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  • Review Article
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Rhythms of the hippocampal network

Key Points

  • The hippocampus shows three main classes of rhythms: theta (4–12 Hz), sharp wave–ripples (150–200 Hz ripples superimposed on 0.01–3 Hz sharp waves) and gamma (25–100 Hz).

  • Theta rhythm generation involves a variety of mechanisms, including theta rhythmic firing in septal and hippocampal interneurons, excitatory inputs to hippocampus and intrinsic properties of hippocampal neurons.

  • Theta rhythms are likely to be important for the formation of memories of sequences of events.

  • Sharp wave–ripple complexes are composed of two distinct network patterns: sharp waves (excitatory events that propagate from CA3 to CA1) and ripples (which reflect high frequency firing in hippocampal interneurons).

  • Accumulating evidence suggests that sharp wave–ripples are important for intrinsic hippocampal operations, including offline memory processing, retrieval of previously stored memories and planning of future behaviours.

  • The class of brain rhythms traditionally defined as gamma probably contains at least two different variants of oscillatory activity.

  • Recent findings suggest that slow (25–55 Hz) and fast (60–100 Hz) variants of gamma have different origins and may have different functions.

Abstract

The hippocampal local field potential (LFP) shows three major types of rhythms: theta, sharp wave–ripples and gamma. These rhythms are defined by their frequencies, they have behavioural correlates in several species including rats and humans, and they have been proposed to carry out distinct functions in hippocampal memory processing. However, recent findings have challenged traditional views on these behavioural functions. In this Review, I discuss our current understanding of the origins and the mnemonic functions of hippocampal theta, sharp wave–ripples and gamma rhythms on the basis of findings from rodent studies. In addition, I present an updated synthesis of their roles and interactions within the hippocampal network.

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Figure 1: Theta sequences in the hippocampus during spatial memory operations.
Figure 2: Replay during sharp wave–ripples.
Figure 3: Slow and fast gamma rhythms.

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References

  1. Quiroga, R. Q. Gnostic cells in the 21st century. Acta Neurobiol. Exp. (Wars) 73, 463–471 (2013).

    Google Scholar 

  2. Hebb, D. O. The Organization of Behavior: A Neuropsychological Theory. (Wiley, 1949).

    Google Scholar 

  3. Squire, L. R., Stark, C. E. & Clark, R. E. The medial temporal lobe. Annu. Rev. Neurosci. 27, 279–306 (2004).

    CAS  PubMed  Google Scholar 

  4. Freund, T. F. & Buzsaki, G. Interneurons of the hippocampus. Hippocampus 6, 347–470 (1996).

    CAS  PubMed  Google Scholar 

  5. Cobb, S. R., Buhl, E. H., Halasy, K., Paulsen, O. & Somogyi, P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75–78 (1995).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  7. O'Keefe, J. Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51, 78–109 (1976).

    CAS  PubMed  Google Scholar 

  8. Vanderwolf, C. H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407–418 (1969). This classic study shows that theta rhythms occur in the rat hippocampus during active movements and REM sleep.

    CAS  PubMed  Google Scholar 

  9. Buzsaki, G., Leung, L. W. & Vanderwolf, C. H. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 287, 139–171 (1983).

    CAS  PubMed  Google Scholar 

  10. Buzsaki, G. Hippocampal sharp waves: their origin and significance. Brain Res. 398, 242–252 (1986). This study describes behavioural correlates of sharp waves and explains how sharp waves in the hippocampus are generated.

    CAS  PubMed  Google Scholar 

  11. Bragin, A. et al. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 15, 47–60 (1995).

    CAS  PubMed  Google Scholar 

  12. Colgin, L. L. Mechanisms and functions of theta rhythms. Annu. Rev. Neurosci. 36, 295–312 (2013).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  14. Colgin, L. L. & Moser, E. I. Gamma oscillations in the hippocampus. Physiology (Bethesda) 25, 319–329 (2010).

    Google Scholar 

  15. Steriade, M. Grouping of brain rhythms in corticothalamic systems. Neuroscience 137, 1087–1106 (2006).

    CAS  PubMed  Google Scholar 

  16. Luthi, A. Sleep spindles: where they come from, what they do. Neuroscientist 20, 243–256 (2014).

    PubMed  Google Scholar 

  17. Jung, R. & Kornmüller, A. E. Eine Methodik der ableitung lokalisierter Potentialschwankungen aus subcorticalen Hirngebieten. Arch. Psychiat Nervenkr 109, 1–30 (1938).

    Google Scholar 

  18. Green, J. D. & Arduini, A. A. Hippocampal electrical activity in arousal. J. Neurophysiol. 17, 533–557 (1954).

    CAS  PubMed  Google Scholar 

  19. Grastyan, E., Lissak, K., Madarasz, I. & Donhoffer, H. Hippocampal electrical activity during the development of conditioned reflexes. Electroencephalogr. Clin. Neurophysiol. 11, 409–430 (1959).

