Skip to main content
SpringerLink
Log in
Book cover

Space,Time and Memory in the Hippocampal Formation pp 303–350Cite as

The Function of Oscillations in the Hippocampal Formation

  • Chapter
  • First Online:

Abstract

Some of the strongest experimental and computational links between oscillations and cognition concern the oscillations in the hippocampal formation supporting spatial and mnemonic processing. We review experimental and theoretical work concerning well-established hippocampal oscillations such as theta, gamma, and high-frequency ripples and how they relate to spatial, mnemonic, and anxiety-related representation and behaviour. We specifically consider the following computational roles for oscillations: organising processing into discrete chunks, as seen in encoding versus retrieval scheduling; ordinal and metric coding by oscillatory phase; temporal integration by oscillatory phase; and interregional communication. The literature on oscillations has typically been concerned with changes in band-specific power. Here, focusing on the theta oscillation, we summarise how key variables are linked not only to power but also to frequency and to coherence. We conclude that the hippocampal formation provides an invaluable model system for understanding the functional roles of neuronal oscillations and the interaction between oscillations.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Addante RJ, Watrous AJ, Yonelinas AP, Ekstrom AD, Ranganath C (2011) Prestimulus theta activity predicts correct source memory retrieval. Proc Natl Acad Sci U S A 108:10702–10707

    CAS  PubMed Central  PubMed  Google Scholar 

  • Adhikari A, Topiwala MA, Gordon JA (2010) Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 65:257–269

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ahmed OJ, Mehta MR (2012) Running speed alters the frequency of hippocampal gamma oscillations. J Neurosci 32(21):7373–7383

    CAS  PubMed Central  PubMed  Google Scholar 

  • Anderson KL, Rajagovindan R, Ghacibeh GA, Meador KJ, Ding M (2010) Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. Cereb Cortex 20(7):1604–1612

    PubMed  Google Scholar 

  • Arnolds DE, Lopes da Silva FH, Aitink JW, Kamp A, Boeijinga P (1980) The spectral properties of hippocampal EEG related to behaviour in man. Electroencephalogr Clin Neurophysiol 50:324–328

    CAS  PubMed  Google Scholar 

  • Averbeck BB, Chafee MV, Crowe DA, Georgopoulos AP (2002) Parallel processing of serial movements in prefrontal cortex. Proc Natl Acad Sci U S A 99(20):13172–13177

    CAS  PubMed Central  PubMed  Google Scholar 

  • Axmacher N, Mormann F, Fernández G, Elger CE, Fell J (2006) Memory formation by neuronal synchronization. Brain Res Rev 52:170–182

    PubMed  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

    PubMed  Google Scholar 

  • Axmacher N, Cohen MX, Fell J, Haupt S, Dümpelmann M, Elger CE, Schlaepfer TE, Lenartz D, Sturm V, Ranganath C (2010a) Intracranial EEG correlates of expectancy and memory formation in the human hippocampus and nucleus accumbens. Neuron 65(4):541–549

    CAS  PubMed  Google Scholar 

  • Axmacher N, Henseler M, Jensen O, Weinreich I, Elger C, Fell J (2010b) Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc Natl Acad Sci U S A 107:3228–3233

    CAS  PubMed Central  PubMed  Google Scholar 

  • Babiloni C, Vecchio F, Mirabella G, Buttiglione M, Sebastiano F, Picardi A, Di Gennaro G, Quarato PP, Grammaldo LG, Buffo P, Esposito V, Manfredi M, Cantore G, Eusebi F (2009) Hippocampal, amygdala, and neocortical synchronization of theta rhythms is related to an immediate recall during rey auditory verbal learning test. Hum Brain Mapp 30(7):2077–2089

    PubMed  Google Scholar 

  • Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T, Zhang WN, Pothuizen HH, Feldon J (2004) Regional dissociations within the hippocampus–memory and anxiety. Neurosci Biobehav Rev 28:273–283

    CAS  PubMed  Google Scholar 

  • Barbeau E, Wendling F, Regis J, Duncan R, Poncet M, Chauvel P, Bartolomei F (2005) Recollection of vivid memories after perirhinal region stimulations: synchronization in the theta range of spatially distributed brain areas. Neuropsychologia 43(9):1329–1337

    PubMed  Google Scholar 

  • Barry C, Hayman R, Burgess N, Jeffery KJ (2007) Experience-dependent rescaling of entorhinal grids. Nat Neurosci 10(6):682–684

    CAS  PubMed  Google Scholar 

  • Barry C, Ginzberg LL, O’Keefe J, Burgess N (2012) Grid cell firing patterns signal environmental novelty by expansion. Proc Natl Acad Sci U S A 109(43):17687–17692

    CAS  PubMed Central  PubMed  Google Scholar 

  • Battaglia FP, Benechenane K, Sirota A, Pennartz CM, Wiener SI (2011) The hippocampus: hub of brain network communication for memory. Trends Cogn Sci 7:310–318

    Google Scholar 

  • Belluscio MA, Mizuseki K, Buzsaki G et al (2012) Cross-frequency phase–phase coupling between theta and gamma oscillations in the hippocampus. J Neurosci 32(2):423–435

    CAS  PubMed Central  PubMed  Google Scholar 

  • Benchenane K, Peyrache A, Khamassi M, Tierney PL, Gioanni Y, Battaglia FP, Wiener SI (2010) Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning. Neuron 66:921–936

    CAS  PubMed  Google Scholar 

  • Berke JD, Hetrick V, Breck J, Greene RW (2008) Transient 23–30 Hz oscillations in mouse hippocampus during exploration of novel environments. Hippocampus 18(5):519–529

    PubMed  Google Scholar 

  • Blair HT, Fanselow MS (2014) Fear and memory: a view of the hippocampus through the lens of the amygdala. In: Derdikman D, Knierim JJ (eds) Space, time & memory in the hippocampal formation. Springer, Heidelberg

    Google Scholar 

  • Blair HT, Gupta K, Zhang K (2008) Conversion of a phase- to a rate-coded position signal by a three-stage model of theta cells, grid cells, and place cells. Hippocampus 18(12):1239–1255

