Hippocampal theta oscillations are slower in humans than in rodents: Implications for models of spatial navigation and memory

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1635, 2014, Pages

  Jacobs, Joshua ^a  

^a DREXEL UNIVERSITY   (United States)

Author keywords

Electroencephalography; Hippocampus; Memory; Navigation; Theta oscillations

Indexed keywords

BRAIN; HUMAN ACTIVITY; HUMAN BEHAVIOR; MEMORY; OSCILLATION; RODENT; SPATIAL COGNITION;

ANIMAL; BAT; DEPTH PERCEPTION; ELECTROENCEPHALOGRAPHY; ELECTROPHYSIOLOGY; HIPPOCAMPUS; HUMAN; MEMORY; NAVIGATION; NERVE CELL; PHYSIOLOGY; RAT; REVIEW; THETA OSCILLATIONS; THETA RHYTHM;

ELECTROENCEPHALOGRAPHY; HIPPOCAMPUS; MEMORY; NAVIGATION; THETA OSCILLATIONS;

ANIMALS; CHIROPTERA; ELECTROPHYSIOLOGY; HIPPOCAMPUS; HUMANS; MEMORY; NEURONS; RATS; SPACE PERCEPTION; THETA RHYTHM;

EID: 84906921433     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0304     Document Type: Review

References (98)