    CAS  PubMed  Google Scholar 

  20. Ekstrom, A. D. et al. Human hippocampal theta activity during virtual navigation. Hippocampus 15, 881–889 (2005).

    PubMed  Google Scholar 

  21. Ulanovsky, N. & Moss, C. F. Hippocampal cellular and network activity in freely moving echolocating bats. Nat. Neurosci. 10, 224–233 (2007).

    CAS  PubMed  Google Scholar 

  22. Jutras, M. J., Fries, P. & Buffalo, E. A. Oscillatory activity in the monkey hippocampus during visual exploration and memory formation. Proc. Natl Acad. Sci. USA 110, 13144–13149 (2013).

    CAS  PubMed  Google Scholar 

  23. Mitchell, S. J. & Ranck, J. B. Generation of theta rhythm in medial entorhinal cortex of freely moving rats. Brain Res. 189, 49–66 (1980).

    CAS  PubMed  Google Scholar 

  24. Vertes, R. P., Hoover, W. B. & Viana Di Prisco, G. Theta rhythm of the hippocampus: subcortical control and functional significance. Behav. Cogn. Neurosci. Rev. 3, 173–200 (2004).

    PubMed  Google Scholar 

  25. Jones, M. W. & Wilson, M. A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol. 3, e402 (2005).

    PubMed  PubMed Central  Google Scholar 

  26. Popa, D., Duvarci, S., Popescu, A. T., Lena, C. & Pare, D. Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep. Proc. Natl Acad. Sci. USA 107, 6516–6519 (2010).

    CAS  PubMed  Google Scholar 

  27. van der Meer, M. A. & Redish, A. D. Theta phase precession in rat ventral striatum links place and reward information. J. Neurosci. 31, 2843–2854 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Freund, T. F. & Antal, M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336, 170–173 (1988). This paper shows that GABAergic cells in the medial septum project to interneurons in the hippocampus.

    CAS  PubMed  Google Scholar 

  29. Varga, V. et al. The presence of pacemaker HCN channels identifies theta rhythmic GABAergic neurons in the medial septum. J. Physiol. 586, 3893–3915 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Hangya, B., Borhegyi, Z., Szilagyi, N., Freund, T. F. & Varga, V. GABAergic neurons of the medial septum lead the hippocampal network during theta activity. J. Neurosci. 29, 8094–8102 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Robinson, R. B. & Siegelbaum, S. A. Hyperpolarization-activated cation currents: from molecules to physiological function. Annu. Rev. Physiol. 65, 453–480 (2003).

    CAS  PubMed  Google Scholar 

  32. Somogyi, P., Katona, L., Klausberger, T., Lasztoczi, B. & Viney, T. J. Temporal redistribution of inhibition over neuronal subcellular domains underlies state-dependent rhythmic change of excitability in the hippocampus. Phil. Trans. R. Soc. B 369, 20120518 (2014).

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  34. Royer, S. et al. Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat. Neurosci. 15, 769–775 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. O'Keefe, J. & Recce, M. L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317–330 (1993). This study describes the discovery of theta phase precession in hippocampal place cells.

    CAS  PubMed  Google Scholar 

  36. Skaggs, W. E., McNaughton, B. L., Wilson, M. A. & Barnes, C. A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149–172 (1996).

    CAS  PubMed  Google Scholar 

  37. Wulff, P. et al. Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proc. Natl Acad. Sci. USA 106, 3561–3566 (2009).

    CAS  PubMed  Google Scholar 

  38. Stark, E. et al. Inhibition-induced theta resonance in cortical circuits. Neuron 80, 1263–1276 (2013).

    CAS  PubMed  Google Scholar 

  39. Kamondi, A., Acsady, L., Wang, X. J. & Buzsaki, G. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 8, 244–261 (1998).

    CAS  PubMed  Google Scholar 

  40. Pernia-Andrade, A. J. & Jonas, P. Theta-gamma-modulated synaptic currents in hippocampal granule cells in vivo define a mechanism for network oscillations. Neuron 81, 140–152 (2014). In this study, whole cell recordings from dentate gyrus granule cells in vivo reveal excitatory inputs from the entorhinal cortex that are coherent with theta rhythms, as well as inhibitory currents that are coherent with gamma rhythms.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Dickson, C. T. et al. Properties and role of Ih in the pacing of subthreshold oscillations in entorhinal cortex layer II neurons. J. Neurophysiol. 83, 2562–2579 (2000).

    CAS  PubMed  Google Scholar 

  42. Hu, H., Vervaeke, K. & Storm, J. F. Two forms of electrical resonance at theta frequencies, generated by M-current, h-current and persistent Na+ current in rat hippocampal pyramidal cells. J. Physiol. 545, 783–805 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Nolan, M. F. et al. A behavioral role for dendritic integration: HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell 119, 719–732 (2004).

    CAS  PubMed  Google Scholar 

  44. Kramis, R., Vanderwolf, C. H. & Bland, B. H. Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp. Neurol. 49, 58–85 (1975).