    PubMed Central  PubMed  Google Scholar 

  • Bland BH, Oddie SD (2001) Theta band oscillation and synchrony in the hippocampal formation and associated structures: the case for its role in sensorimotor integration. Behav Brain Res 127(1–2):119–136

    CAS  PubMed  Google Scholar 

  • Bland BH, Derie-Gillespie D, Mestek P, Jackson J, Crooks R, Cormican A (2007) To move or not: previous experience in a runway avoidance task determines the appearance of hippocampal Type 2 sensory processing theta. Behav Brain Res 16(179):299–304

    Google Scholar 

  • Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G (1995) Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47–60

    CAS  PubMed  Google Scholar 

  • Bragin A, Engel J Jr, Wilson CL, Fried I, Buzsaki G (1999) High-frequency oscillations in human brain. Hippocampus 9(2):137–142

    CAS  PubMed  Google Scholar 

  • Brandon MP, Bogaard AR, Libby CP, Connerney MA, Gupta K, Hasselmo ME (2011) Reduction of theta rhythm dissociates grid cell periodicity from directional tuning. Science 332:595–599

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brankack J, Steward M, Fox SE (1993) Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators. Brain Res 615(2):310–327

    CAS  PubMed  Google Scholar 

  • Buckner RL, Carroll DC (2007) Self-projection and the brain. Trends Cogn Sci 11(2):49–57

    PubMed  Google Scholar 

  • Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain’s default network: anatomy, function, and relevance to disease. Ann NY Acad Sci 1124:1–38

    PubMed  Google Scholar 

  • Bullock D (2004) Adaptive neural models of queuing and timing in fluent action. Trends Cogn Sci 8:427–435

    Google Scholar 

  • Burak Y, Fiete IR (2008) Accurate path integration in continuous attractor network models of grid cells. PLoS Comput Biol 5(2):e1000291

    Google Scholar 

  • Burgess N (2008) Grid cells and theta as oscillatory interference: theory and predictions. Hippocampus 18:1157–1174

    PubMed Central  PubMed  Google Scholar 

  • Burgess N, Hitch GJ (1992) Towards a network model of the articulatory loop. J Mem Lang 31:429–460

    Google Scholar 

  • Burgess N, O’Keefe J (2011) Models of place and grid cell firing and theta rhythmicity. Curr Opin Neurobiol 21(5):734–744

    CAS  PubMed Central  PubMed  Google Scholar 

  • Burgess N, O’Keefe J, Recce M (1993) Using hippocampal ‘place cells’ for navigation, exploiting phase coding. Adv Neural Inf Process Syst 5:929–936

    Google Scholar 

  • Burgess N, Recce M, O’Keefe J (1994) A model of hippocampal function. Neural Netw 7(6–7):1065–1081

    Google Scholar 

  • Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35(4):625–641

    CAS  PubMed  Google Scholar 

  • Burgess N, Barry C, Jeffery KJ, O’Keefe J (2005) A grid and place cell model of path integration utilizing phase precession versus theta. In: Computational cognitive neuroscience conference 2005 poster, Washington, DC. [http://posters.f1000.com/PosterList?posterID=225]

  • Burgess N, Barry C, O’Keefe J (2007) An oscillatory interference model of grid cell firing. Hippocampus 17:801–812

    PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Buzsaki G (1989) 2-stage model of memory trace formation - a role for noisy brain states. Neuroscience 31(3):551–570

    CAS  PubMed  Google Scholar 

  • Buzsaki G (2002) Theta oscillations in the hippocampus. Neuron 33:325–340

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304(5679):1926–1929

    CAS  PubMed  Google Scholar 

  • Buzsaki G, Logothetis N, Singer W (2013) Scaling brain size, keeping timing. Evolutionary preservation of brain rhythms. Neuron 80(3):751–764

    CAS  PubMed  Google Scholar 

  • Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313:1626–1628

    CAS  PubMed Central  PubMed  Google Scholar 

  • Carr MF, Karlsson MP, Frank LM (2012) Transient slow gamma synchrony underlies hippocampal memory replay. Neuron 75(4):700–713

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cashdollar N, Malecki U, Rugg-Gunn FJ, Duncan JS, Lavie N, Duzel E (2009) Hippocampus-dependent and -independent theta-networks of active maintenance. Proc Natl Acad Sci U S A 106:20493–20498

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen G, King JA, Burgess N, O’Keefe J (2013) How vision and movement combine in the hippocampal place code. Proc Natl Acad Sci USA 110(1):378–383

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cheung A, Vickerstaff R (2010) Finding the way with a noisy brain. PLoS Comput Biol 6(11):e1000992

    PubMed Central  PubMed  Google Scholar 

  • Chrobak JJ, Buzsaki G (1998) Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18(1):388–398

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Cornwell BR, Johnson LL, Holroyd T, Carver FW, Grillon C (2008) Human hippocampal and parahippocampal theta during goal-directed spatial navigation predicts performance on a virtual Morris water maze. J Neurosci 28(23):5983–5990

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cornwell BR, Salvadore G, Colon-Rosario V, Latov DR, Holroyd T, Carver FW, Coppola R, Manji HK, Zarate CA Jr, Grillon C (2010) Abnormal hippocampal functioning and impaired spatial navigation in depressed individuals: evidence from whole-head magnetoencephalography. Am J Psychiatry 167(7):836–844

    PubMed Central  PubMed  Google Scholar 

  • Cornwell BR, Arkin N, Overstreet C, Carver FW, Grillon C (2012) Distinct contributions of human hippocampal theta to spatial cognition and anxiety. Hippocampus 22:1848–1859

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Dayan P, Hinton GE, Neal RM, Zemel RS (1995) The Helmholtz machine. Neural Comput 7(5):889–904

    CAS  PubMed  Google Scholar 

  • de Araujo DB, Baffa O, Wakai RT (2002) Theta oscillations and human navigation: a magnetoencephalography study. J Cogn Neurosci 14:70–78

    PubMed  Google Scholar 

  • Douchamps V, Jeewajee A, Blundell P, Burgess N, Lever C (2013) Evidence for encoding vs retrieval scheduling by theta phase and acetylcholine. J Neurosci 33:8689–8704