1. Scoville WB, Milner B. 1957 Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11-21. (doi:10.1136/ jnnp.20.1.11)
2. Berry SD, Thompson RF. 1978 Prediction of learning rate from the hippocampal electroenephalogram. Science 200, 1298-1300. (doi:10.1126/science.663612)
3. Moser MB, Moser EI. 1998 Functional differentiation in the hippocampus. Hippocampus 8, 608-619. (doi:10.1002/(SICI)1098-1063(1998)8:6,608::AIDHIPO3.3.0. CO;2-7)
4. O'Keefe J, Nadel L. 1978 The hippocampus as a cognitive map. New York, NY: Oxford University Press.
5. Eichenbaum H. 2000 A cortical-hippocampal system for declarative memory. Nat. Rev. Neurosci. 1, 41-50. (doi:10.1038/35036213)
6. Buzsáki G. 2005 Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15, 827-840. (doi:10.1002/hipo.20113)
7. Buzsáki G, Moser EI. 2013 Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16, 130-138. (doi:10.1038/ nn.3304)
8. Kahana MJ, Seelig D, Madsen JR. 2001 Theta returns. Curr. Opin. Neurobiol. 11, 739-744. (doi:10.1016/S0959-4388(01)00278-1)
9. Buzsáki G. 2002 Theta oscillations in the hippocampus. Neuron 33, 325-340. (doi:10.1016/ S0896-6273(02)00586-X)
10. Vanderwolf C. 1969 Hippocampal electrical activity and voluntary movement of the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407-418. (doi:10.1016/0013-4694(69)90092-3)
11. Bland BH. 1986 The physiology and pharmacology of hippocampal formation theta rhythms. Prog. Neurobiol. 26, 1-54. (doi:10.1016/0301-0082(86)90019-5)
12. Green JD, Arduini AA. 1954 Hippocampal electrical activity in arousal. J. Neurophysiol. 17, 533-557.
13. Seager MA, Johnson LD, Chabot ES, Asaka Y, Berry SD. 2002 Oscillatory brain states and learning: impact of hippocampal theta-contingent training. Proc. Natl Acad. Sci. USA 99, 1616-1620. (doi:10. 1073/pnas.032662099)
14. O'Keefe J, Recce ML. 1993 Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317-330. (doi:10.1002/hipo.450030307)
15. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. 2005 Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801-806. (doi:10. 1038/nature03721)
16. Burgess N, Barry C, O'Keefe J, London U. 2007 An oscillatory interference model of grid cell firing. Hippocampus 17, 801-812. (doi:10.1002/ hipo.20327)
17. Halgren E, Babb TL, Crandall PH. 1978 Human hippocampal formation EEG desynchronizes during attentiveness and movement. Electroencephalogr. Clin. Neurophysiol. 44, 778-781. (doi:10.1016/ 0013-4694(78)90212-2)
18. Yartsev MM, Witter MP, Ulanovsky N. 2011 Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479, 103-107. (doi:10.1038/ nature10583)
19. Giocomo LM, Moser EI. 2011 Spatial representation: maps in a temporal void. Curr. Biol. 21, R962-R964. (doi:10.1016/j.cub.2011.10.024)
20. Jacobs J, Kahana MJ. 2010 Direct brain recordings fuel advances in cognitive electrophysiology. Trends Cogn. Sci. 14, 162-171. (doi:10.1016/j.tics. 2010.01.005)
21. Miller R. 1991 Cortico-hippocampal interplay and the representation of contexts in the brain. Berlin, Germany: Springer.
22. Lisman J, Idiart MA. 1995 Storage of 7+2 shortterm memories in oscillatory subcycles. Science 267, 1512-1515. (doi:10.1126/science.7878473)
23. Hasselmo ME, Bodelon 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, 793-817. (doi:10.1162/089976602317318965)
24. McFarland WL, Teitelbaum H, Hedges EK. 1975 Relationship between hippocampal theta activity and running speed in the rat. J. Comp. Physiol. Psychol. 88, 324-328. (doi:10.1037/h0076177)
25. Berg RW, Whitmer D, Kleinfeld D. 2006 Exploratory whisking by rat is not phase locked to the hippocampal theta rhythm. J. Neurosci. 26, 6518-6522. (doi:10.1523/JNEUROSCI.0190-06.2006)
26. Huxter J, Burgess N, O'Keefe J. 2003 Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425, 828-832. (doi:10.1038/ nature02058)
27. Jezek K, Henriksen EJ, Treves A, Moser EI, Moser MB. 2011 Theta-paced flickering between place-cell maps in the hippocampus. Nature 478, 246-249. (doi:10. 1038/nature10439)
28. Brandon MP, Bogaard AR, Schultheiss NW, Hasselmo ME. 2013 Segregation of cortical head direction cell assemblies on alternating theta cycles. Nat. Neurosci. 16, 739-748. (doi:10.1038/nn.3383)
