Theta phase shift in spike timing and modulation of gamma oscillation: A dynamic code for spatial alternation during fixation in rat hippocampal area CA1

Journal of Neurophysiology

Volumn 111, Issue 8, 2014, Pages 1601-1614

  Takahashi, Muneyoshi ^a,b   Nishida, Hiroshi ^a   Redish, A David ^c   Lauwereyns, Johan ^a,b  

^a KYUSHU UNIVERSITY   (Japan)

^b TAMAGAWA UNIVERSITY   (Japan)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Gamma oscillations; Memory; Nose poking paradigm; Spike phase shift; Theta rhythm

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CORPUS CALLOSUM; ELECTRIC POTENTIAL; ELECTRODE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS THETA RHYTHM; INFORMATION PROCESSING; MALE; MEMORY; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; STRATUM PYRAMIDALE; TASK PERFORMANCE; ANIMAL; DECISION MAKING; GAMMA RHYTHM; PHYSIOLOGY; THETA RHYTHM; WISTAR RAT;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CHOICE BEHAVIOR; GAMMA RHYTHM; MALE; MEMORY; PYRAMIDAL CELLS; RATS; RATS, WISTAR; THETA RHYTHM;

EID: 84900812759     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00395.2013     Document Type: Article

References (62)

1. Ahmed OJ, Mehta MR. Running speed alters the frequency of hippocampal gamma oscillations. J Neurosci 32: 7373-7383, 2012.
2. Belluscio MA, Mizuseki K, Schmidt R, Kempter R, Buzáki G. Crossfrequency phase-phase coupling between theta and gamma oscillations in the hippocampus. J Neurosci 32: 423-435, 2012.
3. Bland BH. Anatomical, physiological, and pharmacological properties underlying hippocampal sensorimotor integration. In: Information Processing by Neuronal Populations, edited by Hölscher C, Munk M. New York: Cambridge University Press, 2009, p. 283-325.
4. Bland BH, Oddie SD. Theta band oscillation and synchrony in the hippocampal formation and associated structures: the case for its role in sensorimotor integration. Behav Brain Res 127: 119-136, 2001.
5. Bokil H, Andrews P, Kulkarni JE, Mehta S, Mitra PP. Chronux: a platform for analyzing neural signals. J Neurosci Methods 192: 146-151, 2010.
6. Bower MR, Euston DR, McNaughton BL. Sequential-context-dependent hippocampal activity is not necessary to learn sequences with repeated elements. J Neurosci 25: 1313-1323, 2005.
7. Bragin A, Jandó G, Nádasdy Z, Hetke J, Wise K, Buzsáki G. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15: 47-60, 1995.
8. Brankack J, Stewart M, Fox SE. Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators. Brain Res 615: 310-327, 1993.
9. Buzsáki G. Rhythms of the Brain. New York: Oxford University Press, 2006.
10. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT. High gamma power is phase-locked to theta oscillations in human neocortex. Science 313: 1626-1628, 2006.
11. Carr MF, Karlsson MP, Frank LM. Transient slow gamma synchrony underlies hippocampal memory replay. Neuron 75: 700-713, 2012.
12. Chen Z, Resnik E, McFarland JM, Sakmann B, Mehta MR. Speed controls the amplitude and timing of the hippocampal gamma rhythm. PLos One 6: e21408, 2011.
13. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462: 353-357, 2009.
14. Csicsvari J, Hirase H, Czurkó A, Mamiya A, Buzsáki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19: 274-287, 1999.
15. Csicsvari J, Jamieson B, Wise KD, Buzsáki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37: 311-322, 2003.
16. Davidson TJ, Kloosterman F, Wilson MA. Hippocampal replay of extended experience. Neuron 63: 497-507, 2010.
17. Diba K, Buzsáki G. Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 10: 1241-1242, 2007.
18. Ferbinteanu J, Shapiro ML. Prospective and retrospective memory coding in the hippocampus. Neuron 40: 1227-1239, 2003.
19. Foster DJ, Wilson MA. Reverse replay of behavioural sequences in hippocampal place cells during awake state. Nature 440: 680-683, 2006.
20. Gupta AS, van der Meer MA, Touretzky DS, Redish AD. Hippocampal replay is not a simple function of experience. Neuron 65: 695-705, 2010.
21. Gupta AS, Van der Meer MA, Touretzky DS, Redish AD. Segmentation of spatial experience by hippocampal theta sequences. Nat Neurosci 15: 1032-1039, 2012.
22. Harris KD, Henze DA, Hirase H, Leinekugel X, Dragoi G, Czurkó A, Buzsáki G. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417: 738-741, 2002.
23. Harvey CD, Collman F, Dombeck DA, Tank DW. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461: 941-946, 2009.
24. Hasselmo ME. What is the function of hippocampal theta rhythm? Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 15: 936-949, 2005.
25. Hasselmo ME, Bodelón C, Wyble BP. A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput 14: 793-817, 2002.
26. Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME. 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.
27. Jezek K, Henriksen EJ, Treves A, Moser EI, Moser MB. Theta-paced flickering between place-cell maps in the hippocampus. Nature 478: 246-249, 2011.
