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Hippocampal Sharp Wave/Ripple Complexes—Physiology and Mechanisms

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Abstract

Hippocampal sharp wave/ripple complexes (SWRs) are rhythmic electrographic activities that appear strictly coupled with resting behavioral waking states of the brain and slow-wave sleep. Several lines of evidence now support their involvement in the formation and long-term consolidation of hippocampus-dependent memories. During SWRs, the hippocampal networks experience a sharp and transient (~50–100 ms) increase in neuronal activity that is temporally coherent across both hippocampi; further, sharp wave-associated ripple oscillations express a remarkably high oscillation frequency of ~120–250 cycles per second; finally, SWRs are irregular in occurrence. Despite around three decades of research into the mechanistic underpinnings of this phenomenon, a coherent theory of various aspects—e.g. its initiation and termination, and the precise synchronization of thousands of neurons at millisecond precision––is still unavailable. Here, we will outline the current understanding of the implications and the mechanisms that govern SWRs, from both a physiological and a network-theoretical perspective. We will put special emphasis on the contributing neuronal populations and will discuss unresolved aspects.

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References

  • Aivar P, Valero M, Bellistri E, Menendez de la Prida L (2014) Extracellular calcium controls the expression of two different forms of ripple-like hippocampal oscillations. J Neurosci 34:2989–3004

    Article  PubMed  Google Scholar 

  • Andersen P, Løyning Y (1962) Interaction of various afferents on CA1 neurons and dentate granule cells. Colloq Int CNRS 107:23–45

    Google Scholar 

  • Ariav G, Polsky A, Schiller J (2003) Submillisecond precision of the input-output transformation function mediated by fast sodium dendritic spikes in basal dendrites of CA1 pyramidal neurons. J Neurosci 23:7750–7758

    PubMed  Google Scholar 

  • Arszovszki A, Borhegyi Z, Klausberger T (2014) Three axonal projection routes of individual pyramidal cells in the ventral CA1 hippocampus. Front Neuroanat 8:53

    Article  PubMed  PubMed Central  Google Scholar 

  • Axmacher N, Elger CE, Fell J (2008) Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain 131:1806–1817

    Article  PubMed  Google Scholar 

  • Bähner F, Weiss EK, Birke G, Maier N, Schmitz D, Rudolph U, Frotscher M, Traub RD, Both M, Draguhn A (2011) Cellular correlate of assembly formation in oscillating hippocampal networks in vitro. Proc Natl Acad Sci U S A 108:E607–E616

    Article  PubMed  PubMed Central  Google Scholar 

  • Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JP, Jonas P (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc Natl Acad Sci U S A 99:13222–13227

    Article  PubMed  PubMed Central  Google Scholar 

  • Battaglia FP, Sutherland GR, McNaughton BL (2004) Hippocampal sharp wave bursts coincide with neocortical “up-state” transitions. Learn Mem 11:697–704

    Article  PubMed  PubMed Central  Google Scholar 

  • Bazelot M, Telenczuk MT, Miles R (2016) Single CA3 pyramidal cells trigger sharp waves in vitro by exciting interneurones. J Physiol 594:2565–2577

    Google Scholar 

  • Behrens CJ, van den Boom LP, de Hoz L, Friedman A, Heinemann U (2005) Induction of sharp wave-ripple complexes in vitro and reorganization of hippocampal networks. Nat Neurosci 8:1560–1567

    Article  PubMed  Google Scholar 

  • Bragin A, Engel JJ, Wilson CL, Fried I, Buzsáki G (1999) High-frequency oscillations in human brain. Hippocampus 9:137–142

    Article  PubMed  Google Scholar 

  • Brunel N, Wang X-J (2003) What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. J Neurophysiol 90:415–430

    Article  PubMed  Google Scholar 

  • Butler JL, Paulsen O (2015) Hippocampal network oscillations – recent insights from in vitro experiments. Curr Opin Neurobiol 31:40–44

    Google Scholar 

  • Buzsáki G (1986) Hippocampal sharp waves: their origin and significance. Brain Res 398:242–252

    Article  PubMed  Google Scholar 

  • Buzsáki G (1989) Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience 31:551–570

    Article  PubMed  Google Scholar 

  • Buzsáki G (2006) Rhythms of the brain. Oxford University Press, Inc. Oxford, New York

