Hippocampal theta, gamma, and theta-gamma coupling: Effects of aging, environmental change, and cholinergic activation

Journal of Neurophysiology

Volumn 109, Issue 7, 2013, Pages 1852-1865

  Jacobson, Tara K ^a   Howe, Matthew D ^a   Schmidt, Brandy ^a   Hinman, James R ^a   Escabí, Monty A ^a,b   Markus, Etan J ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b University of Connecticut   (United States)

Author keywords

EEG; Encoding; Field potentials; Learning; Novelty; Oscillations; Physostigmine; Theta frequency

Indexed keywords

PHYSOSTIGMINE;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ELECTRODE; ENVIRONMENTAL CHANGE; GAMMA RHYTHM; HIPPOCAMPUS; HISTOLOGY; INFORMATION PROCESSING; MALE; MAZE TEST; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RAT; THETA RHYTHM;

AGING; ANIMALS; BRAIN WAVES; CHOLINESTERASE INHIBITORS; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; MALE; MAZE LEARNING; PHYSOSTIGMINE; RATS; RATS, INBRED F344; THETA RHYTHM;

EID: 84876011925     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00409.2012     Document Type: Article

References (92)

1. Abe Y, Toyosawa K. Age-related changes in rat hippocampal theta rhythms: a difference between type 1 and type 2 theta. J Vet Med Sci 61: 543-548, 1999.
2. Acquas E, Wilson C, Fibiger HC. Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation, and fear. J Neurosci 16: 3089-3096, 1996.
3. Barnes CA, Nadel L, Honig WK. Spatial memory deficit in senescent rats. Can J Psychol 34: 29-39, 1980.
4. Barry C, Heys JG, Hasselmo ME. Possible role of acetylcholine in regulating spatial novelty effects on theta rhythm and grid cells. Front Neural Circuits 6: 5, 2012.
5. Bartus RT, Dean RL 3rd, Beer B, Lippa AS. The cholinergic hypothesis of geriatric memory dysfunction. Science 217: 408-414, 1982.
6. Beninger RJ, Wirsching BA, Mallet PE, Jhamandas K, Boegman RJ. Physostigmine, but not 3,4-diaminopyridine, improves radial maze performance in memory-impaired rats. Pharmacol Biochem Behav 51: 739-746, 1995.
7. Bland BH. The physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26: 1-54, 1986.
8. Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15: 47-60, 1995.
9. Brandeis R, Dachir S, Sapir M, Levy A, Fisher A. Reversal of age-related cognitive impairments by an M1 cholinergic agonist, AF102B. Pharmacol Biochem Behav 36: 89-95, 1990.
10. Canolty RT, Knight RT. The functional role of cross-frequency coupling. Trends Cogn Sci 14: 506-515, 2010.
11. 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.
12. Chrobak JJ, Buzsaki G. Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18: 388-398, 1998a.
13. Chrobak JJ, Buzsaki G. Operational dynamics in the hippocampal-entorhinal axis. Neurosci Biobehav Rev 22: 303-310, 1998b.
14. 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.
15. Colgin LL, Moser EI. Gamma oscillations in the hippocampus. Physiology (Bethesda) 25: 319-329, 2010.
16. Crouzier D, Baubichon D, Bourbon F, Testylier G. Acetylcholine release, EEG spectral analysis, sleep staging and body temperature studies: a multiparametric approach on freely moving rats. J Neurosci Methods 151: 159-167, 2006.
17. Csicsvari J, Jamieson B, Wise KD, Buzsaki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37: 311-322, 2003.
18. Cutsuridis V, Cobb S, Graham BP. Encoding and retrieval in a model of the hippocampal CA1 microcircuit. Hippocampus 20: 423-446, 2010.
19. Decker MW, Pelleymounter MA, Gallagher M. Effects of training on a spatial memory task on high affinity choline uptake in hippocampus and cortex in young adult and aged rats. J Neurosci 8: 90-99, 1988.
20. Dimpfel W. Pharmacological modulation of cholinergic brain activity and its reflection in special EEG frequency ranges from various brain areas in the freely moving rat (Tele-Stereo-EEG). Eur Neuropsychopharmacol 15: 673-682, 2005.
21. Fadda F, Cocco S, Stancampiano R. Hippocampal acetylcholine release correlates with spatial learning performance in freely moving rats. Neuroreport 11: 2265-2269, 2000.