    CAS  PubMed  Google Scholar 

  45. Nakajima, Y., Nakajima, S., Leonard, R. J. & Yamaguchi, K. Acetylcholine raises excitability by inhibiting the fast transient potassium current in cultured hippocampal neurons. Proc. Natl Acad. Sci. USA 83, 3022–3026 (1986).

    CAS  PubMed  Google Scholar 

  46. Kubota, D., Colgin, L. L., Casale, M., Brucher, F. A. & Lynch, G. Endogenous waves in hippocampal slices. J. Neurophysiol. 89, 81–89 (2003).

    PubMed  Google Scholar 

  47. Vandecasteele, M. et al. Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus. Proc. Natl Acad. Sci. USA 111, 13535–13540 (2014).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  49. Petsche, H., Stumpf, C. & Gogolak, G. [The significance of the rabbit's septum as a relay station between the midbrain and the hippocampus. I. The control of hippocampus arousal activity by the septum cells]. Electroencephalogr. Clin. Neurophysiol. 14, 202–211 (1962).

    CAS  PubMed  Google Scholar 

  50. Mizumori, S. J., Perez, G. M., Alvarado, M. C., Barnes, C. A. & McNaughton, B. L. Reversible inactivation of the medial septum differentially affects two forms of learning in rats. Brain Res. 528, 12–20 (1990).

    CAS  PubMed  Google Scholar 

  51. Brandon, M. P., Koenig, J., Leutgeb, J. K. & Leutgeb, S. New and distinct hippocampal place codes are generated in a new environment during septal inactivation. Neuron 82, 789–796 (2014). This paper shows that stable place fields emerge in a new environment when theta rhythms are suppressed.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Wang, Y., Romani, S., Lustig, B., Leonardo, A. & Pastalkova, E. Theta sequences are essential for internally generated hippocampal firing fields. Nat. Neurosci. 18, 282–288 (2015). This paper shows that 'episode fields', which normally emerge as animals run on a wheel during delays in a memory task, are abolished when theta rhythms are blocked by inactivation of the medial septum.

    CAS  PubMed  Google Scholar 

  53. Landfield, P. W., McGaugh, J. L. & Tusa, R. J. Theta rhythm: a temporal correlate of memory storage processes in the rat. Science 175, 87–89 (1972).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  55. Berry, S. D. & Thompson, R. F. Prediction of learning rate from the hippocampal electroencephalogram. Science 200, 1298–1300 (1978).

    CAS  PubMed  Google Scholar 

  56. Macrides, F., Eichenbaum, H. B. & Forbes, W. B. Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning. J. Neurosci. 2, 1705–1717 (1982).

    CAS  PubMed  Google Scholar 

  57. Mitchell, S. J., Rawlins, J. N., Steward, O. & Olton, D. S. Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats. J. Neurosci. 2, 292–302 (1982).

    CAS  PubMed  Google Scholar 

  58. Larson, J., Wong, D. & Lynch, G. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res. 368, 347–350 (1986).

    CAS  PubMed  Google Scholar 

  59. M'Harzi, M. & Jarrard, L. E. Effects of medial and lateral septal lesions on acquisition of a place and cue radial maze task. Behav. Brain Res. 49, 159–165 (1992).

    CAS  PubMed  Google Scholar 

  60. Orr, G., Rao, G., Houston, F. P., McNaughton, B. L. & Barnes, C. A. Hippocampal synaptic plasticity is modulated by theta rhythm in the fascia dentata of adult and aged freely behaving rats. Hippocampus 11, 647–654 (2001).

    CAS  PubMed  Google Scholar 

  61. Hyman, J. M., Wyble, B. P., Goyal, V., Rossi, C. A. & Hasselmo, M. E. 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, 11725–11731 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Griffin, A. L., Asaka, Y., Darling, R. D. & Berry, S. D. Theta-contingent trial presentation accelerates learning rate and enhances hippocampal plasticity during trace eyeblink conditioning. Behav. Neurosci. 118, 403–411 (2004).

    PubMed  Google Scholar 

  63. McNaughton, N., Ruan, M. & Woodnorth, M. A. Restoring theta-like rhythmicity in rats restores initial learning in the Morris water maze. Hippocampus 16, 1102–1110 (2006).

    PubMed  Google Scholar 

  64. Manns, J. R., Zilli, E. A., Ong, K. C., Hasselmo, M. E. & Eichenbaum, H. Hippocampal CA1 spiking during encoding and retrieval: relation to theta phase. Neurobiol. Learn. Mem. 87, 9–20 (2007).

    PubMed  Google Scholar 

  65. Rutishauser, U., Ross, I. B., Mamelak, A. N. & Schuman, E. M. Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464, 903–907 (2010).

    CAS  PubMed  Google Scholar 

  66. Siegle, J. H. & Wilson, M. A. Enhancement of encoding and retrieval functions through theta phase-specific manipulation of hippocampus. eLife 3, e03061 (2014). This study shows that memory encoding and memory retrieval are differentially affected depending on the theta phase at which CA1 is inhibited. Optogenetic techniques were used to inhibit CA1 activity at particular phases of theta.

