Theta Phase Segregation of Input-Specific Gamma Patterns in Entorhinal-Hippocampal Networks

Neuron

Volumn 84, Issue 2, 2014, Pages 470-485

  Schomburg, Erik W ^a,b   Fernández Ruiz, Antonio ^a,c   Mizuseki, Kenji ^a,d   Berényi, Antal ^a,e   Anastassiou, Costas A ^b,d   Koch, Christof ^b,d   Buzsáki, György ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b California Institute of Technology   (United States)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^d ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^e UNIVERSITY OF SZEGED   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

AMPLITUDE MODULATION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGICAL PROCEDURES; ENTORHINAL CORTEX; GAMMA RHYTHM; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; INTERNEURON; LOCOMOTION; MALE; NONHUMAN; PYRAMIDAL NERVE CELL; RAT; REM SLEEP; STRATUM LACUNOSUM MOLECULARE; STRATUM PYRAMIDALE; STRATUM RADIATUM; THETA RHYTHM; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; LONG EVANS RAT; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; ENTORHINAL CORTEX; GAMMA RHYTHM; HIPPOCAMPUS; INTERNEURONS; MALE; MODELS, NEUROLOGICAL; PYRAMIDAL CELLS; RATS, LONG-EVANS; THETA RHYTHM;

EID: 84908247311     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.08.051     Document Type: Article

References (105)