    CAS  PubMed Central  PubMed  Google Scholar 

  • Douglas RJ (1969) Hippocampal theta and disinhibition: a counterreply. Psychol Rev 24:583–586

    CAS  Google Scholar 

  • Easton A, Douchamps V, Eacott M, Lever C (2012) A specific role for septohippocampal acetylcholine in memory? Neuropsychologia 50(13):3156–3168

    PubMed Central  PubMed  Google Scholar 

  • Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I (2003) Cellular networks underlying human spatial navigation. Nature 425(6954):184–188

    CAS  PubMed  Google Scholar 

  • Ekstrom AD, Caplan JB, Ho E, Shattuck K, Fried I, Kahana MJ (2005) Human hippocampal theta activity during virtual navigation. Hippocampus 2005(15):881–889

    Google Scholar 

  • Engel J Jr, Bragin A, Staba R, Mody I (2009) High-frequency oscillations: what is normal and what is not? Epilepsia 50(4):598–604

    PubMed  Google Scholar 

  • Engin E, Treit D (2007) The role of hippocampus in anxiety: intracerebral infusion studies. Behav Pharmacol 18:365–374

    CAS  PubMed  Google Scholar 

  • Engin E, Stellbrink J, Treit D, Dickson CT (2008) Anxiolytic and antidepressant effects of intracerebroventricularly administered somatostatin: behavioural and neurophysiological evidence. Neuroscience 157:666–676

    CAS  PubMed  Google Scholar 

  • Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7–19

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fell J, Klaver P, Lehnertz K, Grunwald T, Schaller C, Elger CE, Fernández G (2001) Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat Neurosci 4:1259–1264

    CAS  PubMed  Google Scholar 

  • Fell J, Klaver P, Elfadil H, Schaller C, Elger CE, Fernández G (2003) Rhinal-hippocampal theta coherence during declarative memory formation: interaction with gamma synchronization? Eur J Neurosci 17:1082–1088

    PubMed  Google Scholar 

  • Fell J, Ludowig E, Rosburg T, Axmacher N, Elger CE (2008) Phase-locking within human mediotemporal lobe predicts memory formation. Neuroimage 43(2):410–419

    PubMed  Google Scholar 

  • Fell J, Ludowig E, Staresina BP, Wagner T, Kranz T, Elger CE, Axmacher N (2011) Medial temporal theta/alpha power enhancement precedes successful memory encoding: evidence based on intracranial EEG. J Neurosci 31:5392–5397

    CAS  PubMed  Google Scholar 

  • Fox SE, Wolfson S, Ranck JB (1986) Hippocampal theta rhythm and the firing of neurons in walking and urethane anesthetized rats. Exp Brain Res 62:495–508

    CAS  PubMed  Google Scholar 

  • Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474–480

    PubMed  Google Scholar 

  • Fries P (2009) The model- and the data-gamma. Neuron 64(5):601–602

    CAS  PubMed  Google Scholar 

  • Fuentemilla L, Penny WD, Cashdollar N, Bunzeck N, Duzel E (2010) Theta-coupled periodic replay in working memory. Curr Biol 20:606–612

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fuhs MC, Touretzky DS (2006) A spin glass model of path integration in rat medial entorhinal cortex. J Neurosci 26(16):4266–4276

    CAS  PubMed  Google Scholar 

  • Fyhn M, Hafting T, Treves A, Moser MB, Moser EI (2007) Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446(7132):190–194

    CAS  PubMed  Google Scholar 

  • Gardner-Medwin AR (1976) The recall of events through the learning of associations between their parts. Proc R Soc Lond B Biol Sci 194(1116):375–402

    CAS  PubMed  Google Scholar 

  • Geisler C, Robbe D, Zugaro M, Sirota A, Buzsaki G (2007) Hippocampal place cell assemblies are speed-controlled oscillators. Proc Natl Acad Sci U S A 104(19):8149–8154

    CAS  PubMed Central  PubMed  Google Scholar 

  • Geisler C, Diba K, Pastalkova E, Mizuseki K, Royer S, Buzsaki G (2010) Temporal delays among place cells determine the frequency of population theta oscillations in the hippocampus. Proc Natl Acad Sci U S A 107(17):7957–7962

    CAS  PubMed Central  PubMed  Google Scholar 

  • Giocomo LM, Zilli EA, Fransen E, Hasselmo ME (2007) Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 315(5819):1719–1722

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gordon JA, Lacefield CO, Kentros CG, Hen R (2005) State-dependent alterations in hippocampal oscillations in serotonin 1A receptor-deficient mice. J Neurosci 25(28):6509–6519

    CAS  PubMed  Google Scholar 

  • Gray JA (1982) The neuropsychology of anxiety: an inquiry into the functions of the septo-hippocampal system. Oxford University Press, Oxford

    Google Scholar 

  • Gray JA, McNaughton N (2000) The neuropsychology of anxiety. Oxford University Press, Oxford

    Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gray CM, König P, Engel AK, Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338(6213):334–337

    CAS  PubMed  Google Scholar 

  • Green JD, Arduini AA (1954) Hippocampal electrical activity in arousal. J Neurophysiol 17:553–557

    Google Scholar 

  • Grossberg S (1972) Neural expectation: cerebellar and retinal analogs of cells fired by learnable or unlearned pattern classes. Kybernetik 10(1):49–57

    CAS  PubMed  Google Scholar 

  • Grossberg S (2009) Beta oscillations and hippocampal place cell learning during exploration of novel environments. Hippocampus 19(9):881–885

    PubMed  Google Scholar 

  • Guderian S, Duzel E (2005) Induced theta oscillations mediate large-scale synchrony with mediotemporal areas during recollection in humans. Hippocampus 15(7):901–912

    PubMed  Google Scholar 

  • Guderian S, Schott BH, Richardson-Klavehn A, Duzel E (2009) Medial temporal theta state before an event predicts episodic encoding success in humans. Proc Natl Acad Sci U S A 106:5365–5370

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guitart-Masip M, Barnes GR, Horner A, Bauer M, Dolan RJ, Duzel E (2013) Synchronization of medial temporal lobe and prefrontal rhythms in human decision making. J Neurosci 33:442–451