22. Frank LM, Stanley GB, Brown EN. Hippocampal plasticity across multiple days of exposure to novel environments. J Neurosci 24: 7681-7689, 2004.
23. Freund JA, Nikitin A, Stocks NG. Phase locking below rate threshold in noisy model neurons. Neural Comput 22: 599-620, 2010.
24. Frotscher M, Leranth C. Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J Comp Neurol 239: 237-246, 1985.
25. Giovannini MG, Rakovska A, Benton RS, Pazzagli M, Bianchi L, Pepeu G. Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience 106: 43-53, 2001.
26. Goldberg JM, Brown PB. Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 32: 613-636, 1969.
27. Gray JA, McNaughton N. Comparison between the behavioural effects of septal and hippocampal lesions: a review. Neurosci Biobehav Rev 7: 119-188, 1983.
28. Griffin AL, Asaka Y, Darling RD, Berry SD. Theta-contingent trial presentation accelerates learning rate and enhances hippocampal plasticity during trace eyeblink conditioning. Behav Neurosci 118: 403-411, 2004.
29. Gupta AS, van der Meer MA, Touretzky DS, Redish AD. Segmentation of spatial experience by hippocampal theta sequences. Nat Neurosci 15: 1032-1039, 2012.
30. Hagan JJ, Jansen JH, Broekkamp CL. Hemicholinium-3 impairs spatial learning and the deficit is reversed by cholinomimetics. Psychopharmacology (Berl) 98: 347-356, 1989.
31. 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.
32. Hasselmo ME, Bodelon 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.
33. Hentschke H, Perkins MG, Pearce RA, Banks MI. Muscarinic blockade weakens interaction of gamma with theta rhythms in mouse hippocampus. Eur J Neurosci 26: 1642-1656, 2007.
34. Hernandez CM, Gearhart DA, Parikh V, Hohnadel EJ, Davis LW, Middlemore ML, Warsi SP, Waller JL, Terry AV Jr. Comparison of galantamine and donepezil for effects on nerve growth factor, cholinergic markers, and memory performance in aged rats. J Pharmacol Exp Ther 316: 679-694, 2006.
35. Hinman JR, Penley SC, Long LL, Escabi MA, Chrobak JJ. Septotemporal variation in dynamics of theta: speed and habituation. J Neurophysiol 105: 2675-2686, 2011.
36. Hirshhorn M, Grady C, Rosenbaum RS, Winocur G, Moscovitch M. Brain regions involved in the retrieval of spatial and episodic details associated with a familiar environment: an fMRI study. Neuropsychologia 50: 3094-3106, 2012.
37. Holz EM, Glennon M, Prendergast K, Sauseng P. Theta-gamma phase synchronization during memory matching in visual working memory. Neuroimage 52: 326-335, 2010.
38. Hunsaker MR, Rogers JL, Kesner RP. Behavioral characterization of a transection of dorsal CA3 subcortical efferents: comparison with scopolamine and physostigmine infusions into dorsal CA3. Neurobiol Learn Mem 88: 127-136, 2007.
39. Huxter JR, Miranda JA, Dias R. The hippocampal physiology of approaching middle-age: early indicators of change. Hippocampus 22: 1923-1940, 2012.
40. Ikonen S, McMahan R, Gallagher M, Eichenbaum H, Tanila H. Cholinergic system regulation of spatial representation by the hippocampus. Hippocampus 12: 386-397, 2002.
41. Janas AM, Cunningham SC, Duffy KB, Devan BD, Greig NH, Holloway HW, Yu QS, Markowska AL, Ingram DK, Spangler EL. The cholinesterase inhibitor, phenserine, improves Morris water maze performance of scopolamine-treated rats. Life Sci 76: 1073-1081, 2005.
42. 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.
43. Jensen O, Colgin LL. Cross-frequency coupling between neuronal oscillations. Trends Cogn Sci 11: 267-269, 2007.
44. Jutras MJ, Buffalo EA. Synchronous neural activity and memory formation. Curr Opin Neurobiol 20: 150-155, 2010.
45. Klimesch W, Doppelmayr M, Yonelinas A, Kroll NE, Lazzara M, Rohm D, Gruber W. Theta synchronization during episodic retrieval: neural correlates of conscious awareness. Brain Res Cogn Brain Res 12: 33-38, 2001.