    Google Scholar 

  • Buzsáki G (2015) Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus 25:1073–1188

    Article  PubMed  PubMed Central  Google Scholar 

  • Buzsáki G, Chrobak JJ (1995) Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neurobiol 5:504–510

    Article  PubMed  Google Scholar 

  • Buzsáki G, Moser EI (2013) Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16:130–138

    Article  PubMed  PubMed Central  Google Scholar 

  • Buzsáki G, Leung L-WS, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287:139–171

    Article  Google Scholar 

  • Buzsáki G, Horváth Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025–1027

    Article  PubMed  Google Scholar 

  • Buzsáki G, Buhl DL, Harris KD, Csicsvari J, Czéh B, Morozov A (2003) Hippocampal network patterns of activity in the mouse. Neuroscience 116:201–211

    Article  PubMed  Google Scholar 

  • Chenkov N, Sprekeler H, Kempter R (2017) Memory replay in balanced recurrent networks. PLOS Comp Biol (under review)

    Google Scholar 

  • Chrobak JJ, Buzsáki G (1994) Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. J Neurosci 14:6160–6170

    PubMed  Google Scholar 

  • Chrobak JJ, Buzsáki G (1996) High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci 16:3056–3066

    PubMed  Google Scholar 

  • Ciocchi S, Passecker J, Malagon-Vina H, Mikus N, Klausberger T (2015) Selective information routing by ventral hippocampal CA1 projection neurons. Science 348:560–563

    Article  PubMed  Google Scholar 

  • Colgin LL (2016) Rhythms of the hippocampal network. Nat Rev Neurosci 17:239–249

    Article  PubMed  Google Scholar 

  • Csicsvari J, Hirase H, Czurkó A, Mamiya A, Buzsáki G (1999) Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat. J Neurosci 19:274–287

    PubMed  Google Scholar 

  • Csicsvari J, Hirase H, Mamiya A, Buzsáki G (2000) Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28:585–594

    Article  PubMed  Google Scholar 

  • Cunningham MO, Roopun A, Schofield IS, Whittaker RG, Duncan R, Russell A, Jenkins A, Nicholson C, Whittington MA, Traub RD (2012) Glissandi: transient fast electrocorticographic oscillations of steadily increasing frequency, explained by temporally increasing gap junction conductance. Epilepsia 53:1205–1214

    Article  PubMed  PubMed Central  Google Scholar 

  • Deuchars J, Thomson AM (1996) CA1 pyramid-pyramid connections in rat hippocampus in vitro: dual intracellular recordings with biocytin filling. Neuroscience 74:1009–1018

    PubMed  Google Scholar 

  • Donoso JR, Maier N, Schmitz D, Kempter R (2017) Hippocampal ripple oscillations and inhibition-first network models (in preparation)

    Google Scholar 

  • Draguhn A, Traub RD, Schmitz D, Jefferys JGR (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394:189–192

    Article  PubMed  Google Scholar 

  • Dur-e-Ahmad M, Nicola W, Campbell SA, Skinner FK (2012) Network bursting using experimentally constrained single compartment CA3 hippocampal neuron models with adaptation. J Comput Neurosci 33:21–40

    Article  PubMed  Google Scholar 

  • Ego-Stengel V, Wilson MA (2010) Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20:1–10

    PubMed  PubMed Central  Google Scholar 

  • Ellender TJ, Nissen W, Colgin LL, Mann EO, Paulsen O (2010) Priming of hippocampal population bursts by individual perisomatic-targeting interneurons. J Neurosci 30:5979–5991

    Article  PubMed  PubMed Central  Google Scholar 

  • English DF, Peyrache A, Stark E, Roux L, Vallentin D, Long MA, Buzsáki G (2014) Excitation and inhibition compete to control spiking during hippocampal ripples: Intracellular study in behaving mice. J Neurosci 34:16509–16517

    Article  PubMed  PubMed Central  Google Scholar 

  • Eschenko O, Ramadan W, Mölle M, Born J, Sara SJ (2008) Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning. Learn Mem 15:222–228

    Article  PubMed  PubMed Central  Google Scholar 

  • Fano S, Çalişkan G, Heinemann U (2012) Differential effects of blockade of ERG channels on gamma oscillations and excitability in rat hippocampal slices. Eur J Neurosci 36:3628–3635