29. Douchamps V, Jeewajee A, Blundell P, Burgess N, Lever C. 2013 Evidence for encoding versus retrieval scheduling in the hippocampus by theta phase and acetylcholine. J. Neurosci. 33, 8689-8704. (doi:10. 1523/JNEUROSCI.4483-12.2013)
30. Jeewajee A, Lever C, Burton S, O'Keefe J, Burgess N. 2008 Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus 18, 340-348. (doi:10.1002/hipo.20394)
31. Barry C, Ginzberg LL, O'Keefe J, Burgess N. 2012 Grid cell firing patterns signal environmental novelty by expansion. Proc. Natl Acad. Sci. USA 109, 17 687-17 692. (doi:10.1073/pnas.1209918109)
32. Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsáki G. 2008 Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60, 683-697. (doi:10.1016/j.neuron.2008.09.014)
33. Siapas A, Lubenov E, Wilson MA. 2005 Prefrontal phase locking to hippocampal theta oscillations. Neuron 46, 141-151. (doi:10.1016/j.neuron.2005. 02.028)
34. Chrobak JJ, Buzsáki G. 1998 Gamma oscillations in the entorhinal cortex of the freely behaving rat. J. Neurosci. 18, 388-298.
35. Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsáki G. 1995 Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 15, 47-60.
36. 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. (doi:10.1126/science.1128115)
37. Belluscio MA, Mizuseki K, Schmidt R, Kempter R, Buzsáki G. 2012 Cross-frequency phase-phase coupling between theta and gamma oscillations in the hippocampus. J. Neurosci. 32, 423-435. (doi:10.1523/JNEUROSCI.4122-11.2012)
38. Doeller CF, Barry C, Burgess N. 2010 Evidence for grid cells in a human memory network. Nature 463, 657-661. (doi:10.1038/nature08704)
39. Jacobs J et al. 2013 Direct recordings of grid-like neuronal activity in human spatial navigation. Nat. Neurosci. 16, 1188-1190. (doi:10.1038/nn.3466)
40. Moser E, Kropff E, Moser M. 2008 Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 31, 69-89. (doi:10.1146/ annurev.neuro.31.061307.090723)
41. Jeewajee A, Barry C, O'Keefe J, Burgess N. 2008 Grid cells and theta as oscillatory interference: electrophysiological data from freely moving rats. Hippocampus 18, 1175-1185. (doi:10.1002/ hipo.20510)
42. Giocomo LM, Zilli EA, Fransen E, Hasselmo ME. 2007 Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 315, 1719-1722. (doi:10.1126/science. 1139207)
43. Brandon MP, Bogaard AR, Libby CP, Connerney MA, Gupta K, Hasselmo ME. 2011 Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 332, 595-599. (doi:10. 1126/science.1201652)
44. 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. (doi:10.1126/science.1201685)
45. Sreenivasan S, Fiete I. 2011 Grid cells generate an analog error-correcting code for singularly precise neural computation. Nat. Neurosci. 14, 1330-1337. (doi:10.1038/nn.2901)
46. Heys JG, MacLeod KM, Moss CF, Hasselmo ME. 2013 Bat and rat neurons differ in theta-frequency resonance despite similar coding of space. Science 340, 363-367. (doi:10.1126/science.1233831)
47. Barry C, Doeller CF. 2013 3D mapping in the brain. Science 340, 279-280. (doi:10.1126/science. 1237569)
48. Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I. 2003 Cellular networks underlying human spatial navigation. Nature 425, 184-187. (doi:10.1038/nature01964)
49. Jacobs J, Kahana MJ, Ekstrom AD, Mollison MV, Fried I. 2010 A sense of direction in human entorhinal cortex. Proc. Natl Acad. Sci. USA 107, 6487-6482. (doi:10.1073/pnas.0911213107)
50. Jacobs J et al. 2010 Right-lateralized brain oscillations in human spatial navigation. J. Cogn. Neurosci. 22, 824-836. (doi:10.1162/ jocn.2009.21240)
51. Sederberg PB, Schulze-Bonhage A, Madsen JR, Bromfield EB, McCarthy DC, Brandt A, Tully MS, Kahana MJ. 2007 Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cereb. Cortex 17, 1190-1196. (doi:10. 1093/cercor/bhl030)
52. Jacobs J, Kahana MJ, Ekstrom AD, Fried I. 2007 Brain oscillations control timing of single-neuron activity in humans. J. Neurosci. 27, 3839-3844. (doi:10.1523/JNEUROSCI.4636-06.2007)