1. Ainge J.A., van der Meer M.A.A., Langston R.F., Wood E.R. Exploring the role of context-dependent hippocampal activity in spatial alternation behavior. Hippocampus 2007, 17:988-1002.
2. Akam T.E., Kullmann D.M. Efficient "communication through coherence" requires oscillations structured to minimize interference between signals. PLoS Comput. Biol. 2012, 8:e1002760.
3. Amaral D.G., Witter M.P. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 1989, 31:571-591.
4. Aru, J., Aru, J., Priesemann, V., Wibral, M., Lana, L., Pipa, G., Singer, W., and Vicente, R. (2014) Untangling cross-frequency coupling in neuroscience. arXiv, arXiv:1405.7965, . http://arxiv.org/abs/1405.7965.
5. Bartos M., Vida I., Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 2007, 8:45-56.
6. Basu J., Srinivas K.V., Cheung S.K., Taniguchi H., Huang Z.J., Siegelbaum S.A. A cortico-hippocampal learning rule shapes inhibitory microcircuit activity to enhance hippocampal information flow. Neuron 2013, 79:1208-1221.
7. Belluscio M.A., Mizuseki K., Schmidt R., Kempter R., Buzsáki G. Cross-frequency phase-phase coupling between θ and γ oscillations in the hippocampus. J.Neurosci. 2012, 32:423-435.
8. Benito N., Fernández-Ruiz A., Makarov V.A., Makarova J., Korovaichuk A., Herreras O. Spatial modules of coherent activity in pathway-specific LFPs in the hippocampus reflect topology and different modes of presynaptic synchronization. Cereb. Cortex 2014, 24:1738-1752.
9. Berényi A., Somogyvári Z., Nagy A.J., Roux L., Long J.D., Fujisawa S., Stark E., Leonardo A., Harris T.D., Buzsáki G. Large-scale, high-density (up to 512 channels) recording of local circuits in behaving animals. J.Neurophysiol. 2014, 111:1132-1149.
10. Bieri K.W., Bobbitt K.N., Colgin L.L. Slow and fast γ rhythms coordinate different spatial coding modes in hippocampal place cells. Neuron 2014, 82:670-681.
11. Bosman C.A., Schoffelen J.-M., Brunet N., Oostenveld R., Bastos A.M., Womelsdorf T., Rubehn B., Stieglitz T., De Weerd P., Fries P. Attentional stimulus selection through selective synchronization between monkey visual areas. Neuron 2012, 75:875-888.
12. Bragin A., Jandó G., Nádasdy Z., Hetke J., Wise K., Buzsáki G. Gamma (40-100Hz) oscillation in the hippocampus of the behaving rat. J.Neurosci. 1995, 15:47-60.
13. Brankack J., Stewart M., Fox S.E. Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators. Brain Res. 1993, 615:310-327.
14. Brun V.H., Leutgeb S., Wu H.-Q., Schwarcz R., Witter M.P., Moser E.I., Moser M.-B. Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron 2008, 57:290-302.
15. Brunel N., Wang X.J. What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. J.Neurophysiol. 2003, 90:415-430.
16. Brunet N.M., Bosman C.A., Vinck M., Roberts M., Oostenveld R., Desimone R., De Weerd P., Fries P. Stimulus repetition modulates gamma-band synchronization in primate visual cortex. Proc. Natl. Acad. Sci. USA 2014, 111:3626-3631.
17. Buzsáki G. Feed-forward inhibition in the hippocampal formation. Prog. Neurobiol. 1984, 22:131-153.
18. Buzsáki G. Theta oscillations in the hippocampus. Neuron 2002, 33:325-340.
19. Buzsáki G., Wang X.-J. Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 2012, 35:203-225.
20. Buzsáki G., Leung L.W., Vanderwolf C.H. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 1983, 287:139-171.
21. Buzsáki G., Czopf J., Kondákor I., Kellényi L. Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: current-source density analysis, effects of urethane and atropine. Brain Res. 1986, 365:125-137.
22. Buzsáki G., Penttonen M., Bragin A., Nádasdy Z., Chrobak J.J. Possible physiological role of the perforant path-CA1 projection. Hippocampus 1995, 5:141-146.
23. Buzsáki G., Anastassiou C.A., Koch C. The origin of extracellular fields and currents-EEG, ECoG, LFP and spikes. Nat. Rev. Neurosci. 2012, 13:407-420.
24. Cabral H.O., Vinck M., Fouquet C., Pennartz C.M.A., Rondi-Reig L., Battaglia F.P. Oscillatory dynamics and place field maps reflect hippocampal ensemble processing of sequence and place memory under NMDA receptor control. Neuron 2014, 81:402-415.
25. Canolty R.T., Knight R.T. The functional role of cross-frequency coupling. Trends Cogn. Sci. 2010, 14:506-515.
26. Carr M.F., Karlsson M.P., Frank L.M. Transient slow gamma synchrony underlies hippocampal memory replay. Neuron 2012, 75:700-713.