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gupta K, Hasselmo ME (2014) Modulatory influences on the hippocampus and entorhinal cortex. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, Heidelberg

    Google Scholar 

  • Gupta AS, van der Meer MA, Touretzky DS, Redish AD (2012) Segmentation of spatial experience by hippocampal theta sequences. Nat Neurosci 15(7):1032–1039

    CAS  PubMed  Google Scholar 

  • Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436(7052):801–806

    CAS  PubMed  Google Scholar 

  • Hafting T, Fyhn M, Bonnevie T, Moser MB, Moser EI (2008) Hippocampus-independent phase precession in entorhinal grid cells. Nature 453(7199):1248–1252

    CAS  PubMed  Google Scholar 

  • Halgren E, Tl B, Crandall PH (1978) Human hippocampal formation EEG desynchronizes during attentiveness and movement. Electroencephalogr Clin Neurophysiol 44:778–781

    CAS  PubMed  Google Scholar 

  • Harris KD, Henze DA, Hirase H, Leinekugel X, Dragoi G, Czurko A, Buzsaki G (2002) Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417(6890):738–741

    CAS  PubMed  Google Scholar 

  • Hartley T, Burgess N, Lever C, Cacucci F, O’Keefe J (2000) Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 10(4):369–379

    CAS  PubMed  Google Scholar 

  • Harvey CD, Collman F, Dombeck DA, Tank DW (2009) Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461(7266):941–946

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hassabis D, Maguire EA (2007) Deconstructing episodic memory with construction. Trends Cogn Sci 11(7):299–306

    PubMed  Google Scholar 

  • Hasselmo ME (2008) Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting. Hippocampus 18:1213–1229

    PubMed Central  PubMed  Google Scholar 

  • Hasselmo ME (2012) How we remember: brain mechanisms of episodic memory. MIT, Cambridge, MA

    Google Scholar 

  • Hasselmo ME, Schnell E (1994) Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J Neurosci 14(6):3898–3914

    CAS  PubMed  Google Scholar 

  • Hasselmo ME, Wyble BP, Wallenstein GV (1996) Encoding and retrieval of episodic memories: role of cholinergic and GABAergic modulation in the hippocampus. Hippocampus 6:693–708

    CAS  PubMed  Google Scholar 

  • Hasselmo ME, Bodelón C, Wyble BP (2002) A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput 14(4):793–817

    PubMed  Google Scholar 

  • Hinman JR, Penley SC, Long LL, Escabí MA, Chrobak JJ (2011) Septotemporal variation in dynamics of theta: speed and habituation. J Neurophysiol 105:2675–2686

    PubMed  Google Scholar 

  • Hipp JF, Hawellek DJ, Corbetta M, Siegel M, Engel AK (2012) Large-scale cortical correlation structure of spontaneous oscillatory activity. Nat Neurosci 15(6):884–890

    CAS  PubMed  Google Scholar 

  • Hölscher C, Anwyl R, Rowan MJ (1997) Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can Be depotentiated by stimulation on the negative phase in area CA1 in vivo. J Neurosci 17(16):6470–6477

    PubMed  Google Scholar 

  • Hopfield JJ (1995) Pattern recognition computation using action potential timing for stimulus representation. Nature 376(6535):33–36

    CAS  PubMed  Google Scholar 

  • Houghton G (1990) The problem of serial order: a neural network model of sequence learning and recall. In: Dale R, Mellish C, Zock M (eds) Current research in natural language generation. Academic, London, pp 287–319

    Google Scholar 

  • Huerta PT, Lisman JE (1993) Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364(6439):723–725

    CAS  PubMed  Google Scholar 

  • Huerta PT, Lisman JE (1995) Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron 15(5):1053–1063

    CAS  PubMed  Google Scholar 

  • Huerta PT, Lisman JE (1996) Low-frequency stimulation at the troughs of theta-oscillation induces long-term depression of previously potentiated CA1 synapses. J Neurophysiol 75(2):877–884

    CAS  PubMed  Google Scholar 

  • Huxter J, Burgess N, O’Keefe J (2003) Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425(6960):828–832

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huxter JR, Senior TJ, Allen K, Csicvari J (2008) Theta phase-specific codes for two-dimensional position, trajectory and heading in the hippocampus. Nat Neurosci 11:587–594

    CAS  PubMed  Google Scholar 

  • Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME (2003) Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci 23(37):11725–11731

    CAS  PubMed  Google Scholar 

  • Hyman JM, Zilli EA, Paley AM, Hasselmo ME (2005) Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behaviour. Hippocampus 15:739–749

    PubMed  Google Scholar 

  • Ikonen S, McMahan R, Gallagher M, Eichenbaum H, Tanila H (2002) Cholinergic system regulation of spatial representation by the hippocampus. Hippocampus 12:386–397

    PubMed  Google Scholar 

  • Jacobs J, Kahana MJ (2010) Direct brain recordings fuel advances in cognitive electrophysiology. Trends Cogn Sci 14(4):162–171

    PubMed Central  PubMed  Google Scholar 

  • Jacobs J, Kahana MJ, Ekstrom AD, Mollison MV, Fried I (2010) A sense of direction in human entorhinal cortex. Proc Natl Acad Sci U S A 107:6487–6492

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jacobs J, Weidemann CT, Miller JF, Solway A, Burke JF, Wei XX, Suthana N, Sperling MR, Sharan AD, Fried I, Kahana MJ (2013) Direct recordings of grid-like neuronal activity in human spatial navigation. Nat Neurosci 16:1188–1190

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jadhav SP, Frank LM (2014) Memory replay in the hippocampus. In: Knierim JJ, Derdikman D (eds) Space, time amd memory in the hippocampal formation. Springer, Heidelberg

    Google Scholar 

  • Jadhav SP, Kemere C, German PW, Frank LM (2012) Awake hippocampal sharp-wave ripples support spatial memory. Science 336(6087):1454–1458

    CAS  PubMed  Google Scholar 

  • Jarosiewicz B, Skaggs WE (2004a) Level of arousal during the small irregular activity state in the rat hippocampal EEG. J Neurophysiol 91(6):2649–2657