    PubMed  PubMed Central  Google Scholar 

  67. Belchior, H., Lopes-Dos-Santos, V., Tort, A. B. & Ribeiro, S. Increase in hippocampal theta oscillations during spatial decision making. Hippocampus 24, 693–702 (2014).

    PubMed  PubMed Central  Google Scholar 

  68. Wilson, M. A. & McNaughton, B. L. Dynamics of the hippocampal ensemble code for space. Science 261, 1055–1058 (1993).

    CAS  PubMed  Google Scholar 

  69. Leutgeb, S., Leutgeb, J. K., Treves, A., Moser, M. B. & Moser, E. I. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305, 1295–1298 (2004).

    CAS  PubMed  Google Scholar 

  70. Frank, L. M., Stanley, G. B. & Brown, E. N. Hippocampal plasticity across multiple days of exposure to novel environments. J. Neurosci. 24, 7681–7689 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Yartsev, M. M. & Ulanovsky, N. Representation of three-dimensional space in the hippocampus of flying bats. Science 340, 367–372 (2013).

    CAS  PubMed  Google Scholar 

  72. Dragoi, G. & Buzsaki, G. Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50, 145–157 (2006).

    CAS  PubMed  Google Scholar 

  73. Foster, D. J. & Wilson, M. A. Hippocampal theta sequences. Hippocampus 17, 1093–1099 (2007).

    PubMed  Google Scholar 

  74. Feng, T., Silva, D. & Foster, D. J. Dissociation between the experience-dependent development of hippocampal theta sequences and single-trial phase precession. J. Neurosci. 35, 4890–4902 (2015). This study reveals that theta phase precession is present immediately in a novel environment but that theta sequences develop with experience.

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Gupta, A. S., van der Meer, M. A., Touretzky, D. S. & Redish, A. D. Segmentation of spatial experience by hippocampal theta sequences. Nat. Neurosci. 15, 1032–1039 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Wikenheiser, A. M. & Redish, A. D. Hippocampal theta sequences reflect current goals. Nat. Neurosci. 18, 289–294 (2015). This paper shows that theta sequences dynamically represent paths extending ahead of an animal's location towards upcoming goal locations.

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Komisaruk, B. R. Synchrony between limbic system theta activity and rhythmical behavior in rats. J. Comp. Physiol. Psychol. 70, 482–492 (1970).

    CAS  PubMed  Google Scholar 

  78. Kepecs, A., Uchida, N. & Mainen, Z. F. Rapid and precise control of sniffing during olfactory discrimination in rats. J. Neurophysiol. 98, 205–213 (2007).

    PubMed  Google Scholar 

  79. Berg, R. W., Whitmer, D. & Kleinfeld, D. Exploratory whisking by rat is not phase locked to the hippocampal theta rhythm. J. Neurosci. 26, 6518–6522 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Jezek, K., Henriksen, E. J., Treves, A., Moser, E. I. & Moser, M. B. Theta-paced flickering between place-cell maps in the hippocampus. Nature 478, 246–249 (2011).

    CAS  PubMed  Google Scholar 

  81. Dupret, D., O'Neill, J. & Csicsvari, J. Dynamic reconfiguration of hippocampal interneuron circuits during spatial learning. Neuron 78, 166–180 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Brandon, M. P., Bogaard, A. R., Schultheiss, N. W. & Hasselmo, M. E. Segregation of cortical head direction cell assemblies on alternating theta cycles. Nat. Neurosci. 16, 739–748 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Montgomery, S. M., Sirota, A. & Buzsaki, G. Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep. J. Neurosci. 28, 6731–6741 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Louie, K. & Wilson, M. A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29, 145–156 (2001).

    CAS  PubMed  Google Scholar 

  85. Chrobak, J. J. & Buzsaki, G. Selective activation of deep layer (V-Vi) retrohippocampal cortical-neurons during hippocampal sharp waves in the behaving rat. J. Neurosci. 14, 6160–6170 (1994).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Colgin, L. L., Kubota, D., Jia, Y., Rex, C. S. & Lynch, G. Long-term potentiation is impaired in rat hippocampal slices that produce spontaneous sharp waves. J. Physiol. 558, 953–961 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Papatheodoropoulos, C. & Koniaris, E. α5GABAA receptors regulate hippocampal sharp wave–ripple activity in vitro. Neuropharmacology 60, 662–673 (2011).

    CAS  PubMed  Google Scholar 

  89. Buzsaki, G., Gage, F. H., Kellenyi, L. & Bjorklund, A. Behavioral dependence of the electrical activity of intracerebrally transplanted fetal hippocampus. Brain Res. 400, 321–333 (1987).

    CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  91. Sullivan, D. et al. Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity. J. Neurosci. 31, 8605–8616 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Ylinen, A. et al. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15, 30–46 (1995).