53. Buzsáki G, Draguhn A. 2004 Neuronal oscillations in cortical networks. Science 304, 1926-1929. (doi:10. 1126/science.1099745)
54. Ekstrom AD, Caplan JB, Ho E, Shattuck K, Fried I, Kahana MJ. 2005 Human hippocampal theta activity during virtual navigation. Hippocampus 15, 881-889. (doi:10.1002/hipo.20109)
55. Watrous AJ, Fried I, Ekstrom AD. 2011 Behavioral correlates of human hippocampal delta and theta oscillations during navigation. J. Neurophysiol. 105, 1747-1755. (doi:10.1152/jn.00921.2010)
56. Lega BC, Jacobs J, Kahana MJ. 2011 Human hippocampal theta oscillations and the formation of episodic memories. Hippocampus 22, 748-761. (doi:10.1002/hipo.20937)
57. Clemens Z et al. 2013 Increased mesiotemporal delta activity characterizes virtual navigation in humans. Neurosci. Res. 76, 67-75. (doi:10.1016/j. neures.2013.03.004)
58. van Vugt MK, Sederberg PB, Kahana MJ. 2007 Comparison of spectral analysis methods for characterizing brain oscillations. J. Neurosci. Methods 162, 49-63. (doi:10.1016/j.jneumeth.2006.12.004)
59. Burgess N. 2008 Grid cells and theta as oscillatory interference: theory and predictions. Hippocampus 18, 1157-1174. (doi:10.1002/hipo.20518)
60. Manning JR, Jacobs J, Fried I, Kahana MJ. 2009 Broadband shifts in LFP power spectra are correlated with single-neuron spiking in humans. J. Neurosci. 29, 13 613-13 620. (doi:10.1523/ JNEUROSCI.2041-09.2009)
61. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser M-B, Moser EI. 2009 Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462, 353-357. (doi:10. 1038/nature08573)
62. Fell J, Klaver P, Elfadil H, Schaller C, Elger CE, Fernandez G. 2003 Rhinal-hippocampal theta coherence during declarative memory formation: interaction with gamma synchronization? Eur. J. Neurosci. 17, 1082-1088. (doi:10.1046/j. 1460-9568.2003.02522.x)
63. Babiloni C et al. 2010 Cortical sources of resting EEG rhythms in mild cognitive impairment and subjective memory complaint. Neurobiol. Aging 31, 1787-1798. (doi:10.1016/j.neurobiolaging.2008. 09.020)
64. Foster BL, Kaveh A, Dastjerdi M, Miller KJ, Parvizi J. 2013 Human retrosplenial cortex displays transient theta phase locking with medial temporal cortex prior to activation during autobiographical memory retrieval. J. Neurosci. 33, 10 439-10 446. (doi:10. 1523/JNEUROSCI.0513-13.2013)
65. Bódizs R, Kántor S, Szabó G, Szûcs A, Erõss L, Halász P. 2001 Rhythmic hippocampal slow oscillation characterizes REM sleep in humans. Hippocampus 11, 747-753. (doi:10.1002/hipo.1090)
66. Moroni F et al. 2012 Slow EEG rhythms and interhemispheric synchronization across sleep and wakefulness in the human hippocampus. Neuroimage 60, 497-504. (doi:10.1016/j. neuroimage.2011.11.093)
67. Clemens Z, Weiss B, Szücs A, Eröss L, Rásonyi G, Halász P. 2009 Phase coupling between rhythmic slow activity and gamma characterizes mesiotemporal rapid-eye-movement sleep in humans. Neuroscience 163, 388-396. (doi:10.1016/ j.neuroscience.2009.06.044)
68. Ferrara M, Moroni F, De Gennaro L, Nobili L. 2012 Hippocampal sleep features: relations to human memory function. Front. Neurol. 3, 57. (doi:10. 3389/fneur.2012.00057)
69. Jacobs J, Kahana MJ. 2009 Neural representations of individual stimuli in humans revealed by gammaband ECoG activity. J. Neurosci. 29, 10 203-10 214. (doi:10.1523/JNEUROSCI.2187-09.2009)
70. de Araujo DB, Baffa O, Wakai RT. 2002 Theta oscillations and human navigation: a magnetoencephalography study. J. Cogn. Neurosci. 14, 70-78. (doi:10.1162/089892902317205339)
71. 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, 5983-5990. (doi:10. 1523/JNEUROSCI.5001-07.2008)
72. Kaplan R, Doeller CF, Barnes GR, Litvak V, Düzel E, Bandettini PA, Burgess N, Eichenbaum HB. 2012 Movement-related theta rhythm in humans: coordinating self-directed hippocampal learning. PLoS Biol. 10, e1001267. (doi:10.1371/journal. pbio.1001267)
73. Guderian S, Düzel E. 2005 Induced theta oscillations mediate large-scale synchrony with mediotemporal areas during recollection in humans. Hippocampus 15, 901-912. (doi:10.1002/hipo.20125)