    Article  PubMed  Google Scholar 

  • Gasparini S, Magee JC (2006) State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. J Neurosci 26:2088–2100

    Article  PubMed  Google Scholar 

  • Gasparini S, Migliore M, Magee JC (2004) On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J Neurosci 24:11046–11056

    Article  PubMed  Google Scholar 

  • Girardeau G, Zugaro M (2011) Hippocampal ripples and memory consolidation. Curr Opin Neurobiol 21:452–459

    Article  PubMed  Google Scholar 

  • Girardeau G, Benchenane K, Wiener SI, Buzsáki G, Zugaro MB (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci 12:1222–1223

    Article  PubMed  Google Scholar 

  • Girardeau G, Cei A, Zugaro M (2014) Learning-induced plasticity regulates hippocampal sharp wave-ripple drive. J Neurosci 34:5176–5183

    Article  PubMed  Google Scholar 

  • Goutagny R, Jackson J, Williams S (2009) Self-generated theta oscillations in the hippocampus. Nat Neurosci 12:1491–1493

    Article  PubMed  Google Scholar 

  • Graves AR, Moore SJ, Bloss EB, Mensh BD, Kath WL, Spruston N (2012) Hippocampal pyramidal neurons comprise two distinct cell types that are countermodulated by metabotropic receptors. Neuron 76:776–789

    Article  PubMed  PubMed Central  Google Scholar 

  • Gulyás AI, Freund TT (2015) Generation of physiological and pathological high frequency oscillations: The role of perisomatic inhibition in sharp-wave ripple and interictal spike generation. Curr Opin Neurobiol 31:26–32

    Article  PubMed  Google Scholar 

  • Hájos N, Karlócai MR, Németh B, Ulbert I, Monyer H, Szabó G, Erdélyi F, Freund TF, Gulyás AI (2013) Input-output features of anatomically identified CA3 neurons during hippocampal sharp wave/ripple oscillation in vitro. J Neurosci 33:11677–11691

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasselmo ME (1999) Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3:351–359

    Article  PubMed  Google Scholar 

  • Hebb DO (1949) The organization of behavior. Wiley, New York

    Google Scholar 

  • Hofer KT, Kandrács Á, Ulbert I, Pál I, Szabó C, Héja L, Wittner L (2015) The hippocampal CA3 region can generate two distinct types of sharp wave-ripple complexes, in vitro. Hippocampus 25:169–186

    Article  PubMed  Google Scholar 

  • Hollnagel JO, Maslarova A, ul Haq R, Heinemann U (2014) GABAB receptor dependent modulation of sharp wave-ripple complexes in the rat hippocampus in vitro. Neurosci Lett 574:15–20

    Article  PubMed  Google Scholar 

  • Hulse BK, Moreaux LC, Lubenov EV, Siapas AG (2016) Membrane potential dynamics of CA1 pyramidal neurons during hippocampal ripples in awake mice. Neuron 89:800–813

    Google Scholar 

  • Ishikawa D, Matsumoto N, Sakaguchi T, Matsuki N, Ikegaya Y (2014) Operant conditioning of synaptic and spiking activity patterns in single hippocampal neurons. J Neurosci 34:5044–5053

    Article  PubMed  Google Scholar 

  • Isomura Y, Sirota A, Özen S, Montgomery S, Mizuseki K, Henze DA, Buzsáki G (2006) Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 52:871–882

    Article  PubMed  Google Scholar 

  • Jadhav SP, Kemere C, German PW, Frank LM (2012) Awake hippocampal sharp-wave ripples support spatial memory. Science 336:1454–1458

    Google Scholar 

  • Jadhav SP, Rothschild G, Roumis DK, Frank LM (2016) Coordinated excitation and inhibition of prefrontal ensembles during awake hippocampal sharp-wave ripple events. Neuron 90:113–127

    Google Scholar 

  • Jahnke S, Timme M, Memmesheimer R (2015) A unified dynamic model for learning, replay, and sharp-wave/ripples. J Neurosci 35:16236–16258

    Google Scholar 

  • Jefferys JGR, Menendez de la Prida L, Wendling F, Bragin A, Avoli M, Timofeev I, Lopes da Silva FH (2012) Mechanisms of physiological and epileptic HFO generation. Prog Neurobiol 98:250–264