27. Colgin L.L., Denninger T., Fyhn M., Hafting T., Bonnevie T., Jensen O., Moser M.-B., Moser E.I. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 2009, 462:353-357.
28. Csicsvari J., Hirase H., Czurko A., Buzsáki G. Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 1998, 21:179-189.
29. Csicsvari J., Hirase H., Czurkó A., Mamiya A., Buzsáki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat. J.Neurosci. 1999, 19:274-287.
30. Csicsvari J., Hirase H., Mamiya A., Buzsáki G. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 2000, 28:585-594.
31. Csicsvari J., Jamieson B., Wise K.D., Buzsáki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 2003, 37:311-322.
32. Diba K., Buzsáki G. Hippocampal network dynamics constrain the time lag between pyramidal cells across modified environments. J.Neurosci. 2008, 28:13448-13456.
33. Dudman J.T., Tsay D., Siegelbaum S.A. A role for synaptic inputs at distal dendrites: instructive signals for hippocampal long-term plasticity. Neuron 2007, 56:866-879.
34. Dvorak-Carbone H., Schuman E.M. Long-term depression of temporoammonic-CA1 hippocampal synaptic transmission. J.Neurophysiol. 1999, 81:1036-1044.
35. Dvorak-Carbone H., Schuman E.M. Patterned activity in stratum lacunosum moleculare inhibits CA1 pyramidal neuron firing. J.Neurophysiol. 1999, 82:3213-3222.
36. Einevoll G.T., Kayser C., Logothetis N.K., Panzeri S. Modelling and analysis of local field potentials for studying the function of cortical circuits. Nat. Rev. Neurosci. 2013, 14:770-785.
37. Fell J., Axmacher N. The role of phase synchronization in memory processes. Nat. Rev. Neurosci. 2011, 12:105-118.
38. Fernández-Ruiz A., Herreras O. Identifying the synaptic origin of ongoing neuronal oscillations through spatial discrimination of electric fields. Front Comput Neurosci 2013, 7:5.
39. Fernández-Ruiz A., Makarov V.A., Benito N., Herreras O. Schaffer-specific local field potentials reflect discrete excitatory events at gamma frequency that may fire postsynaptic hippocampal CA1 units. J.Neurosci. 2012, 32:5165-5176.
40. Fishell G., Rudy B. Mechanisms of inhibition within the telencephalon: "where the wild things are". Ann. Rev. Neurosci. 2011, 34:535-567.
41. Freund T.F., Buzsáki G. Interneurons of the hippocampus. Hippocampus 1996, 6:347-470.
42. Fries P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 2005, 9:474-480.
43. Fries P. Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 2009, 32:209-224.
44. Galarreta M., Hestrin S. Spike transmission and synchrony detection in networks of GABAergic interneurons. Science 2001, 292:2295-2299.
45. Glickfeld L.L., Roberts J.D., Somogyi P., Scanziani M. Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis. Nat. Neurosci. 2009, 12:21-23.
46. Golding N.L., Staff N.P., Spruston N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 2002, 418:326-331.
47. Golding N.L., Mickus T.J., Katz Y., Kath W.L., Spruston N. Factors mediating powerful voltage attenuation along CA1 pyramidal neuron dendrites. J.Physiol. 2005, 568:69-82.
48. Gregoriou G.G., Gotts S.J., Zhou H., Desimone R. High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 2009, 324:1207-1210.
49. Gregoriou G.G., Gotts S.J., Desimone R. Cell-type-specific synchronization of neural activity in FEF with V4 during attention. Neuron 2012, 73:581-594.
50. Han E.B., Heinemann S.F. Distal dendritic inputs control neuronal activity by heterosynaptic potentiation of proximal inputs. J.Neurosci. 2013, 33:1314-1325.
51. Hargreaves E.L., Rao G., Lee I., Knierim J.J. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 2005, 308:1792-1794.
52. Hasselmo M.E., Bodelón C., Wyble B.P. A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput. 2002, 14:793-817.
53. Henriksen E.J., Colgin L.L., Barnes C.A., Witter M.P., Moser M.-B., Moser E.I. Spatial representation along the proximodistal axis of CA1. Neuron 2010, 68:127-137.
54. Hu H., Martina M., Jonas P. Dendritic mechanisms underlying rapid synaptic activation of fast-spiking hippocampal interneurons. Science 2010, 327:52-58.
55. Igarashi K.M., Lu L., Colgin L.L., Moser M.-B., Moser E.I. Coordination of entorhinal-hippocampal ensemble activity during associative learning. Nature 2014, 510:143-147.
56. Isaacson J.S., Scanziani M. How inhibition shapes cortical activity. Neuron 2011, 72:231-243.
