10.1038/ncomms9521
Duan AR, Varela C, Zhang Y, Shen Y, Xiong L, Wilson MA, Lisman J (2015) Delta frequency optogenetic stimulation of the thalamic nucleus reuniens is sufficient to produce working memory deficits: relevance to schizophrenia. Biol Psychiatry 77(12):1098–1107. doi:10.1016/j.biopsych.2015.01.020
Unal G, Joshi A, Viney TJ, Kis V, Somogyi P (2015) Synaptic targets of medial septal projections in the hippocampus and extrahippocampal cortices of the mouse. J Neurosci 35(48):15812–15826. doi:10.1523/JNEUROSCI.2639-15.2015
Buzsaki G, Leung LW, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287(2):139–171
Zhang F, Gradinaru V, Adamantidis AR, Durand R, Airan RD, de Lecea L, Deisseroth K (2010) Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat Protoc 5(3):439–456, nprot.2009.226
Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI (2010) Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2. Nat Protoc 5(2):247–254, nprot.2009.228
Yizhar O, Fenno LE, Davidson TJ, Mogri M, Deisseroth K (2011) Optogenetics in neural systems. Neuron 71(1):9–34. doi:10.1016/j.neuron.2011.06.004
Tye KM, Deisseroth K (2012) Optogenetic investigation of neural circuits underlying brain disease in animal models. Nat Rev Neurosci 13(4):251–266. doi:10.1038/nrn3171
Hangya B, Borhegyi Z, Szilagyi N, Freund TF, Varga V (2009) GABAergic neurons of the medial septum lead the hippocampal network during theta activity. J Neurosci 29(25):8094–8102. doi:10.1523/JNEUROSCI.5665-08.2009
Herrera CG, Cadavieco MC, Jego S, Ponomarenko A, Korotkova T, Adamantidis A (2016) Hypothalamic feedforward inhibition of thalamocortical network controls arousal and consciousness. Nat Neurosci 19:290. doi:10.1038/nn.4209
Lubenov EV, Siapas AG (2009) Hippocampal theta oscillations are travelling waves. Nature 459(7246):534–539. doi:10.1038/nature08010
Mattis J, Tye KM, Ferenczi EA, Ramakrishnan C, O’Shea DJ, Prakash R, Gunaydin LA, Hyun M, Fenno LE, Gradinaru V, Yizhar O, Deisseroth K (2012) Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins. Nat Methods 9(2):159–172. doi:10.1038/nmeth.1808
Berndt A, Yizhar O, Gunaydin LA, Hegemann P, Deisseroth K (2009) Bi-stable neural state switches. Nat Neurosci 12(2):229–234. doi:10.1038/nn.2247
Ren J, Qin C, Hu F, Tan J, Qiu L, Zhao S, Feng G, Luo M (2011) Habenula “cholinergic” neurons co-release glutamate and acetylcholine and activate postsynaptic neurons via distinct transmission modes. Neuron 69(3):445–452. doi:10.1016/j.neuron.2010.12.038
Stuber GD, Sparta DR, Stamatakis AM, van Leeuwen WA, Hardjoprajitno JE, Cho S, Tye KM, Kempadoo KA, Zhang F, Deisseroth K, Bonci A (2011) Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475(7356):377–380. doi:10.1038/nature10194
Kim SY, Adhikari A, Lee SY, Marshel JH, Kim CK, Mallory CS, Lo M, Pak S, Mattis J, Lim BK, Malenka RC, Warden MR, Neve R, Tye KM, Deisseroth K (2013) Diverging neural pathways assemble a behavioural state from separable features in anxiety. Nature 496(7444):219–223. doi:10.1038/nature12018
Lobo MK, Covington HE 3rd, Chaudhury D, Friedman AK, Sun H, Damez-Werno D, Dietz DM, Zaman S, Koo JW, Kennedy PJ, Mouzon E, Mogri M, Neve RL, Deisseroth K, Han MH, Nestler EJ (2010) Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 330(6002):385–390. doi:10.1126/science.1188472
Bass CE, Grinevich VP, Kulikova AD, Bonin KD, Budygin EA (2013) Terminal effects of optogenetic stimulation on dopamine dynamics in rat striatum. J Neurosci Methods 214(2):149–155. doi:10.1016/j.jneumeth.2013.01.024