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanamori N (1985) A spindle-like wave in the cat hippocampus: a novel vigilance level-dependent electrical activity. Brain Res 334:180–182

    Google Scholar 

  • Karlócai MR, Kohus Z, Káli S, Ulbert I, Szabó G, Máté Z, Freund TF, Gulyás AI (2014) Physiological sharp wave-ripples and interictal events in vitro: what’s the difference? Brain 137:463–485

    Google Scholar 

  • Katona L, Lapray D, Viney TJ, Oulhaj A, Borhegyi Z, Micklem BR, Klausberger T, Somogyi P (2014) Sleep and movement differentiates actions of two types of somatostatin-expressing GABAergic interneuron in rat hippocampus. Neuron 82:872–886

    Article  PubMed  PubMed Central  Google Scholar 

  • King C, Henze DA, Leinekugel X, Buzsáki G (1999) Hebbian modification of a hippocampal population pattern in the rat. J Physiol 521:159–167

    Article  PubMed  PubMed Central  Google Scholar 

  • Kirov SA, Petrak LJ, Fiala JC, Harris KM (2004) Dendritic spines disappear with chilling but proliferate excessively upon rewarming of mature hippocampus. Neuroscience 127:69–80

    Article  PubMed  Google Scholar 

  • Klausberger T, Magill PJ, Márton LF, Roberts JDB, Cobden PM, Buzsáki G, Somogyi P (2003) Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844–848

    Article  PubMed  Google Scholar 

  • Klausberger T, Márton LF, Baude A, Roberts JDB, Magill PJ, Somogyi P (2004) Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci 7:41–47

    Article  PubMed  Google Scholar 

  • Klausberger T, Marton LF, O’Neill J, Huck JHJ, Dalezios Y, Fuentealba P, Suen WY, Papp E, Kaneko T, Watanabe M, Csicsvari J, Somogyi P (2005) Complementary roles of cholecystokinin- and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations. J Neurosci 25:9782–9793

    Article  PubMed  Google Scholar 

  • Kohus Z, Káli S, Rovira L, Schlingloff D, Papp O, Freund TF, Hájos N, Gulyás AI (2016) Properties and dynamics of inhibitory synaptic communication within the CA3 microcircuits of pyramidal cells and interneurons expressing parvalbumin or cholecystokinin. J Physiol 594:3745–3774

    Google Scholar 

  • Koniaris E, Drimala P, Sotiriou E, Papatheodoropoulos C (2011) Different effects of zolpidem and diazepam on hippocampal sharp wave-ripple activity in vitro. Neuroscience 175:224–234

    Article  PubMed  Google Scholar 

  • Kouvaros S, Kotzadimitriou D, Papatheodoropoulos C (2015) Hippocampal sharp waves and ripples: effects of aging and modulation by NMDA receptors and L-type Ca2+ channels. Neuroscience 298:26–41

    Article  PubMed  Google Scholar 

  • Lapray D, Lasztoczi B, Lagler M, Viney TJ, Katona L, Valenti O, Hartwich K, Borhegyi Z, Somogyi P, Klausberger T (2012) Behavior-dependent specialization of identified hippocampal interneurons. Nat Neurosci 15:1265–1271

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee AK, Wilson MA (2002) Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36:1183–1194

    Article  PubMed  Google Scholar 

  • Lee SH, Marchionni I, Bezaire M, Varga C, Danielson N, Lovett-Barron M, Losonczy A, Soltesz I (2014) Parvalbumin-positive basket cells differentiate among hippocampal pyramidal cells. Neuron 82:1129–1144

    Article  PubMed  PubMed Central  Google Scholar 

  • Leung LWS, Lopes da Silva FH, Wadman WJ (1982) Spectral characteristics of the hippocampal EEG in the freely moving rat. Electroencephalogr Clin Neurophysiol 54:203–219

    Article  PubMed  Google Scholar 

  • Logothetis NK, Eschenko O, Murayama Y, Augath M, Steudel T, Evrard HC, Besserve M, Oeltermann A (2013) Hippocampal-cortical interaction during periods of subcortical silence. Nature 491:547–553

    Article  Google Scholar 

  • Maex R, De Schutter E (2003) Resonant synchronization in heterogeneous networks of inhibitory neurons. J Neurosci 23:10503–10514

    PubMed  Google Scholar 

  • Maier N, Nimmrich V, Draguhn A (2003) Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices. J Physiol 550:873–887