46. Kocsis B, Li S, Hajos M. Behavior-dependent modulation of hippocampal EEG activity by the selective norepinephrine reuptake inhibitor reboxetine in rats. Hippocampus 17: 627-633, 2007.
47. 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.
48. Kuo TB, Li JY, Hsieh SS, Chen JJ, Tsai CY, Yang CC. Effect of aging on treadmill exercise induced theta power in the rat. Age (Dordr) 32: 297-308, 2010.
49. Lamberty Y, Gower AJ. Cholinergic modulation of spatial learning in mice in a Morris-type water maze. Arch Int Pharmacodyn Ther 309: 5-19, 1991.
50. Lawson VH, Bland BH. The role of the septohippocampal pathway in the regulation of hippocampal field activity and behavior: analysis by the intraseptal microinfusion of carbachol, atropine, and procaine. Exp Neurol 120: 132-144, 1993.
51. Lee MG, Chrobak JJ, Sik A, Wiley RG, Buzsaki G. Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62: 1033-1047, 1994.
52. Lega BC, Jacobs J, Kahana M. Human hippocampal theta oscillations and the formation of episodic memories. Hippocampus 22: 748-761, 2012.
53. Leutgeb S, Mizumori SJ. Excitotoxic septal lesions result in spatial memory deficits and altered flexibility of hippocampal single-unit representations. J Neurosci 19: 6661-6672, 1999.
54. Light LL. Memory and aging: four hypotheses in search of data. Annu Rev Psychol 42: 333-376, 1991.
55. Lisman JE, Idiart MA. Storage of 7 / 2 short-term memories in oscillatory subcycles. Science 267: 1512-1515, 1995.
56. Manns JR, Howard MW, Eichenbaum H. Gradual changes in hippocampal activity support remembering the order of events. Neuron 56: 530-540, 2007a.
57. Manns JR, Zilli EA, Ong KC, Hasselmo ME, Eichenbaum H. Hippocampal CA1 spiking during encoding and retrieval: relation to theta phase. Neurobiol Learn Mem 87: 9-20, 2007b.
58. Markowska AL, Olton DS, Givens B. Cholinergic manipulations in the medial septal area: age-related effects on working memory and hippocampal electrophysiology. J Neurosci 15: 2063-2073, 1995.
59. McIntyre CK, Marriott LK, Gold PE. Patterns of brain acetylcholine release predict individual differences in preferred learning strategies in rats. Neurobiol Learn Mem 79: 177-183, 2003.
60. Montgomery SM, Betancur MI, Buzsaki G. Behavior-dependent coordination of multiple theta dipoles in the hippocampus. J Neurosci 29: 1381-1394, 2009.
61. Montgomery SM, Buzsaki G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proc Natl Acad Sci USA 104: 14495-14500, 2007.
62. Nyhus E, Curran T. Functional role of gamma and theta oscillations in episodic memory. Neurosci Biobehav Rev 34: 1023-1035, 2010.
63. Oler JA, Markus EJ. Age-related deficits in the ability to encode contextual change: a place cell analysis. Hippocampus 10: 338-350, 2000.
64. Olpe HR, Klebs K, Kung E, Campiche P, Glatt A, Ortmann R, D'Amato F, Pozza MF, Mondadori C. Cholinomimetics induce theta rhythm and reduce hippocampal pyramidal cell excitability. Eur J Pharmacol 142: 275-283, 1987.
65. Opello KD, Stackman RW, Ackerman S, Walsh TJ. AF64A (ethylcholine mustard aziridinium) impairs acquisition and performance of a spatial, but not a cued water maze task: relation to cholinergic hypofunction. Physiol Behav 54: 1227-1233, 1993.
66. Podol'skii IY, Vorob'ev VV, Belova NA. Long-term changes in hippocampus and neocortex EEG spectra in response to pharmacological treatments affecting the cholinergic system. Neurosci Behav Physiol 31: 589-595, 2001.
67. Quirion R, Wilson A, Rowe W, Aubert I, Richard J, Doods H, Parent A, White N, Meaney MJ. Facilitation of acetylcholine release and cognitive performance by an M2-muscarinic receptor antagonist in aged memoryimpaired. J Neurosci 15: 1455-1462, 1995.
68. Rapp PR, Rosenberg RA, Gallagher M. An evaluation of spatial information processing in aged rats. Behav Neurosci 101: 3-12, 1987.
69. Roark RM, Escabi MA. B-spline design of maximally flat and prolate spheroidal-type FIR filters. IEEE Trans Signal Processing 47: 701-716, 1999.