28. Johnson A, Redish AD. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J Neurosci 27: 12176-12189, 2007.
29. Karlsson MP, Frank LM. Awake replay of remote experiences in the hippocampus. Nat Neurosci 12: 913-918, 2009.
30. Kemere C, Carr MF, Karlsson MP, Frank LM. Rapid and continuous modulation of hippocampal network state during exploration of new place. PLos One 8: e73114, 2013.
31. Kempter R, Leibold C, Buzsáki G, Diba K, Schmidt R. Quantifying circular-linear associations: hippocampal phase precession. J Neurosci Methods 207: 113-124, 2012.
32. Kramis R, Vanderwolf CH, Bland BH. 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.
33. Lever C, Wills T, Cacucci F, Burgess N, O'Keefe J. Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416: 90-94, 2002.
34. Lisman J. The theta/gamma discrete phase code occurring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus 15: 913-922, 2005.
35. Lisman J, Redish AD. Prediction, sequences and the hippocampus. Philos Trans R Soc Lond B Biol Sci 364: 1193-1201, 2009.
36. Mitra P, Bokil H. Observed Brain Dynamics. New York: Oxford University Press, 2008.
37. O'Keefe J, Nadel L. The Hippocampus as a Cognitive Map. Oxford, UK: Clarendon, 1978.
38. O'Keefe J, Recce ML. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3: 317-30, 1993.
39. O'Neil J, Senior TJ, Allen K, Huxter JR, Csicsvari J. Reactivation of experience-dependent cell assembly patterns in the hippocampus. Nat Neurosci 11: 209-215, 2008.
40. Pastalkova E, Itskov V, Amarasingham A, Buzsáki G. Internally generated cell assembly sequences in the rat hippocampus. Science 321: 1322-1327, 2008.
41. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates (5th Ed.). San Diego, CA: Elsevier Academic, 2004.
42. Poe GR, Nitz DA, McNaughton BL, Barnes CA. Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res 855: 176-180, 2000.
43. Redish AD. Beyond the Cognitive Map: From Place Cells to Episodic Memory. Cambridge, MA: MIT, 1999.
44. Royer S, Zemelman BV, Losonczy A, Kim J, Chance F, Magee JC, Buzsáki G. Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat Neurosci 15: 769-775, 2012.
45. Sakurai Y. Involvement of auditory cortical and hippocampal neurons in auditory working memory and reference memory in the rat. J Neurosci 14: 2606-2623, 1994.
46. Sakurai Y. Hippocampal and neocortical cell assemblies encode memory processes for different types of stimuli in the rat. J Neurosci 16: 2809-2819, 1996.
47. Scheffer-Teixeira R, Beichior H, Caixeta FV, Souza BC, Ribeiro S, Tort AB. Theta phase modulates multiple layer-specific oscillations in the CA1 region. Cereb Cortex 22: 2404-2414, 2012.
48. Schmidt R, Diba K, Leibold C, Schmitz D, Buzsáki G, Kempter R. Single-trial phase precession in the hippocampus. J Neurosci 29: 13232-13241, 2009.
49. Schmitzer-Torbert N, Redish AD. Neuronal activity in the rodent dorsal striatum in sequential navigation: separation of spatial and reward responses on the multiple T task. J Neurophysiol 91: 2259-2272, 2004.
50. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6: 149-172, 1996.
51. Smith DM, Mizumori SJ. Learning-related development of context-specific neuronal responses to places and events: the hippocampal role in context processing. J Neurosci 26: 3154-3163, 2006.
52. Takahashi M, Lauwereyns J, Sakurai Y, Tsukada M. A code for spatial alternation during fixation in rat hippocampal CA1 neurons. J Neurophysiol 102: 556-567, 2009a
53. Takahashi M, Lauwereyns J, Sakurai Y, Tsukada M. Behavioral statedependent episodic representations in rat CA1 neuronal activity during spatial alternation. Cogn Neurodyn 3: 165-175, 2009b
54. Tort AB, Kramer MA, Thorn C, Gibson DJ, Kubota Y, Graybiel AM, Kopell NJ. 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: 20517-20522, 2008.
55. Tort AB, Komorowski RW, Manns JR, Kopell NJ, Eichenbaum H. Theta-gamma coupling increases during the learning of item-context associations. Proc Natl Acad Sci U S A 106: 20942-20947, 2009.
56. Tort AB, Komorowski R, Eichenbaum H, Kopell N. Measuring phaseamplitude coupling between neuronal oscillations of different frequencies. J Neurophysiol 104: 1195-1210, 2010.
57. Vanderwolf CH. Limbic-diencephalic mechanisms of voluntary movement. Psychol Rev 78: 83-113, 1971.
58. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27: 623-633, 2000.
59. Yamaguchi Y, Aota Y, McNaughton BL, Lipa P. Bimodality of theta phase precession in hippocampal place cells in freely running rats. J Neurophysiol 87: 2629-2642, 2002.
60. Yamaguchi Y, Sato N, Wagatsuma H, Wu Z, Molter C, Aota Y. A unified view of theta-phase coding in the entorhinal-hippocampal system. Curr Opin Neurobiol 17: 197-204, 2007.
61. Ylinen A, Bragin A, Nádasdy Z, Jandó G, Szabó I, Sik A, Buzsáki G. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15: 30-46, 1995.
62. Zar JH. Biostatistical Analysis (5th Ed.). Upper Saddle River, NJ: Prentice- Hall/Pearson, 2007.