Ripples are brief (<150 ms) high-frequency oscillatory neural activities in the brain with a range of 140 to 200 Hz in rodents and 80 to 140 Hz in humans. Ripples are regarded as playing an essential role in several aspects of memory function, mainly in the hippocampus. This type of ripple generally occurs with sharp waves and is called a sharp-wave ripple (SPW-R). Extensive research of SPW-Rs in the rodent brain while actively awake has also linked the function of these SPW-Rs to navigation and decision making. Although many studies with rodents unveiled SPW-R function, research in humans on this subject is still sparse. Therefore, unveiling SPW-R function in the human hippocampus is warranted. A certain type of ripples may also be a biomarker of epilepsy. This type of ripple is called a pathological ripple (p-ripple). p-ripples have a wider range of frequency (80-500 Hz) than SPW-Rs, and the range of frequency is especially higher in brain regions that are intrinsically linked to epilepsy onset. Brain regions producing ripples are too small for scalp electrode recording, and intracranial recording is typically needed to detect ripples. In addition, SPW-Rs in the human hippocampus have been recorded from patients with epilepsy who may have p-ripples. Differentiating SPW-Rs and p-ripples is often not easy. We need to develop more sophisticated methods to record SPW-Rs to differentiate them from p-ripples. This paper reviews the general features and roles of ripple waves.
YlinenABraginANadasdyZ, et al.Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci. 1995;15(1 Pt 1):30-46.
2.
BuzsakiGBuhlDLHarrisKDCsicsvariJCzehBMorozovA. Hippocampal network patterns of activity in the mouse. Neuroscience. 2003;116(1):201-211.
3.
BuzsakiGLeungLWVanderwolfCH. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 1983;287(2):139-171.
4.
BuzsakiGHorvathZUriosteRHetkeJWiseK. High-frequency network oscillation in the hippocampus. Science. 1992;256(5059):1025-1027.
5.
ZelmannRLinaJMSchulze-BonhageAGotmanJJacobsJ. Scalp EEG is not a blur: it can see high frequency oscillations although their generators are small. Brain Topogr. 2014;27(5):683-704.
6.
BuzsakiG. Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus. 2015;25(10):1073-1188.
7.
BraginAEngelJJrWilsonCLFriedIBuzsakiG. High-frequency oscillations in human brain. Hippocampus. 1999;9(2):137-142.
8.
Le Van QuyenMBraginAStabaRCreponBWilsonCLEngelJJr. Cell type-specific firing during ripple oscillations in the hippocampal formation of humans. J Neurosci. 2008;28(24):6104-6110.
9.
StabaRJBraginA. High-frequency oscillations and other electrophysiological biomarkers of epilepsy: underlying mechanisms. Biomark Med. 2011;5(5):545-556.
10.
StabaRJ. Normal and pathologic high-frequency oscillations. In: NoebelsJLAvoliMRogawskiMAOlsenRWDelgado-EscuetaAV, eds. Jasper's Basic Mechanisms of the Epilepsies. National Center for Biotechnology Information; 2012:285-302.
11.
KuhnkeNSchwindJDumpelmannMMaderMSchulze-BonhageAJacobsJ. High frequency oscillations in the ripple band (80–250 Hz) in scalp EEG: higher density of electrodes allows for better localization of the seizure onset zone. Brain Topogr. 2018;31(6):1059-1072.
12.
von EllenriederNFrauscherBDubeauFGotmanJ. Interaction with slow waves during sleep improves discrimination of physiologic and pathologic high-frequency oscillations (80–500 Hz). Epilepsia. 2016;57(6):869-878.
13.
Menendez de la PridaLStabaRJDianJA. Conundrums of high-frequency oscillations (80–800 Hz) in the epileptic brain. J Clin Neurophysiol. 2015;32(3):207-219.
14.
NavarreteMAlvarado-RojasCLe Van QuyenMValderramaM. RIPPLELAB: a comprehensive application for the detection, analysis and classification of high frequency oscillations in electroencephalographic signals. PLoS One. 2016;11(6):e0158276.
15.
CanoltyRTEdwardsEDalalSS, et al.High gamma power is phase-locked to theta oscillations in human neocortex. Science. 2006;313(5793):1626-1628.
16.
ChrobakJJBuzsakiG. High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J Neurosci. 1996;16(9):3056-3066.
17.
CsicsvariJHiraseHCzurkoAMamiyaABuzsakiG. Fast network oscillations in the hippocampal CA1 region of the behaving rat. J Neurosci. 1999;19(16):RC20.
18.
NormanYYeagleEMKhuvisSHarelMMehtaADMalachR. Hippocampal sharp-wave ripples linked to visual episodic recollection in humans. Science. 2019;365(6454):650-657.
19.
JooHRFrankLM. The hippocampal sharp wave-ripple in memory retrieval for immediate use and consolidation. Nat Rev Neurosci. 2018;19(12):744-757.
20.