    PubMed  Google Scholar 

  • Jarosiewicz B, Skaggs WE (2004b) Hippocampal place cells are not controlled by visual input during the small irregular activity in the rat. J Neurosci 24(21):5070–5077

    CAS  PubMed  Google Scholar 

  • Jarosiewicz B, McNaughton BL, Skaggs WE (2002) Hippocampal population activity during the small-amplitude irregular activity state in the rat. J Neurosci 22(4):1373–1384

    CAS  PubMed  Google Scholar 

  • Jeewajee A, Lever C, Burton S, O’Keefe J, Burgess N (2008a) Environmental novelty is signalled by reduction of the hippocampal theta frequency. Hippocampus 18(4):340–348

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jeewajee A, Barry C, O’Keefe J, Burgess N (2008b) Grid cells and theta as oscillatory interference: electrophysiological data from freely moving rats. Hippocampus 18(12):1175–1185

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jensen O, Lisman JE (1996) Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn Mem 3:279–287

    CAS  PubMed  Google Scholar 

  • Jensen O, Colgin L (2007) Cross-frequency coupling between neural oscillations. Trends Cogn Sci 11:267–269

    PubMed  Google Scholar 

  • Jensen O, Lisman JE (2000) Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding. J Neurophysiol 83(5):2602–2609

    CAS  PubMed  Google Scholar 

  • Jezek K, Henriksen EJ, Treves A, Moser EI, Moser MB (2011) Theta-paced flickering between place-cell maps in the hippocampus. Nature 478(7368):246–249

    CAS  PubMed  Google Scholar 

  • Jones MW, Wilson MA (2005) Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol 3:e402

    PubMed Central  PubMed  Google Scholar 

  • Jutras MJ, Buffalo EA (2009) Gamma-band synchronization in the macaque hippocampus and memory formation. J Neurosci 29(40):12521–12531

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jutras MJ, Buffalo EA (2010) Synchronous neural activity and memory formation. Curr Opin Neurobiol 20:150–155

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kahana MJ, Sekuler R, Caplan JB, Kirschen M, Madsen JR (1999) Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399:781–784

    CAS  PubMed  Google Scholar 

  • Kali S, Dayan P (2004) Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions. Nat Neurosci 7(3):286–294

    CAS  PubMed  Google Scholar 

  • Kaplan R, Doeller CF, Barnes GR, Litvak V, Duzel E, Bandettini PA, Burgess N (2012) Movement-related theta rhythm in humans: coordinating self-directed hippocampal learning. PLoS Biol 10:e1001267

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kentros C, Hargreaves E, Hawkins RD, Kandel ER, Shapiro M, Muller RV (1998) Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science 280(5372):2121–2126

    CAS  PubMed  Google Scholar 

  • Kjelstrup KG, Tuvnes FA, Steffenach HA, Murison R, Moser EI, Moser MB (2002) Reduced fear expression after lesions of the ventral hippocampus. Proc Natl Acad Sci U S A 99:10825–10830

    CAS  PubMed Central  PubMed  Google Scholar 

  • Klimesch W (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Rev 29(2–3):169–195

    CAS  PubMed  Google Scholar 

  • Klimesch W, Doppelmayr M, Stadler W, Pollhuber D, Sauseng P, Rohm D (2001) Episodic retrieval is reflected by a process specific increase in human electroencephalographic theta activity. Neurosci Lett 302:49–52

    CAS  PubMed  Google Scholar 

  • Koenig J, Linder AN, Leutgeb JK, Leutgeb S (2011) The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332:592–595

    CAS  PubMed  Google Scholar 

  • Kramis R, Vanderwolf CH, Bland BH (1975) Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behaviour and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp Neurol 49:58–85

    CAS  PubMed  Google Scholar 

  • Kunec S, Hasselmo ME, Kopell N (2005) Encoding and retrieval in the CA3 region of the hippocampus: a model of theta-phase separation. J Neurophysiol 94:70–82

    PubMed  Google Scholar 

  • Lakatos P, Shah AS, Knuth KH, Ulbert I, Karmos G, Schroeder CE (2005) An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory. J Neurophysiol 94(3):1904–1911

    PubMed  Google Scholar 

  • Lakatos P, Karmos G, Mehta AD, Ulbert I, Schroeder CE (2008) Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320(5872):110–113

    CAS  PubMed  Google Scholar 

  • Le Van Quyen M, Staba R, Bragin A, Dickson C, Valderrama M, Fried I, Engel J (2010) Large-scale microelectrode recordings of high-frequency gamma oscillations in human cortex during sleep. J Neurosci 30(23):7770–7782

    CAS  Google Scholar 

  • Lega BC, Jacobs J, Kahana M (2012) Human hippocampal theta oscillations and the formation of episodic memories. Hippocampus 22:748–761

    PubMed  Google Scholar 

  • Lengyel M, Szatmary Z, Erdi P (2003) Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing. Hippocampus 13(6):700–714

    PubMed  Google Scholar 

  • Leutgeb S, Leutgeb JK, Treves A, Moser MB, Moser EI (2004) Distinct ensemble coders in hippocampal areas CA3 and CA1. Science 305(5688):1295–1298

    CAS  PubMed  Google Scholar 

  • Leutgeb JK, Leutgeb S, Treves A, Meyer R, Barnes CA, McNaughton BL, Moser MB, Moser EI (2005) Progressive transformation of hippocampal neuronal representations in ‘morphed’ environments. Neuron 48(2):345–358

    CAS  PubMed  Google Scholar 

  • Lever C, Wills T, Cacucci F, Burgess N, O’Keefe J (2002) Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416(6876):90–94

    CAS  PubMed  Google Scholar 

  • Lever C, Jeewajee A, Burton S, O’Keefe J, Burgess N (2009) Hippocampal theta frequency, novelty, and behavior. Hippocampus 19:409–410

    Google Scholar 

  • Lever C, Burton S, Jeewajee A, Wills TJ, Cacucci F, Burgess N, O'Keefe J (2010) Environmental novelty elicits a later theta phase of firing in CA1 but not subiculum. Hippocampus 20(2):229–234

    PubMed Central  PubMed  Google Scholar 

  • Lisman JE, Idiart MA (1995) Storage of 7+/-2 short-term memories in oscillatory subcycles. Science 267(5203):1512–1515