    CAS  PubMed  Google Scholar 

  93. Klausberger, T. et al. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421, 844–848 (2003).

    CAS  PubMed  Google Scholar 

  94. Schlingloff, D., Kali, S., Freund, T. F., Hajos, N. & Gulyas, A. I. Mechanisms of sharp wave initiation and ripple generation. J. Neurosci. 34, 11385–11398 (2014).

    PubMed  PubMed Central  Google Scholar 

  95. Csicsvari, J., Hirase, H., Czurko, A., Mamiya, A. & Buzsaki, G. Fast network oscillations in the hippocampal CA1 region of the behaving rat. J. Neurosci 19, RC20 (1999).

    CAS  PubMed  Google Scholar 

  96. Kudrimoti, H. S., Barnes, C. A. & McNaughton, B. L. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J. Neurosci. 19, 4090–4101 (1999).

    CAS  PubMed  Google Scholar 

  97. Nadasdy, Z., Hirase, H., Czurko, A., Csicsvari, J. & Buzsaki, G. Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 19, 9497–9507 (1999).

    CAS  PubMed  Google Scholar 

  98. Lee, A. K. & Wilson, M. A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183–1194 (2002).

    CAS  PubMed  Google Scholar 

  99. Karlsson, M. P. & Frank, L. M. Awake replay of remote experiences in the hippocampus. Nat. Neurosci. 12, 913–918 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Carr, M. F., Karlsson, M. P. & Frank, L. M. Transient slow gamma synchrony underlies hippocampal memory replay. Neuron 75, 700–713 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Nakashiba, T., Buhl, D. L., McHugh, T. J. & Tonegawa, S. Hippocampal CA3 output is crucial for ripple-associated reactivation and consolidation of memory. Neuron 62, 781–787 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Siapas, A. G. & Wilson, M. A. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21, 1123–1128 (1998).

    CAS  PubMed  Google Scholar 

  103. Clemens, Z. et al. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 130, 2868–2878 (2007).

    PubMed  Google Scholar 

  104. Ramadan, W., Eschenko, O. & Sara, S. J. Hippocampal sharp wave/ripples during sleep for consolidation of associative memory. PLoS ONE 4, e6697 (2009).

    PubMed  PubMed Central  Google Scholar 

  105. Girardeau, G., Benchenane, K., Wiener, S. I., Buzsaki, G. & Zugaro, M. B. Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 12, 1222–1223 (2009).

    CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  107. Dupret, D., O'Neill, J., Pleydell-Bouverie, B. & Csicsvari, J. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat. Neurosci. 13, 995–1002 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Sirota, A., Csicsvari, J., Buhl, D. & Buzsaki, G. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl Acad. Sci. USA 100, 2065–2069 (2003).

    CAS  PubMed  Google Scholar 

  109. English, D. F. et al. Excitation and inhibition compete to control spiking during hippocampal ripples: intracellular study in behaving mice. J. Neurosci. 34, 16509–16517 (2014). In this study, intracellular recordings in behaving mice show that pyramidal cells are depolarized during sharp wave–ripples but their spiking is suppressed by ripple-associated shunting inhibition.

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Lee, I., Rao, G. & Knierim, J. J. A double dissociation between hippocampal subfields: differential time course of CA3 and CA1 place cells for processing changed environments. Neuron 42, 803–815 (2004).

    CAS  PubMed  Google Scholar 

  111. Roumis, D. K. & Frank, L. M. Hippocampal sharp-wave ripples in waking and sleeping states. Curr. Opin. Neurobiol. 35, 6–12 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Mehta, M. R. Cortico-hippocampal interaction during up-down states and memory consolidation. Nat. Neurosci. 10, 13–15 (2007).

    CAS  PubMed  Google Scholar 

  113. Carr, M. F., Jadhav, S. P. & Frank, L. M. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat. Neurosci. 14, 147–153 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Jadhav, S. P., Kemere, C., German, P. W. & Frank, L. M. Awake hippocampal sharp-wave ripples support spatial memory. Science 336, 1454–1458 (2012). This study disrupts sharp wave–ripples in rats while they carry out a spatial memory task and shows that task performance is impaired, suggesting that sharp wave–ripples in awake animals have a role in memory-guided trajectory planning.

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Gupta, A. S., van der Meer, M. A., Touretzky, D. S. & Redish, A. D. Hippocampal replay is not a simple function of experience. Neuron 65, 695–705 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Pfeiffer, B. E. & Foster, D. J. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497, 74–79 (2013). In this paper, sequences of place cell spikes observed during sharp wave–ripples while the animal is at rest are shown to represent paths that animals subsequently traverse to reach goal locations.

    CAS  PubMed  PubMed Central  Google Scholar 

  117. Singer, A. C., Carr, M. F., Karlsson, M. P. & Frank, L. M. Hippocampal SWR activity predicts correct decisions during the initial learning of an alternation task. Neuron 77, 1163–1173 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. Davidson, T. J., Kloosterman, F. & Wilson, M. A. Hippocampal replay of extended experience. Neuron 63, 497–507 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Foster, D. J. & Wilson, M. A. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440, 680–683 (2006).