Royer S, Zemelman BV, Losonczy A, Kim J, Chance F, Magee JC, Buzsaki G (2012) Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat Neurosci 15(5):769–775, nn.3077
Wu F, Stark E, Ku PC, Wise KD, Buzsaki G, Yoon E (2015) Monolithically integrated muLEDs on silicon neural probes for high-resolution optogenetic studies in behaving animals. Neuron 88(6):1136–1148. doi:10.1016/j.neuron.2015.10.032
Ung K, Arenkiel BR (2012) Fiber-optic implantation for chronic optogenetic stimulation of brain tissue. J Vis Exp (68):e50004. doi: 10.3791/50004
Vandecasteele M, M S, Royer S, Belluscio M, Berenyi A, Diba K, Fujisawa S, Grosmark A, Mao D, Mizuseki K, Patel J, Stark E, Sullivan D, Watson B, Buzsaki G (2012) Large-scale recording of neurons by movable silicon probes in behaving rodents. J Vis Exp (61):e3568. doi: 10.3791/3568
Hazan L, Zugaro M, Buzsaki G (2006) Klusters, NeuroScope, NDManager: a free software suite for neurophysiological data processing and visualization. J Neurosci Methods 155(2):207–216
Hasselmo ME, Hay J, Ilyn M, Gorchetchnikov A (2002) Neuromodulation, theta rhythm and rat spatial navigation. Neural Netw 15(4-6):689–707
Kaifosh P, Lovett-Barron M, Turi GF, Reardon TR, Losonczy A (2013) Septo-hippocampal GABAergic signaling across multiple modalities in awake mice. Nat Neurosci 16(9):1182–1184. doi:10.1038/nn.3482
Frank LM, Stanley GB, Brown EN (2004) Hippocampal plasticity across multiple days of exposure to novel environments. J Neurosci 24(35):7681–7689. doi:10.1523/JNEUROSCI.1958-04.2004
Kramis RC, Routtenberg A (1977) Dissociation of hippocampal EEG from its behavioral correlates by septal and hippocampal electrical stimulation. Brain Res 125(1):37–49
Buzsaki G (2002) Theta oscillations in the hippocampus. Neuron 33(3):325–340
Grosenick L, Marshel JH, Deisseroth K (2015) Closed-loop and activity-guided optogenetic control. Neuron 86(1):106–139. doi:10.1016/j.neuron.2015.03.034
Fenno LE, Mattis J, Ramakrishnan C, Hyun M, Lee SY, He M, Tucciarone J, Selimbeyoglu A, Berndt A, Grosenick L, Zalocusky KA, Bernstein H, Swanson H, Perry C, Diester I, Boyce FM, Bass CE, Neve R, Huang ZJ, Deisseroth K (2014) Targeting cells with single vectors using multiple-feature Boolean logic. Nat Methods 11(7):763–772. doi:10.1038/nmeth.2996
Acknowledgements
We thank Franziska Bender, Maria Gorbati, Marta Carus, Xiaojie Gao, and Suzanne van der Veldt for their valuable contributions to the results and protocols described here. This work was supported by the Deutsche Forschungsgemeinschaft (DFG; Exc 257 NeuroCure, TK and AP; SPP1665, AP), The Human Frontier Science Program (HFSP; RGY0076/2012, TK), and The German-Israeli Foundation for Scientific Research and Development (GIF; I-1326-421.13/2015, TK).
Author information
Authors and Affiliations
Corresponding authors
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer Science+Business Media New York
About this protocol
Cite this protocol
Korotkova, T., Ponomarenko, A. (2017). Optogenetic Manipulations of Neuronal Network Oscillations: Combination of Optogenetics and Electrophysiological Recordings in Behaving Mice. In: Philippu, A. (eds) In Vivo Neuropharmacology and Neurophysiology. Neuromethods, vol 121. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-6490-1_4
Download citation
DOI: https://doi.org/10.1007/978-1-4939-6490-1_4
Published:
Publisher Name: Humana Press, New York, NY
Print ISBN: 978-1-4939-6488-8
Online ISBN: 978-1-4939-6490-1
eBook Packages: Springer Protocols