70. Rogers JL, Kesner RP. Cholinergic modulation of the hippocampus during encoding and retrieval. Neurobiol Learn Mem 80: 332-342, 2003.
71. Sava S, Markus EJ. Activation of the medial septum reverses age-related hippocampal encoding deficits: a place field analysis. J Neurosci 28: 1841-1853, 2008.
72. Schack B, Vath N, Petsche H, Geissler HG, Moller E. Phase-coupling of theta-gamma EEG rhythms during short-term memory processing. Int J Psychophysiol 44: 143-163, 2002.
73. Schliebs R, Arendt T. The cholinergic system in aging and neuronal degeneration. Behav Brain Res 221: 555-563, 2011.
74. Schmidt B, Hinman JR, Jacobson TK, Szkudlarek E, Argraves M, Escabi M, Markus EJ. Dissociation between dorsal and ventral hippocampal theta oscillations during a place and response task. J Neurosci. In press.
75. Seager MA, Johnson LD, Chabot ES, Asaka Y, Berry SD. Oscillatory brain states and learning: impact of hippocampal theta-contingent training. Proc Natl Acad Sci USA 99: 1616-1620, 2002.
76. Sederberg PB, Schulze-Bonhage A, Madsen JR, Bromfield EB, Litt B, Brandt A, Kahana MJ. Gamma oscillations distinguish true from false memories. Psychol Sci 18: 927-932, 2007a.
77. Sederberg PB, Schulze-Bonhage A, Madsen JR, Bromfield EB, McCarthy DC, Brandt A, Tully MS, Kahana MJ. Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cereb Cortex 17: 1190-1196, 2007b.
78. Shirvalkar PR, Rapp PR, Shapiro ML. Bidirectional changes to hippocampal theta-gamma comodulation predict memory for recent spatial episodes. Proc Natl Acad Sci USA 107: 7054-7059, 2010.
79. Smith DM, Mizumori SJ. Hippocampal place cells, context, and episodic memory. Hippocampus 16: 716-729, 2006.
80. Stanley EM, Fadel JR, Mott DD. Interneuron loss reduces dendritic inhibition and GABA release in hippocampus of aged rats. Neurobiol Aging 33: 431.e1-431.e13, 2012.
81. Stemmelin J, Cassel JC, Will B, Kelche C. Sensitivity to cholinergic drug treatments of aged rats with variable degrees of spatial memory impairment. Behav Brain Res 98: 53-66, 1999.
82. Stewart DJ, Vanderwolf CH. Hippocampal rhythmical slow activity following ibotenic acid lesions of the septal region. I. Relations to behavior and effects of atropine and urethane. Brain Res 423: 88-100, 1987.
83. Sugaya K, Greene R, Personett D, Robbins M, Kent C, Bryan D, Skiba E, Gallagher M, McKinney M. Septo-hippocampal cholinergic and neurotrophin markers in age-induced cognitive decline. Neurobiol Aging 19: 351-361, 1998.
84. Sullivan D, Csicsvari J, Mizuseki K, Montgomery S, Diba K, Buzsaki G. Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity. J Neurosci 31: 8605-8616, 2011.
85. Tort AB, Komorowski R, Eichenbaum H, Kopell N. Measuring phaseamplitude coupling between neuronal oscillations of different frequencies. J Neurophysiol 104: 1195-1210, 2010.
86. 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 USA 106: 20942-20947, 2009.
87. Wang T, Tang XC. Reversal of scopolamine-induced deficits in radial maze performance by (-)-huperzine A: comparison with E2020 and tacrine. Eur J Pharmacol 349: 137-142, 1998.
88. Welch PD. Use of fast Fourier transform for estimation of power spectra-a method based on time averaging over short modified periodograms. IEEE Trans Audio Electroacoust 15: 70-73, 1967.
89. Whishaw IQ. Cholinergic receptor blockade in the rat impairs locale but not taxon strategies for place navigation in a swimming pool. Behav Neurosci 99: 979-1005, 1985.
90. Womelsdorf T, Schoffelen JM, Oostenveld R, Singer W, Desimone R, Engel AK, Fries P. Modulation of neuronal interactions through neuronal synchronization. Science 316: 1609-1612, 2007.
91. Wyble BP, Hyman JM, Rossi CA, Hasselmo ME. Analysis of theta power in hippocampal EEG during bar pressing and running behavior in rats during distinct behavioral contexts. Hippocampus 14: 662-674, 2004.
92. Zyzak DR, Otto T, Eichenbaum H, Gallagher M. Cognitive decline associated with normal aging in rats: a neuropsychological approach. Learn Mem 2: 1-16, 1995.