    CAS  PubMed  Google Scholar 

  120. Csicsvari, J., O'Neill, J., Allen, K. & Senior, T. Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field exploration. Eur. J. Neurosci. 26, 704–716 (2007).

    PubMed  PubMed Central  Google Scholar 

  121. Bendor, D. & Wilson, M. A. Biasing the content of hippocampal replay during sleep. Nat. Neurosci. 15, 1439–1444 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Csicsvari, J., Jamieson, B., Wise, K. D. & Buzsaki, G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37, 311–322 (2003).

    CAS  PubMed  Google Scholar 

  123. Colgin, L. L. et al. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462, 353–357 (2009).

    CAS  PubMed  Google Scholar 

  124. Belluscio, M. A., Mizuseki, K., Schmidt, R., Kempter, R. & Buzsaki, G. Cross-frequency phase-phase coupling between theta and gamma oscillations in the hippocampus. J. Neurosci. 32, 423–435 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  125. Kemere, C., Carr, M. F., Karlsson, M. P. & Frank, L. M. Rapid and continuous modulation of hippocampal network state during exploration of new places. PLoS ONE 8, e73114 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Schomburg, E. W. et al. Theta phase segregation of input-specific gamma patterns in entorhinal-hippocampal networks. Neuron 84, 470–485 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Kay, L. M. Two species of gamma oscillations in the olfactory bulb: dependence on behavioral state and synaptic interactions. J. Integr. Neurosci. 2, 31–44 (2003).

    PubMed  Google Scholar 

  128. van der Meer, M. A. & Redish, A. D. Low and high gamma oscillations in rat ventral striatum have distinct relationships to behavior, reward, and spiking activity on a learned spatial decision task. Front. Integr. Neurosci. 3, 9 (2009).

    PubMed  PubMed Central  Google Scholar 

  129. Manabe, H. & Mori, K. Sniff rhythm-paced fast and slow gamma-oscillations in the olfactory bulb: relation to tufted and mitral cells and behavioral states. J. Neurophysiol. 110, 1593–1599 (2013).

    PubMed  Google Scholar 

  130. Bastos, A. M. et al. Visual areas exert feedforward and feedback influences through distinct frequency channels. Neuron 85, 390–401 (2015).

    CAS  PubMed  Google Scholar 

  131. Zheng, C. G. & Colgin, L. L. Beta and gamma rhythms go with the flow. Neuron 85, 236–237 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Bartos, M., Vida, I. & Jonas, P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 8, 45–56 (2007).

    CAS  PubMed  Google Scholar 

  133. Soltesz, I. & Deschenes, M. Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J. Neurophysiol. 70, 97–116 (1993).

    CAS  PubMed  Google Scholar 

  134. Tukker, J. J., Fuentealba, P., Hartwich, K., Somogyi, P. & Klausberger, T. Cell type-specific tuning of hippocampal interneuron firing during gamma oscillations in vivo. J. Neurosci. 27, 8184–8189 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  135. Senior, T. J., Huxter, J. R., Allen, K., O'Neill, J. & Csicsvari, J. Gamma oscillatory firing reveals distinct populations of pyramidal cells in the CA1 region of the hippocampus. J. Neurosci. 28, 2274–2286 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Penttonen, M., Kamondi, A., Acsady, L. & Buzsaki, G. Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur. J. Neurosci. 10, 718–728 (1998).

    CAS  PubMed  Google Scholar 

  137. Zheng, C., Bieri, K. W., Hsiao, Y. T. & Colgin, L. L. Spatial sequence coding differs during slow and fast gamma rhythms in the hippocampus. Neuron 89, 398–408 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  138. Lasztoczi, B. & Klausberger, T. Layer-specific GABAergic control of distinct gamma oscillations in the CA1 hippocampus. Neuron 81, 1126–1139 (2014).

    CAS  PubMed  Google Scholar 

  139. Yamamoto, J., Suh, J., Takeuchi, D. & Tonegawa, S. Successful execution of working memory linked to synchronized high-frequency gamma oscillations. Cell 157, 845–857 (2014).

    CAS  PubMed  Google Scholar 

  140. Pastoll, H., Solanka, L., van Rossum, M. C. & Nolan, M. F. Feedback inhibition enables theta-nested gamma oscillations and grid firing fields. Neuron 77, 141–154 (2013).

    CAS  PubMed  Google Scholar 

  141. Traub, R. D., Whittington, M. A., Colling, S. B., Buzsaki, G. & Jefferys, J. G. Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J. Physiol. 493, 471–484 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  142. Zheng, C., Bieri, K. W., Trettel, S. G. & Colgin, L. L. The relationship between gamma frequency and running speed differs for slow and fast gamma rhythms in freely behaving rats. Hippocampus 25, 924–938 (2015).

    PubMed  PubMed Central  Google Scholar 

  143. Kropff, E., Carmichael, J. E., Moser, M. B. & Moser, E. I. Speed cells in the medial entorhinal cortex. Nature 523, 419–424 (2015).