    CAS  PubMed  Google Scholar 

  • Logothetis NK, Eschenko O, Murayama Y, Augath M, Steudel T, Evrard HC, Besserve M, Oeltermann A (2012) Hippocampal-cortical interaction during periods of subcortical silence. Nature 491(7425):547–553

    CAS  PubMed  Google Scholar 

  • Lubenov EV, Siapas AG (2009) Hippocampal theta oscillations are travelling waves. Nature 459(7246):534–539

    CAS  PubMed  Google Scholar 

  • Manns JR, Zilli EA, Ong KC, Hasselmo ME, Eichenbaum H (2007) Hippocampal CA1 spiking during encoding and retrieval: relation to theta phase. Neurobiol Learn Mem 87(1):9–20

    PubMed  Google Scholar 

  • Marr D (1971) Simple memory - theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262(841):23–81

    CAS  PubMed  Google Scholar 

  • Maurer AP, Cowen SL, Burke SN, Barnes CA, McNaughton BL (2006) Phase precession in hippocampal interneurons showing functional coupling to individual pyramidal cells. J Neurosci 26(52):13485–13492

    CAS  PubMed  Google Scholar 

  • McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, Lowell BB, Fanselow MS, Wilson MA, Tonegawa S (2007) Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317(5834):94–99

    CAS  PubMed  Google Scholar 

  • McNaughton BL (1983) Activity dependent modulation of hippocampal synaptic efficacy: some implications for memory processes. In: Seifert W (ed) Neurobiology of the hippocampus. Academic, New York, pp 233–251

    Google Scholar 

  • McNaughton N, Morris RG (1987) Chlordiazepoxide, an anxiolytic benzodiazepine. Impairs place navigation in rats. Behav Brain Res 24(1):39–46

    CAS  PubMed  Google Scholar 

  • McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the ‘cognitive map’. Nat Rev Neurosci 7:663–678

    CAS  PubMed  Google Scholar 

  • McNaughton N, Kocsis B, Hajos M (2007) Elicited hippocampal theta rhythm : a screen for anxiolytic and procognitive drugs through changes in hippocampal function ? Behav Pharmacol 18(5–6):329–346

    CAS  PubMed  Google Scholar 

  • Meeter M, Murre JMJ, Talamini LM (2004) Mode shifting between storage and recall based on novelty detection in oscillating hippocampal circuits. Hippocampus 14(6):722–741

    CAS  PubMed  Google Scholar 

  • Mehta MR, Lee AK, Wilson MA (2002) Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417(6890):741–746

    CAS  PubMed  Google Scholar 

  • Mitchell SJ, Ranck JB Jr (1980) Generation of theta rhythm in medial entorhinal cortex of freely moving rats. Brain Res 189(1):49–68

    CAS  PubMed  Google Scholar 

  • Mitchell DJ, McNaughton N, Flanagan D, Kirk IJ (2008) Frontal-midline theta from the perspective of hippocampal ‘theta’. Prog Neurobiol 86:156–185

    PubMed  Google Scholar 

  • Mizuseki K, Sirota A, Pastalkova E, Buzsáki G (2009) Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 64(2):267–280

    CAS  PubMed Central  PubMed  Google Scholar 

  • Montgomery SM, Sirota A, Buzsaki G (2008) Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep. J Neurosci 28(26):6731–6741

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mormann F, Osterhage H, Andrzejak RG, Weber B, Fernández G, Fell K, Elger CE, Lehnertz K (2008) Independent delta/theta rhythms in the human hippocampus and entorhinal cortex. Front Hum Neurosci 2:3

    PubMed Central  PubMed  Google Scholar 

  • Muller RU, Kubie JL (1987) The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 7(7):1951–1968

    CAS  PubMed  Google Scholar 

  • Mumford D (1994) Neuronal architectures for pattern-theoretic problems. In: Koch C, Davis J (eds) Large-scale theories of the cortex. MIT, Cambridge, MA, pp 125–152

    Google Scholar 

  • Nadasdy Z (2009) Information encoding and reconstruction from the phase of action potentials. Front Syst Neurosci 3:6

    PubMed Central  PubMed  Google Scholar 

  • Nadasdy Z (2010) Binding by asynchrony: the neuronal phase code. Front Neurosci 4

    Google Scholar 

  • Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Rodriguez Barrera V, Chittajallu R, Iwamoto KS, McBain CJ, Fanselow MS, Tonegawa S (2012) Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149(1):188–201

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nakazawa K, Sun LD, Quirk MC, Rondi-Reig L, Wilson MA, Tonegawa S (2003) Hippocampal CA3 NMDA receptors are crucial for memory acquisition of one-time experience. Neuron 38(2):305–315

    CAS  PubMed  Google Scholar 

  • Navratilova Z, Giocomo LM, Fellous JM, Hasselmo ME, McNaughton BL (2012) Phase precession and variable spatial scaling in a periodic attractor map model of medial entorhinal grid cells with realistic after-spike dynamics. Hippocampus 22(4):772–789

    PubMed  Google Scholar 

  • Nerad L, Bilkey DK (2005) Ten- to 12-Hz EEG oscillation in the rat hippocampus and rhinal cortex that is modulated by environmental familiarity. J Neurophysiol 93(3):1246–1254

    PubMed  Google Scholar 

  • O’Keefe J (2007) Hippocampal neurophysiology in the behaving animal. In: Andersen P, Morris RGM, Amaral DG, Bliss TVP, O’Keefe J (eds) The hippocampus book. Oxford Neuroscience, Oxford, pp 458–475

    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(1):171–175

    PubMed  Google Scholar 

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

    Google Scholar 

  • O’Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3(3):317–330

    PubMed  Google Scholar 

  • O’Neill J, Pleydell-Bouverie B, Dupret D, Csicsvari J (2010) Play it again: reactivation of waking experience and memory. Trends Neurosci 33(5):220–229

    PubMed  Google Scholar 

  • Oler JA, Fox AS, Shelton SE, Rogers J, Dyer TD, Davidson RJ, Shelledy W, Oakes TR, Blangero J, Kalin NH (2010) Amygdalar and hippocampal substrates of anxious temperament differ in their heritability. Nature 466:864–868