    Article  PubMed  PubMed Central  Google Scholar 

  • Maier N, Morris G, Johenning FW, Schmitz D (2009) An approach for reliably investigating hippocampal sharp wave-ripples in vitro. PLoS ONE 4:e6925

    Article  Google Scholar 

  • Maier N, Tejero-Cantero Á, Dorrn AL, Winterer J, Beed PS, Morris G, Kempter R, Poulet JFA, Leibold C, Schmitz D (2011) Coherent phasic excitation during hippocampal ripples. Neuron 72:137–152

    Article  PubMed  Google Scholar 

  • Maier N, Morris G, Schuchmann S, Korotkova T, Ponomarenko A, Böhm C, Wozny C, Schmitz D (2012) Cannabinoids disrupt hippocampal sharp wave-ripples via inhibition of glutamate release. Hippocampus 22:1350–1362

    Article  PubMed  Google Scholar 

  • Malik R, Dougherty KA, Parikh K, Byrne C, Johnston D (2015) Mapping the electrophysiological and morphological properties of CA1 pyramidal neurons along the longitudinal hippocampal axis. Hippocampus 26:341–361

    Google Scholar 

  • Marshall L, Helgadóttir H, Mölle M, Born J (2006) Boosting slow oscillations during sleep potentiates memory. Nature 444:610–613

    Article  PubMed  Google Scholar 

  • Martin SJ, Grimwood PD, Morris RGM (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649–711

    Google Scholar 

  • McNaughton BL, Morris RGM (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415

    Article  Google Scholar 

  • Memmesheimer RM (2010) Quantitative prediction of intermittent high-frequency oscillations in neural networks with supralinear dendritic interactions. Proc Natl Acad Sci U S A 107:11092–11097

    Article  PubMed  PubMed Central  Google Scholar 

  • Mercer A, Bannister AP, Thomson AM (2006) Electrical coupling between pyramidal cells in adult cortical regions. Brain Cell Biol 35:13–27

    Article  PubMed  Google Scholar 

  • Nakashiba T, Young JZ, McHugh TJ, Buhl DL, Tonegawa S (2008) Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning. Science 319:1260–1264

    Article  PubMed  Google Scholar 

  • Nakashiba T, Buhl DL, McHugh TJ, Tonegawa S (2009) Hippocampal CA3 output is crucial for ripple-associated reactivation and consolidation of memory. Neuron 62:781–787

    Article  PubMed  PubMed Central  Google Scholar 

  • Ngo HV, Martinetz T, Born J, Mölle M (2013) Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. Neuron 78:545–553

    Article  PubMed  Google Scholar 

  • Nguyen DP, Kloosterman F, Barbieri R, Brown EN, Wilson MA (2009) Characterizing the dynamic frequency structure of fast oscillations in the rodent hippocampus. Front Integr Neurosci 3:11

    Article  PubMed  PubMed Central  Google Scholar 

  • Nicole O, Hadzibegovic S, Gajda J, Bontempi B, Bem T, Meyrand P (2016) Soluble amyloid beta oligomers block the learning-induced increase in hippocampal sharp wave-ripple rate and impair spatial memory formation. Sci Rep 6:22728

    Article  PubMed  PubMed Central  Google Scholar 

  • Nimmrich V, Maier N, Schmitz D, Draguhn A (2005) Induced sharp wave-ripple complexes in the absence of synaptic inhibition in mouse hippocampal slices. J Physiol 563:663–670

    Article  PubMed  PubMed Central  Google Scholar 

  • Nokia MS, Penttonen M, Wikgren J (2010) Hippocampal ripple-contingent training accelerates trace eyeblink conditioning and retards extinction in rabbits. J Neurosci 30:11486–11492

    Article  PubMed  Google Scholar 

  • O’Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171–175

    Article  PubMed  Google Scholar 

  • O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, Oxford

    Google Scholar 

  • O’Neill J, Senior T, Csicsvari J (2006) Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 49:143–155

    Article  PubMed  Google Scholar 

  • Omura Y, Carvalho XMM, Inokuchi K, Fukai XT (2015) A lognormal recurrent network model for burst generation during hippocampal sharp waves. J Neurosci 35:14585–14601