    CAS  PubMed  Google Scholar 

  144. Sun, C. et al. Distinct speed dependence of entorhinal island and ocean cells, including respective grid cells. Proc. Natl Acad. Sci. USA 112, 9466–9471 (2015).

    CAS  PubMed  Google Scholar 

  145. Ahmed, O. J. & Mehta, M. R. Running speed alters the frequency of hippocampal gamma oscillations. J. Neurosci. 32, 7373–7383 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  146. Canto, C. B., Wouterlood, F. G. & Witter, M. P. What does the anatomical organization of the entorhinal cortex tell us? Neural Plast. 2008, 381243 (2008).

    PubMed  PubMed Central  Google Scholar 

  147. Newman, E. L., Gillet, S. N., Climer, J. R. & Hasselmo, M. E. Cholinergic blockade reduces theta-gamma phase amplitude coupling and speed modulation of theta frequency consistent with behavioral effects on encoding. J. Neurosci. 33, 19635–19646 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  148. Bieri, K. W., Bobbitt, K. N. & Colgin, L. L. Slow and fast gamma rhythms coordinate different spatial coding modes in hippocampal place cells. Neuron 82, 670–681 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  149. Cabral, H. O. et al. Oscillatory dynamics and place field maps reflect hippocampal ensemble processing of sequence and place memory under NMDA receptor control. Neuron 81, 402–415 (2014).

    CAS  PubMed  Google Scholar 

  150. Takahashi, M., Nishida, H., Redish, A. D. & Lauwereyns, J. Theta phase shift in spike timing and modulation of gamma oscillation: a dynamic code for spatial alternation during fixation in rat hippocampal area CA1. J. Neurophysiol. 111, 1601–1614 (2014).

    PubMed  PubMed Central  Google Scholar 

  151. Treves, A. & Rolls, E. T. Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2, 189–199 (1992).

    CAS  PubMed  Google Scholar 

  152. Brun, V. H. et al. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296, 2243–2246 (2002).

    CAS  PubMed  Google Scholar 

  153. Steffenach, H. A., Sloviter, R. S., Moser, E. I. & Moser, M. B. Impaired retention of spatial memory after transection of longitudinally oriented axons of hippocampal CA3 pyramidal cells. Proc. Natl Acad. Sci. USA 99, 3194–3198 (2002).

    CAS  PubMed  Google Scholar 

  154. Nakazawa, K. et al. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297, 211–218 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  155. Tort, A. B., Komorowski, R. W., Manns, J. R., Kopell, N. J. & Eichenbaum, H. Theta-gamma coupling increases during the learning of item-context associations. Proc. Natl Acad. Sci. USA 106, 20942–20947 (2009).

    CAS  PubMed  Google Scholar 

  156. Shirvalkar, P. R., Rapp, P. R. & Shapiro, M. L. Bidirectional changes to hippocampal theta-gamma comodulation predict memory for recent spatial episodes. Proc. Natl Acad. Sci. USA 107, 7054–7059 (2010).

    CAS  PubMed  Google Scholar 

  157. Igarashi, K. M., Lu, L., Colgin, L. L., Moser, M. B. & Moser, E. I. Coordination of entorhinal-hippocampal ensemble activity during associative learning. Nature 510, 143–147 (2014).

    CAS  PubMed  Google Scholar 

  158. Martin, C., Beshel, J. & Kay, L. M. An olfacto-hippocampal network is dynamically involved in odor-discrimination learning. J. Neurophysiol. 98, 2196–2205 (2007).

    PubMed  Google Scholar 

  159. Pfeiffer, B. E. & Foster, D. J. Autoassociative dynamics in the generation of sequences of hippocampal place cells. Science 349, 180–183 (2015).

    CAS  PubMed  Google Scholar 

  160. Trimper, J. B., Stefanescu, R. A. & Manns, J. R. Recognition memory and theta-gamma interactions in the hippocampus. Hippocampus 24, 341–353 (2014).

    PubMed  Google Scholar 

  161. Kitanishi, T. et al. Novelty-induced phase-locked firing to slow gamma oscillations in the hippocampus: requirement of synaptic plasticity. Neuron 86, 1265–1276 (2015).

    CAS  PubMed  Google Scholar 

  162. Jeewajee, A., Lever, C., Burton, S., O'Keefe, J. & Burgess, N. Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus 18, 340–348 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  163. Diba, K. & Buzsaki, G. Forward and reverse hippocampal place-cell sequences during ripples. Nat. Neurosci. 10, 1241–1242 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  164. Wu, X. & Foster, D. J. Hippocampal replay captures the unique topological structure of a novel environment. J. Neurosci. 34, 6459–6469 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  165. Uhlhaas, P. J. & Singer, W. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52, 155–168 (2006).

    CAS  PubMed  Google Scholar 

  166. Zhang, H. & Jacobs, J. Traveling theta waves in the human hippocampus. J. Neurosci. 35, 12477–12487 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  167. Lubenov, E. V. & Siapas, A. G. Hippocampal theta oscillations are travelling waves. Nature 459, 534–539 (2009).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  169. Watrous, A. J. et al. A comparative study of human and rat hippocampal low-frequency oscillations during spatial navigation. Hippocampus 23, 656–661 (2013).