LeonardTKHoffmanKL. Sharp-wave ripples in primates are enhanced near remembered visual objects. Curr Biol. 2017;27(2):257-262.
21.
LeonardTKMikkilaJMEskandarEN, et al.Sharp wave ripples during visual exploration in the primate hippocampus. J Neurosci. 2015;35(44):14771-14782.
22.
CanoltyRTKnightRT. The functional role of cross-frequency coupling. Trends Cogn Sci. 2010;14(11):506-515.
23.
MooijAHFrauscherBGoemansSAMHuiskampGJMBraunKPJZijlmansM. Ripples in scalp EEGs of children: co-occurrence with sleep-specific transients and occurrence across sleep stages. Sleep. 2018;41(11):169-171.
24.
BraginAEngelJJrWilsonCLFriedIMathernGW. Hippocampal and entorhinal cortex high-frequency oscillations (100–500 Hz) in human epileptic brain and in kainic acid-treated rats with chronic seizures. Epilepsia. 1999;40(2):127-137.
25.
Alvarado-RojasCHuberfeldGBaulacM, et al.Different mechanisms of ripple-like oscillations in the human epileptic subiculum. Ann Neurol. 2015;77(2):281-290.
26.
StabaRJWilsonCLBraginAFriedIEngelJJr. Quantitative analysis of high-frequency oscillations (80–500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J Neurophysiol. 2002;88(4):1743-1752.
27.
OchiAOtsuboHDonnerEJ, et al.Dynamic changes of ictal high-frequency oscillations in neocortical epilepsy: using multiple band frequency analysis. Epilepsia. 2007;48(2):286-296.
28.
JacobsJLeVanPChanderRHallJDubeauFGotmanJ. Interictal high-frequency oscillations (80–500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain. Epilepsia. 2008;49(11):1893-1907.
29.
Andrade-ValencaLPDubeauFMariFZelmannRGotmanJ. Interictal scalp fast oscillations as a marker of the seizure onset zone. Neurology. 2011;77(6):524-531.
30.
van KlinkNEvan ‘t KloosterMALeijtenFSJacobsJBraunKPZijlmansM. Ripples on rolandic spikes: a marker of epilepsy severity. Epilepsia. 2016;57(7):1179-1189.
31.
BuzsakiG. Two-stage model of memory trace formation: a role for “noisy” brain states. Neuroscience. 1989;31(3):551-570.
32.
BuzsakiG. The hippocampo-neocortical dialogue. Cereb Cortex. 1996;6(2):81-92.
33.
HoffmanKLBattagliaFPHarrisKMacLeanJNMarshallLMehtaMR. The upshot of up states in the neocortex: from slow oscillations to memory formation. J Neurosci. 2007;27(44):11838-11841.
34.
BattagliaFPBenchenaneKSirotaAPennartzCMWienerSI. The hippocampus: hub of brain network communication for memory. Trends Cogn Sci. 2011;15(7):310-318.
35.
McClellandJLMcNaughtonBLO’ReillyRC. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev. 1995;102(3):419-457.
36.
LogothetisNKEschenkoOMurayamaY, et al.Hippocampal-cortical interaction during periods of subcortical silence. Nature. 2012;491(7425):547-553.
37.
WilsonMAMcNaughtonBL. Reactivation of hippocampal ensemble memories during sleep. Science. 1994;265(5172):676-679.
38.
KudrimotiHSBarnesCAMcNaughtonBL. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci. 1999;19(10):4090-4101.
39.
CsicsvariJHiraseHMamiyaABuzsakiG. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron. 2000;28(2):585-594.
40.
FosterDJWilsonMA. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature. 2006;440(7084):680-683.
41.
JiDWilsonMA. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci. 2007;10(1):100-107.
42.
PeyracheAKhamassiMBenchenaneKWienerSIBattagliaFP. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat Neurosci. 2009;12(7):919-926.
43.
BenchenaneKPeyracheAKhamassiM, et al.Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron. 2010;66(6):921-936.
44.
Ego-StengelVWilsonMA. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus. 2010;20(1):1-10.
RothschildGEbanEFrankLM. A cortical-hippocampal-cortical loop of information processing during memory consolidation. Nat Neurosci. 2017;20(2):251-259.
47.
RajasethupathyPSankaranSMarshelJH, et al.Projections from neocortex mediate top-down control of memory retrieval. Nature. 2015;526(7575):653-659.
48.
DavidsonTJKloostermanFWilsonMA. Hippocampal replay of extended experience. Neuron. 2009;63(4):497-507.
49.
WuCTHaggertyDKemereCJiD. Hippocampal awake replay in fear memory retrieval. Nat Neurosci. 2017;20(4):571-580.
50.
GirardeauGInemaIBuzsakiG. Reactivations of emotional memory in the hippocampus-amygdala system during sleep. Nat Neurosci. 2017;20(11):1634-1642.
51.