    Article  PubMed  Google Scholar 

  • Pangalos M, Donoso JR, Winterer J, Zivkovic AR, Kempter R, Maier N, Schmitz D (2013) Recruitment of oriens-lacunosum-moleculare interneurons during hippocampal ripples. Proc Natl Acad Sci U S A 110:4398–4403

    Article  PubMed  PubMed Central  Google Scholar 

  • Papatheodoropoulos C (2008) A possible role of ectopic action potentials in the in vitro hippocampal sharp wave-ripple complexes. Neuroscience 157:495–501

    Article  PubMed  Google Scholar 

  • Papatheodoropoulos C, Kostopoulos G (2002) Spontaneous, low frequency (~2–3 Hz) field activity generated in rat ventral hippocampal slices perfused with normal medium. Brain Res Bull 57:187–193

    Article  PubMed  Google Scholar 

  • Papatheodoropoulos C, Sotiriou E, Kotzadimitriou D, Drimala P (2007) At clinically relevant concentrations the anaesthetic/amnesic thiopental but not the anticonvulsant phenobarbital interferes with hippocampal sharp wave-ripple complexes. BMC Neurosci 8:60

    Article  PubMed  PubMed Central  Google Scholar 

  • Patel J, Schomburg EW, Berényi A, Fujisawa S, Buzsáki G (2013) Local generation and propagation of ripples along the septotemporal axis of the hippocampus. J Neurosci 33:17029–17041

    Google Scholar 

  • Pietersen ANJ, Patel N, Jefferys JGR, Vreugdenhil M (2009) Comparison between spontaneous and kainate-induced gamma oscillations in the mouse hippocampus in vitro. Eur J Neurosci 29:2145–2156

    Article  PubMed  Google Scholar 

  • Ponomarenko AA, Knoche A, Korotkova TM, Haas HL (2003) Aminergic control of high-frequency (~200 Hz) network oscillations in the hippocampus of the behaving rat. Neurosci Lett 348:101–104

    Article  PubMed  Google Scholar 

  • Ponomarenko AA, Korotkova TM, Sergeeva OA, Haas HL (2004) Multiple GABAA receptor subtypes regulate hippocampal ripple oscillations. Eur J Neurosci 20:2141–2148

    Article  PubMed  Google Scholar 

  • Ramirez-Villegas JF, Logothetis NK, Besserve M (2015) Diversity of sharp-wave-ripple LFP signatures reveals differentiated brain-wide dynamical events. Proc Natl Acad Sci U S A 112:E6379-6387

    Google Scholar 

  • Robbe D, Montgomery SM, Thome A, Rueda-Orozco PE, McNaughton BL, Buzsáki G (2006) Cannabinoids reveal importance of spike timing coordination in hippocampal function. Nat Neurosci 9:1526–1533

    Google Scholar 

  • Routtenberg A (1968) Hippocampal correlates of consummatory and observed behavior. Physiol Behav 3:533–535

    Article  Google Scholar 

  • Sadowski JHLP, Jones MW, Mellor JR (2016) Sharp-wave ripples orchestrate the induction of synaptic plasticity during reactivation of place cell firing patterns in the hippocampus. Cell Rep 14:1916–1929

    Article  PubMed  PubMed Central  Google Scholar 

  • Sainsbury RS (1970) Hippocampal activity during natural behavior in the guinea pig. Physiol Behav 5:317–324

    Article  PubMed  Google Scholar 

  • Schlingloff D, Káli S, Freund TF, Hájos N, Gulyás AI (2014) Mechanisms of sharp wave initiation and ripple generation. J Neurosci 34:11385–11398

    Article  PubMed  Google Scholar 

  • Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez E, Dermietzel R, Heinemann U, Traub RD (2001) Axo-axonal coupling: a novel mechanism for ultrafast neuronal communication. Neuron 31:831–840

    Article  PubMed  Google Scholar 

  • Shein-Idelson M, Ondracek JM, Liaw H, Reiter S, Laurent G (2016) Slow waves, sharp waves, ripples, and REM in sleeping dragons. Science 352:590–595

    Article  PubMed  Google Scholar 

  • Siapas AG, Wilson MA (1998) Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21:1123–1128

    Article  PubMed  Google Scholar 

  • Simon A, Traub RD, Vladimirov N, Jenkins A, Nicholson C, Whittaker RG, Schofield I, Clowry GJ, Cunningham MO, Whittington MA (2014) Gap junction networks can generate both ripple-like and fast ripple-like oscillations. Eur J Neurosci 39:46–60