    CAS  PubMed Central  PubMed  Google Scholar 

  • Patel J, Fujisawa S, Berenyi A, Royer S, Buzsaki G (2012) Traveling theta waves along the entire septotemporal axis of the hippocampus. Neuron 75(3):410–417

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pavlides C, Greenstein YJ, Grudman M, Winson J (1988) Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439(1–2):383–387

    CAS  PubMed  Google Scholar 

  • Pentkowski NS, Blanchard DC, Lever C, Litvin Y, Blanchard RJ (2006) Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats. Eur J Neurosci 23:2185–2196

    PubMed  Google Scholar 

  • Pfeiffer BE, Foster DJ (2013) Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497:74–79

    CAS  PubMed  Google Scholar 

  • Poch C, Fuentemilla L, Barnes GR, Duzel E (2011) Hippocampal theta-phase modulation of replay correlates with configural-relational short-term memory performance. J Neurosci 31:7038–7042

    CAS  PubMed  Google Scholar 

  • Raghavachari S, Kahana MJ, Rizzuto DS, Caplan JB, Kirschen MP, Bourgeois B, Madsen JR, Lisman JE (2001) Gating of human theta oscillations by a working memory task. J Neurosci 21(9):3175–3183

    CAS  PubMed  Google Scholar 

  • Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci U S A 98(2):676–682

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ramadan W, Eschenko O, Sara SJ (2009) Hippocampal sharp wave/ripples during sleep for consolidation of associative memory. PLoS One 4:e6697

    PubMed Central  PubMed  Google Scholar 

  • Remme MW, Lengyel M, Gutkin BS (2010) Democracy-independence trade-off in oscillating dendrites and its implications for grid cells. Neuron 66(3):429–437

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rutishauser U, Ross IB, Mamelak AN, Schuman EM (2010) Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464(7290):903–907

    CAS  PubMed  Google Scholar 

  • Sainsbury RS (1998) Hippocampal theta: a sensory-inhibition theory of function. Neurosci Biobehav Rev 22(2):237–241

    CAS  PubMed  Google Scholar 

  • Sainsbury RS, Heynen A, Montoya CP (1987) Behavioral correlates of hippocampal type 2 theta in the rat. Physiol Behav 39:513–519

    CAS  PubMed  Google Scholar 

  • Sato N, Ozaki TJ, Someya Y, Anami K, Ogawa S, Mizuhara H, Yamaguchi Y (2010) Subsequent memory-dependent EEG theta correlates to parahippocampal blood oxygenation level-dependent response. Neuroreport 21(3):168–172

    PubMed  Google Scholar 

  • Sava S, Markus EJ (2008) Activation of the medial septum reverses age-related hippocampal encoding deficits: a place field analysis. J Neurosci 28(8):1841–1853

    CAS  PubMed  Google Scholar 

  • Scheffer-Teixeira R, Belchior H, Caixeta FV, Souza BC, Ribeiro S, Tort AB (2011) Theta phase modulates multiple layer-specific oscillations in the CA1 region. Cereb Cortex 22:2404–2414

    PubMed  Google Scholar 

  • Schroeder CE, Lakatos P (2009a) Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci 32:9–18

    CAS  PubMed  Google Scholar 

  • Schroeder CE, Lakatos P (2009b) The gamma oscillation: master or slave? Brain Topogr 22(1):24–26

    PubMed  Google Scholar 

  • Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20(1):11–21

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sederberg PB, Kahana MJ, Howard MW, Donner EJ, Madsen JR (2003) Theta and gamma oscillations during encoding predict subsequent recall. J Neurosci 23(34):10809–10814

    CAS  PubMed  Google Scholar 

  • Sederberg PB, Schulze-Bonhage A, Madsen JR, Bromfield EB, Mc Carthy DC, Brandt A, Tully MS, Kahana MJ (2007) Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cereb Cortex 17(5):1190–1196

    PubMed  Google Scholar 

  • Seidenbecher T, Laxmi TR, Stork O, Pape HC (2003) Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301(5634):846–850

    CAS  PubMed  Google Scholar 

  • Senior TJ, Huxter JR, Allen K, O’Neill J, Csicsvari J (2008) Gamma oscillatory firing reveals distinct populations of pyramidal cells in the CA1 region of the hippocampus. J Neurosci 28(9):2274–2286

    CAS  PubMed  Google Scholar 

  • Shapiro ML, Riceberg JS, Seip-Cammack K, Guise K (2014) Functional interactions of prefrontal cortex and the hippocampus in learning and memory. In: Derdikman D, Knierim JJ (eds) Space, time & memory in the hippocampal formation. Springer, Heidelberg

    Google Scholar 

  • Shin J, Gireesh G, Kim SW, Kim DS, Lee S, Kim YS, Watanabe M, Shin HS (2009) Phospholipase C beta 4 in the medial septum controls cholinergic theta oscillations and anxiety behaviours. J Neurosci 29(49):15375–15385

    CAS  PubMed  Google Scholar 

  • Siapas AG, Lubenov EV, Wilson MA (2005) Prefrontal phase locking to hippocampal theta oscillations. Neuron 46:141–151

    CAS  PubMed  Google Scholar 

  • Sigurdsson T et al (2010) Impaired hippocampal–prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 464:763–767

    CAS  PubMed Central  PubMed  Google Scholar 

  • Singer W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18:555–586

    CAS  PubMed  Google Scholar 

  • Siok CJ, Taylor CP, Hajos M (2009) Anxiolytic profile of pregabalin on elicited hippocampal theta oscillation. Neuropharmacology 56:379–385

    CAS  PubMed  Google Scholar 

  • 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 60:683–697

    CAS  PubMed Central  PubMed  Google Scholar 

  • Skaggs WE, McNaughton BL (1996) Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271(5257):1870–1873

    CAS  PubMed  Google Scholar 

  • Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6(2):149–172

    CAS  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(2):898–910

    PubMed  Google Scholar 

  • Sullivan D, Csicsvari J, Mizuseki K, Montgomery S, Diba K, Buzsaki G (2011) Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity. J Neurosci 31(23):8605–8616