StaresinaBPBergmannTOBonnefondM, et al.Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep. Nat Neurosci. 2015;18(11):1679-1686.
52.
O’NeillJSeniorTCsicsvariJ. Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron. 2006;49(1):143-155.
53.
TortABKramerMAThornC, et al.Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. Proc Natl Acad Sci U S A. 2008;105(51):20517-20522.
54.
DupretDO’NeillJPleydell-BouverieBCsicsvariJ. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat Neurosci. 2010;13(8):995-1002.
JadhavSPKemereCGermanPWFrankLM. Awake hippocampal sharp-wave ripples support spatial memory. Science. 2012;336(6087):1454-1458.
57.
O’NeillJPleydell-BouverieBDupretDCsicsvariJ. Play it again: reactivation of waking experience and memory. Trends Neurosci. 2010;33(5):220-229.
58.
CarrMFJadhavSPFrankLM. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat Neurosci. 2011;14(2):147-153.
59.
GirardeauGZugaroM. Hippocampal ripples and memory consolidation. Curr Opin Neurobiol. 2011;21(3):452-459.
60.
YuJYFrankLM. Hippocampal-cortical interaction in decision making. Neurobiol Learn Mem. 2015;117:34-41.
61.
AkiyamaTMcCoyBGoCY, et al.Focal resection of fast ripples on extraoperative intracranial EEG improves seizure outcome in pediatric epilepsy. Epilepsia. 2011;52(10):1802-1811.
62.
TakagiS. Sleep and epilepsy. Sleep Biol Rhythms. 2017;15(3):189-196.
63.
WirrellEC. Prognostic significance of interictal epileptiform discharges in newly diagnosed seizure disorders. J Clin Neurophysiol. 2010;27(4):239-248.
64.
MelaniFZelmannRMariFGotmanJ. Continuous high frequency activity: a peculiar SEEG pattern related to specific brain regions. Clin Neurophysiol. 2013;124(8):1507-1516.
65.
StabaRJFrighettoLBehnkeEJ, et al.Increased fast ripple to ripple ratios correlate with reduced hippocampal volumes and neuron loss in temporal lobe epilepsy patients. Epilepsia. 2007;48(11):2130-2138.
66.
UrrestarazuEChanderRDubeauFGotmanJ. Interictal high-frequency oscillations (100–500 Hz) in the intracerebral EEG of epileptic patients. Brain. 2007;130(Pt 9):2354-2366.
67.
JacobsJZijlmansMZelmannR, et al.High-frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery. Ann Neurol. 2010;67(2):209-220.
68.
WuJYSankarRLernerJTMatsumotoJHVintersHVMathernGW. Removing interictal fast ripples on electrocorticography linked with seizure freedom in children. Neurology. 2010;75(19):1686-1694.
69.
WangSWangIZBulacioJC, et al.Ripple classification helps to localize the seizure-onset zone in neocortical epilepsy. Epilepsia. 2013;54(2):370-376.
70.
PailMHalamekJDanielP, et al.Intracerebrally recorded high frequency oscillations: simple visual assessment versus automated detection. Clin Neurophysiol. 2013;124(10):1935-1942.
71.
JacobsJVogtCLeVanPZelmannRGotmanJKobayashiK. The identification of distinct high-frequency oscillations during spikes delineates the seizure onset zone better than high-frequency spectral power changes. Clin Neurophysiol. 2016;127(1):129-142.
72.
KobayashiKAkiyamaTOkaMEndohFYoshinagaH. A storm of fast (40–150 Hz) oscillations during hypsarrhythmia in West syndrome. Ann Neurol. 2015;77(1):58-67.
73.
KobayashiKOkaMAkiyamaT, et al.Very fast rhythmic activity on scalp EEG associated with epileptic spasms. Epilepsia. 2004;45(5):488-496.
74.
ChaitanyaGSinhaSNarayananMSatishchandraP. Scalp high frequency oscillations (HFOs) in absence epilepsy: an independent component analysis (ICA) based approach. Epilepsy Res. 2015;115:133-140.
75.
KobayashiKYoshinagaHTodaYInoueTOkaMOhtsukaY. High-frequency oscillations in idiopathic partial epilepsy of childhood. Epilepsia. 2011;52(10):1812-1819.
76.
KobayashiKWatanabeYInoueTOkaMYoshinagaHOhtsukaY. Scalp-recorded high-frequency oscillations in childhood sleep-induced electrical status epilepticus. Epilepsia. 2010;51(10):2190-2194.
77.
BagshawAPJacobsJLeVanPDubeauFGotmanJ. Effect of sleep stage on interictal high-frequency oscillations recorded from depth macroelectrodes in patients with focal epilepsy. Epilepsia. 2009;50(4):617-628.
78.
StabaRJWilsonCLBraginAJhungDFriedIEngelJJr. High-frequency oscillations recorded in human medial temporal lobe during sleep. Ann Neurol. 2004;56(1):108-115.