    Article  PubMed  Google Scholar 

  • Skaggs WE, McNaughton BL, Permenter M, Archibeque M, Vogt J, Amaral DG, Barnes CA (2007) EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. J Neurophysiol 98:898–910

    Google Scholar 

  • Sirota A, Csicsvari J, Buhl D, Buzsáki G (2003) Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci U S A 100:2065–2069

    Article  PubMed  PubMed Central  Google Scholar 

  • Somogyi P (1977) A specific “axo-axonal” interneuron in the visual cortex of the rat. Brain Res 136:345–350

    Article  PubMed  Google Scholar 

  • Somogyi P, Katona L, Klausberger T, Lasztóczi B, Viney TJ (2014) Temporal redistribution of inhibition over neuronal subcellular domains underlies state-dependent rhythmic change of excitability in the hippocampus. Philos Trans R Soc Lond B Biol Sci 369:20120518

    Article  PubMed  PubMed Central  Google Scholar 

  • Stark E, Roux L, Eichler R, Senzai Y, Royer S, Buzsáki G (2014) Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations. Neuron 83:467–480

    Article  PubMed  PubMed Central  Google Scholar 

  • Stumpf C (1965) The fast component in the electrical activity of rabbit’s hippocampus. Electroencephalogr Clin Neurophysiol 18:477–486

    Article  PubMed  Google Scholar 

  • Suh J, Foster DJ, Davoudi H, Wilson MA, Tonegawa S (2013) Impaired hippocampal ripple-associated replay in a mouse model of schizophrenia. Neuron 80:484–493

    Article  PubMed  Google Scholar 

  • Sullivan D, Csicsvari J, Mizuseki K, Montgomery S, Diba K, Buzsáki G (2011) Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity. J Neurosci 31:8605–8616

    Article  PubMed  PubMed Central  Google Scholar 

  • Suzuki SS, Smith GK (1987) Spontaneous EEG spikes in the normal hippocampus. I. Behavioral correlates, laminar profiles and bilateral synchrony. Electroencephalogr Clin Neurophysiol 67:348–359

    Article  PubMed  Google Scholar 

  • Suzuki SS, Smith GK (1988) Spontaneous EEG spikes in the normal hippocampus. V. Effects of ether, urethane, pentobarbital, atropine, diazepam and bicuculline. Electroencephalogr Clin Neurophysiol 70:84–95

    Article  PubMed  Google Scholar 

  • Szabó GG, Holderith N, Gulyás AI, Freund TF, Hájos N (2010) Distinct synaptic properties of perisomatic inhibitory cell types and their different modulation by cholinergic receptor activation in the CA3 region of the mouse hippocampus. Eur J Neurosci 31:2234–2246

    Article  PubMed  PubMed Central  Google Scholar 

  • Takeuchi T, Duszkiewicz AJ, Morris RGM (2014) The synaptic plasticity and memory hypothesis: encoding, storage and persistence. Philos Trans R Soc Lond B Biol Sci 369:20130288

    Article  PubMed  PubMed Central  Google Scholar 

  • Taxidis J, Coombes S, Mason R, Owen MR (2012) Modeling sharp wave-ripple complexes through a CA3-CA1 network model with chemical synapses. Hippocampus 22:995–1017

    Article  PubMed  Google Scholar 

  • Taxidis J, Mizuseki K, Mason R, Owen MR (2013) Influence of slow oscillation on hippocampal activity and ripples through cortico-hippocampal synaptic interactions, analyzed by a cortical-CA3-CA1 network model. Front Comput Neurosci 7:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Thome C, Kelly T, Yanez A, Schultz C, Engelhardt M, Cambridge SB, Both M, Draguhn A, Beck H, Egorov AV (2014) Axon-carrying dendrites convey privileged synaptic input in hippocampal neurons. Neuron 83:1418–1430

    Article  PubMed  Google Scholar 

  • Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55:189–208

    Article  PubMed  Google Scholar 

  • Traub RD, Bibbig A (2000) A model of high-frequency ripples in the hippocampus based on synaptic coupling plus axon-axon gap junctions between pyramidal neurons. J Neurosci 20:2086–2093