74. 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. USA 106, 5365-5370. (doi:10.1073/ pnas.0900289106)
75. Poch C, Fuentemilla L, Barnes GR, Düzel E. 2011 Hippocampal theta-phase modulation of replay correlates with configural-relational short-term memory performance. J. Neurosci. 31, 7038-7042. (doi:10.1523/JNEUROSCI.6305-10.2011)
76. 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. (doi:10. 1523/JNEUROSCI.2573-12.2013)
77. Staudigl T, Hanslmayr S. 2013 Theta oscillations at encoding mediate the context-dependent nature of human episodic memory. Curr. Biol. 23, 1101-1106. (doi:10.1016/j.cub.2013.04.074)
78. Rutishauser U, Ross IB, Mamelak AN, Schuman EM. 2010 Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464, 903-907. (doi:10.1038/nature08860)
79. Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J. 2010 Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc. Natl Acad. Sci. USA 107, 3228-3233. (doi:10.1073/pnas.0911531107)
80. 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. (doi:10.1523/ JNEUROSCI.3668-10.2011)
81. Steinvorth S, Wang C, Ulbert I, Schomer D, Halgren E. 2009 Human entorhinal gamma and theta oscillations selective for remote autobiographical memory. Hippocampus 20, 166-173. (doi:10.1002/ hipo.20597)
82. Watrous AJ, Tandon N, Conner CR, Pieters T, Ekstrom AD. 2013 Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval. Nat. Neurosci. 16, 349-356. (doi:10.1038/ nn.3315)
83. Fujisawa S, Buzsáki G. 2011 A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities. Neuron 72, 153-165. (doi:10.1016/j.neuron.2011.08.018)
84. Raghavachari S, Lisman JE, Tully M, Madsen JR, Bromfield EB, Kahana MJ. 2006 Theta oscillations in human cortex during a working memory task: evidence for local generators. J. Neurophysiol. 95, 1630-1638. (doi:10.1152/jn.00409.2005)
85. Montgomery SM, Betancur MI, Buzsaki G. 2009 Behavior-dependent coordination of multiple theta dipoles in the hippocampus. J. Neurosci. 29, 1381-1394. (doi:10.1523/ JNEUROSCI.4339-08.2009)
86. Cantero JL, Atienza M, Stickgold R, Kahana MJ, Madsen JR, Kocsis B. 2003 Sleep-dependent theta oscillations in the human hippocampus and neocortex. J. Neurosci. 23, 10 897-10 903.
87. Barry C, Bush D, O'Keefe J, Burgess N. 2012 Models of grid cells and theta oscillations. Nature 488, E1. (doi:10.1038/nature11276)
88. Hasselmo ME, Giocomo LM, Zilli EA. 2007 Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus 17, 1252-1271. (doi:10.1002/ hipo.20374)
89. Mormann F, Osterhage H, Andrzejak RG, Weber B, Fernández G, Fell J, Elger CE, Lehnertz K. 2008 Independent delta/theta rhythms in the human hippocampus and entorhinal cortex. Front. Hum. Neurosci. 2, 3. (doi:10.3389/neuro.09.003.2008)
90. Steriade M. 2001 Impact of network activities on neuronal properties in corticothalamic systems. J. Neurophysiol. 86, 1-39.
91. Diba K, Buzsáki G. 2008 Hippocampal network dynamics constrain the time lag between pyramidal cells across modified environments. J. Neurosci. 28, 13 448-13 456. (doi:10.1523/JNEUROSCI.3824-08.2008)
92. Lisman J, Buzsaki G. 2008 A neural coding scheme formed by the combined function of gamma and theta oscillations. Schizophr. Bull. 34, 974-980. (doi:10.1093/schbul/sbn060)
93. Buzsáki G. 2006 Rhythms of the brain. New York, NY: Oxford University Press.
94. Palva JM, Palva S, Kaila K. 2005 Phase synchrony among neuronal oscillations in the human cortex. J. Neurosci. 25, 3962-3972. (doi:10.1523/ JNEUROSCI.4250-04.2005)
95. Watrous AJ, Lee DJ, Izadi A, Gurkoff GG, Shahlaie K, Ekstrom AD. 2013 A comparative study of human and rat hippocampal low-frequency oscillations during spatial navigation. Hippocampus 23, 656-661. (doi:10.1002/hipo.22124)
96. Hasselmo ME. 2008 Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting. Hippocampus 18, 1213-1229. (doi:10.1002/hipo.20512)
97. 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. (doi:10.1038/21645)
98. Klausberger T, Magill PJ, Marton LF, Roberts JD, Cobden PM, Buzsáki G, Somogyi P. 2003 Brainstate-and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421, 844-848. (doi:10.1038/nature01374)