    CAS  PubMed Central  PubMed  Google Scholar 

  • Suthana N, Haneef Z, Stern J, Mukamel R, Behnke E, Knowlton B, Fried I (2012) Memory enhancement and deep-brain stimulation of the entorhinal area. N Engl J Med 9:502–510

    Google Scholar 

  • Sutherland GR, McNaughton B (2000) Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr Opin Neurobiol 10(2):180–186

    CAS  PubMed  Google Scholar 

  • Tesche CD, Karhu J (2000) Theta oscillations index human hippocampal activation during a working memory task. Proc Natl Acad Sci U S A 97:919–924

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tort AB, Kramer MA, Thorn C, Gibson DJ, Kubota Y, Graybiel AM, Kopell NJ (2008) 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 105(51):20517–20522

    CAS  PubMed Central  PubMed  Google Scholar 

  • Treves A, Rolls ET (1994) Computational analysis of the role of the hippocampus in memory. Hippocampus 4(3):374–391

    CAS  PubMed  Google Scholar 

  • Tsodyks MV, Skaggs WE, Sejnowski TJ, McNaughton BL (1996) Population dynamics and theta rhythm phase precession of hippocampal place cell firing: a spiking neuron model. Hippocampus 6:271–280

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Vanderwolf CH (2001) The hippocampus as an olfacto-motor mechanism: were the classical anatomists right after all? Behav Brain Res 127(1–2):25–47

    CAS  PubMed  Google Scholar 

  • Vinogradova OS (2001) Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11(5):578–598

    CAS  PubMed  Google Scholar 

  • von der Malsburg C (1995) Binding in models of perception and brain function. Curr Opin Neurobiol 5(4):520–526

    PubMed  Google Scholar 

  • Von Stein A, Sarnthein J (2000) Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. Int J Psychophysiol 38(3):301–313

    Google Scholar 

  • Wang D, Buhmann J, von der Malsburg C (1990) Pattern segmentation in associative memory. Neural Comput 2(1):94–106

    Google Scholar 

  • Watrous AJ, Fried I, Ekstrom AD (2011) Behavioral correlates of human hippocampal delta and theta oscillations during navigation. J Neurophysiol 105(4):1747–1755

    PubMed  Google Scholar 

  • Watrous AJ, Tandon N, Conner CR, Pieters T, Ekstrom AD (2013a) Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval. Nat Neurosci 16(3):349–365

    CAS  PubMed Central  PubMed  Google Scholar 

  • Watrous AJ, Lee DJ, Izadi A, Gurkoff GG, Shahlaie K, Ekstrom AD (2013b) A comparative study of human and rat hippocampal low frequency oscillations during spatial navigation. Hippocampus 23:656–661

    PubMed  Google Scholar 

  • Welday AC, Shlifer IG, Bloom ML, Zhang K, Blair HT (2011) Cosine directional tuning of theta cell burst frequencies: evidence for spatial coding by oscillatory interference. J Neurosci 31(45):16157–16176

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wells CE, Amos DP, Jeewajee A, Douchamps V, Rodgers RJ, O’Keefe J, Burgess N, Lever C (2013) Novelty and anxiolytic drugs dissociate two components of hippocampal theta in behaving rats. J Neurosci 33:8650–8667

    CAS  PubMed Central  PubMed  Google Scholar 

  • Whishaw IQ, Vanderwolf CH (1971) Hippocampal EEG and behavior: effects of variation in body temperature and relation of EEG to vibrissae movement, swimming and shivering. Physiol Behav 6:391–397

    CAS  PubMed  Google Scholar 

  • Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373(6515):612–615

    CAS  PubMed  Google Scholar 

  • Wills TJ, Lever C, Cacucci F, Burgess N, O’Keefe J (2005) Attractor dynamics in the hippocampal representation of the local environment. Science 308(5723):873–876

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wills TJ, Cacucci F, Burgess N, O’Keefe J (2010) Development of the hippocampal cognitive map in preweanling rats. Science 328:1573–1576

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265(5172):676–679

    CAS  PubMed  Google Scholar 

  • Winson J (1978) Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201:160–163

    CAS  PubMed  Google Scholar 

  • Wolansky T, Clement EA, Peters SR, Palczak MA, Dickson CT (2006) Hippocampal slow oscillation: a novel EEG state and its coordination with ongoing neocortical activity. J Neurosci 26(23):6213–6229

    CAS  PubMed  Google Scholar 

  • Womelsdorf T, Fries P, Mitra PP, Desimone R (2006) Gamma-band synchronization in visual cortex predicts speed of change detection. Nature 439(7077):733–736

    CAS  PubMed  Google Scholar 

  • Yeung M, Treit D, Dickson CT (2012) A critical test of the hippocampal theta model of anxiolytic drug action. Neuropharmacology 62(1):155–160

    CAS  PubMed  Google Scholar 

  • Zhang K (1996) Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J Neurosci 16(6):2112–2126

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Psychology, University of Durham, Durham, DH1 3LE, UK

    Colin Lever

  2. Laboratory of Brain and Cognition, National Institute of Mental Health, Bethseda, MD, USA

    Raphael Kaplan

  3. UCL Institute of Cognitive Neuroscience, London, WC1N 3AR, UK

    Raphael Kaplan & Neil Burgess

  4. UCL Institute of Neurology, London, WC1N 3BG, UK

    Neil Burgess

Authors
  1. Colin Lever
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Raphael Kaplan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Neil Burgess
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Colin Lever or Neil Burgess .

Editor information

Editors and Affiliations

  1. Rappaport Faculty of Medicine, Technion- Israel Institute of Technology, Haifa, Israel

    Dori Derdikman

  2. The Solomon H. Snyder Dept. of Neurosc., John Hopkins University The Zanvyl Krieger Mind/Brain Institute, Baltimore, Maryland, USA

    James J. Knierim

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Wien

About this chapter

Cite this chapter

Lever, C., Kaplan, R., Burgess, N. (2014). The Function of Oscillations in the Hippocampal Formation. In: Derdikman, D., Knierim, J. (eds) Space,Time and Memory in the Hippocampal Formation. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1292-2_12

Download citation

Publish with us

Policies and ethics

Search

Navigation