    Google Scholar 

  • Traub RD, Whittington MA (2010) Cortical oscillations in health and disease. Oxford University Press, Oxford

    Book  Google Scholar 

  • Traub RD, Wong RKS (1982) Cellular mechanism of neuronal synchronization in epilepsy. Science 216:745–747

    Google Scholar 

  • Traub RD, Schmitz D, Jefferys JGR, Draguhn A (1999) High-frequency population oscillations are predicted to occur in hippocampal pyramidal neuronal networks interconnected by axoaxonal gap junctions. Neuroscience 92:407–426

    Article  PubMed  Google Scholar 

  • ul Haq R, Anderson ML, Hollnagel JO, Worschech F, Sherkheli MA, Behrens CJ, Heinemann U (2016) Serotonin dependent masking of hippocampal sharp wave ripples. Neuropharmacology 101:188–203

    Article  PubMed  Google Scholar 

  • Ulanovsky N, Moss CF (2007) Hippocampal cellular and network activity in freely moving echolocating bats. Nat Neurosci 10:224–233

    Article  PubMed  Google Scholar 

  • Valero M, Cid E, Averkin RG, Aguilar J, Sanchez-Aguilera A, Viney TJ, Gomez-Dominguez D, Bellistri E, de la Prida LM (2015) Determinants of different deep and superficial CA1 pyramidal cell dynamics during sharp-wave ripples. Nat Neurosci 18:1281–1290

    Article  PubMed  PubMed Central  Google Scholar 

  • Vandecasteele M, Varga V, Berényi A, Papp E, Barthó P, Venance L, Freund TF, Buzsáki 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 111:13535–13540

    Article  PubMed  PubMed Central  Google Scholar 

  • Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407–418

    Article  PubMed  Google Scholar 

  • Varga C, Golshani P, Soltesz I (2012) Frequency-invariant temporal ordering of interneuronal discharges during hippocampal oscillations in awake mice. Proc Natl Acad Sci U S A 109:E2726–E2734

    Article  PubMed  PubMed Central  Google Scholar 

  • Varga C, Oijala M, Lish J, Szabo GG, Bezaire M, Marchionni I, Golshani P, Soltesz I (2014) Functional fission of parvalbumin interneuron classes during fast network events. eLife 3:e04006

    Google Scholar 

  • Viereckel T, Kostic M, Bähner F, Draguhn A, Both M (2013) Effects of the GABA-uptake blocker NNC-711 on spontaneous sharp wave-ripple complexes in mouse hippocampal slices. Hippocampus 23:323–329

    Article  PubMed  Google Scholar 

  • Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676–679

    Google Scholar 

  • Witton J, Staniaszek LE, Bartsch U, Randall AD, Jones MW, Brown JT (2014) Disrupted hippocampal sharp-wave ripple-associated spike dynamics in a transgenic mouse model of dementia. J Physiol 594:4615–4630

    Google Scholar 

  • Wu C, Shen H, Luk WP, Zhang L (2002) A fundamental oscillatory state of isolated rodent hippocampus. J Physiol 540:509–527

    Article  PubMed  PubMed Central  Google Scholar 

  • Ylinen A, Bragin A, Nádasdy Z, Jandó G, Szabó I, Sik A, Buzsáki G (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15:30–46

    PubMed  Google Scholar 

  • Yoshii N, Shimokochi M, Miyamoto K, Ito M (1966) Studies on the neural basis of behavior by continuous frequency analysis of EEG. Prog Brain Res 21:217–250

    Article  PubMed  Google Scholar 

  • Zhang L, Sheppy E, Wu C (2006) Regulation of hippocampal sharp waves by Ca2+-dependent slow after hyperpolarization. Crit Rev Neurobiol 18:159–167

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank Aarti Swaminathan, André Holzbecher, Barbara Imbrosci, Benedikt Salmen, Dietmar Schmitz, José Donoso, Nikolay Chenkov, Roberta Evangelista and Roger D. Traub for helpful comments on the manuscript.

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Maier, N., Kempter, R. (2017). Hippocampal Sharp Wave/Ripple Complexes—Physiology and Mechanisms. In: Axmacher, N., Rasch, B. (eds) Cognitive Neuroscience of Memory Consolidation. Studies in Neuroscience, Psychology and Behavioral Economics. Springer, Cham. https://doi.org/10.1007/978-3-319-45066-7_14

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