    PubMed  PubMed Central  Google Scholar 

  170. Jacobs, J. Hippocampal theta oscillations are slower in humans than in rodents: implications for models of spatial navigation and memory. Phil. Trans. R. Soc. B 369, 20130304 (2014).

    PubMed  Google Scholar 

  171. Bragin, A. et al. High-frequency oscillations in human brain. Hippocampus 9, 137–142 (1999).

    CAS  PubMed  Google Scholar 

  172. Axmacher, N., Elger, C. E. & Fell, J. Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain 131, 1806–1817 (2008).

    PubMed  Google Scholar 

  173. Staresina, B. P. et al. Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep. Nat. Neurosci. 18, 1679–1686 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  174. Skaggs, W. E. et al. EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. J. Neurophysiol. 98, 898–910 (2007).

    PubMed  Google Scholar 

  175. Leonard, T. K. et al. Sharp wave ripples during visual exploration in the primate hippocampus. J. Neurosci. 35, 14771–14782 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  176. Sederberg, P. B. et al. Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cereb. Cortex 17, 1190–1196 (2007).

    PubMed  Google Scholar 

  177. Jutras, M. J., Fries, P. & Buffalo, E. A. Gamma-band synchronization in the macaque hippocampus and memory formation. J. Neurosci. 29, 12521–12531 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  178. de Almeida, L., Idiart, M. & Lisman, J. E. A second function of gamma frequency oscillations: an E%-max winner-take-all mechanism selects which cells fire. J. Neurosci. 29, 7497–7503 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  179. Sigurdsson, T., Stark, K. L., Karayiorgou, M., Gogos, J. A. & Gordon, J. A. Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 464, 763–U139 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  180. Dickerson, D. D., Wolff, A. R. & Bilkey, D. K. Abnormal long-range neural synchrony in a maternal immune activation animal model of schizophrenia. J. Neurosci. 30, 12424–12431 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  181. Lee, H. et al. Early cognitive experience prevents adult deficits in a neurodevelopmental schizophrenia model. Neuron 75, 714–724 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  182. Racz, A., Ponomarenko, A. A., Fuchs, E. C. & Monyer, H. Augmented hippocampal ripple oscillations in mice with reduced fast excitation onto parvalbumin-positive cells. J. Neurosci. 29, 2563–2568 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  183. Suh, J., Foster, D. J., Davoudi, H., Wilson, M. A. & Tonegawa, S. Impaired hippocampal ripple-associated replay in a mouse model of schizophrenia. Neuron 80, 484–493 (2013).

    CAS  PubMed  Google Scholar 

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Acknowledgements

The author thanks K. Bieri, E. Hwaun, and C. Zheng for assistance with data collection and/or figure preparation. The work of L.L.C. is supported by the Klingenstein Fund, the Whitehall Foundation, Alzheimer's Association grant NIRP-14- 305205, National Institute of Mental Health (NIMH) grant 1R01MH102450-01A1, the Office of Naval Research Young Investigator Program award N00014-14-1-0322 and National Science Foundation CAREER award #1453756.

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PowerPoint slides

Glossary

Sleep spindles

Thalamocortical oscillations of 7–14 Hz that occur in bouts lasting for a few seconds and recurring approximately once every 10 seconds during slow-wave sleep, particularly around the onset of sleep.

Slow oscillations

Cortically generated oscillations of 0.5–1 Hz, consisting of alternating depolarizing 'up' states and hyperpolarizing 'down' states that regulate the occurrence of other oscillations, including sleep spindles, during slow-wave sleep.

Neuronal ensembles

Co-active neurons that work together to carry out neuronal computations and operations such as stimuli coding or memory storage.

Theta sequences

Ordered series of place cell spikes that occur within theta cycles and that represent the succession of locations traversed during active behaviours.

Head direction cells

Neurons that fire when an animal's head is pointing in a particular direction and are found in several brain areas including the postsubiculum, the thalamus and the medial entorhinal cortex.

Replay

The phenomenon by which ordered place cell spike trains that occur during exploratory theta-related behaviours later reactivate in a temporally compressed manner during sharp wave–ripples while the animal is at rest and during slow-wave sleep.

Stratum radiatum

Apical dendritic layer in CA3 and CA1 in which axons from CA3 pyramidal neurons terminate.

Stratum lacunosum-moleculare

Distal apical dendritic layer in CA3 and CA1 in which perforant pathway fibres from the entorhinal cortex terminate.

Delayed nonmatching-to-place task

A behavioural task that assesses memory by first allowing animals to visit one of two goal locations and then, after a delay period, requiring animals to navigate to the other goal location in order to receive a reward.

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Colgin, L. Rhythms of the hippocampal network. Nat Rev Neurosci 17, 239–249 (2016). https://doi.org/10.1038/nrn.2016.21

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