57. Jarsky T., Roxin A., Kath W.L., Spruston N. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2005, 8:1667-1676.
58. Jia X., Tanabe S., Kohn A. γ and the coordination of spiking activity in early visual cortex. Neuron 2013, 77:762-774.
59. Kamondi A., Acsády L., Wang X.J., Buzsáki G. Theta oscillations in somata and dendrites of hippocampal pyramidal cells invivo: activity-dependent phase-precession of action potentials. Hippocampus 1998, 8:244-261.
60. Klausberger T., Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008, 321:53-57.
61. Kopell N., Ermentrout G.B., Whittington M.A., Traub R.D. Gamma rhythms and beta rhythms have different synchronization properties. Proc. Natl. Acad. Sci. USA 2000, 97:1867-1872.
62. Lasztóczi B., Klausberger T. Layer-specific GABAergic control of distinct gamma oscillations in the CA1 hippocampus. Neuron 2014, 81:1126-1139.
63. Leão R.N., Mikulovic S., Leão K.E., Munguba H., Gezelius H., Enjin A., Patra K., Eriksson A., Loew L.M., Tort A.B.L., Kullander K. OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons. Nat. Neurosci. 2012, 15:1524-1530.
64. Lever C., Burton S., Jeewajee A., Wills T.J., Cacucci F., Burgess N., O'Keefe J. Environmental novelty elicits a later theta phase of firing in CA1 but not subiculum. Hippocampus 2010, 20:229-234.
65. Lisman J.E., Jensen O. The θ-γ neural code. Neuron 2013, 77:1002-1016.
66. 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. 2007, 87:9-20.
67. Mizuseki K., Sirota A., Pastalkova E., Buzsáki G. Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 2009, 64:267-280.
68. Mizuseki K., Diba K., Pastalkova E., Buzsáki G. Hippocampal CA1 pyramidal cells form functionally distinct sublayers. Nat. Neurosci. 2011, 14:1174-1181.
69. Mizuseki K., Royer S., Diba K., Buzsáki G. Activity dynamics and behavioral correlates of CA3 and CA1 hippocampal pyramidal neurons. Hippocampus 2012, 22:1659-1680.
70. Mizuseki K., Diba K., Pastalkova E., Teeters J., Sirota A., Buzsáki G. Neurosharing: large-scale data sets (spike, LFP) recorded from the hippocampal-entorhinal system in behaving rats. F1000Res 2014, 3:98.
71. Montgomery S.M., Buzsáki G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proc. Natl. Acad. Sci. USA 2007, 104:14495-14500.
72. Montgomery S.M., Sirota A., Buzsáki G. Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep. J.Neurosci. 2008, 28:6731-6741.
73. Montgomery S.M., Betancur M.I., Buzsáki G. Behavior-dependent coordination of multiple theta dipoles in the hippocampus. J.Neurosci. 2009, 29:1381-1394.
74. Naber P.A., Lopes da Silva F.H., Witter M.P. Reciprocal connections between the entorhinal cortex and hippocampal fields CA1 and the subiculum are in register with the projections from CA1 to the subiculum. Hippocampus 2001, 11:99-104.
75. Nicholson C., Freeman J.A. Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. J.Neurophysiol. 1975, 38:356-368.
76. O'Keefe J., Nadel L. The Hippocampus as a Cognitive Map 1978, Clarendon Press, Oxford.
77. O'Keefe J., Recce M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 1993, 3:317-330.
78. Pastalkova E., Itskov V., Amarasingham A., Buzsáki G. Internally generated cell assembly sequences in the rat hippocampus. Science 2008, 321:1322-1327.
79. Poe G.R., Nitz D.A., McNaughton B.L., Barnes C.A. Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res. 2000, 855:176-180.
80. Pouille F., Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 2001, 293:1159-1163.
81. Ray S., Maunsell J.H.R. Differences in gamma frequencies across visual cortex restrict their possible use in computation. Neuron 2010, 67:885-896.
82. Ray S., Maunsell J.H.R. Different origins of gamma rhythm and high-gamma activity in macaque visual cortex. PLoS Biol. 2011, 9:e1000610.
83. Remondes M., Schuman E.M. Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature 2002, 416:736-740.
84. Scheffer-Teixeira R., Belchior H., Leão R.N., Ribeiro S., Tort A.B.L. On high-frequency field oscillations (>100Hz) and the spectral leakage of spiking activity. J.Neurosci. 2013, 33:1535-1539.
85. Schomburg E.W., Anastassiou C.A., Buzsáki G., Koch C. The spiking component of oscillatory extracellular potentials in the rat hippocampus. J.Neurosci. 2012, 32:11798-11811.
86. Shadlen M.N., Movshon J.A. Synchrony unbound: a critical evaluation of the temporal binding hypothesis. Neuron 1999, 24:67-77. 111-125.
87. Singer W. Synchronization of cortical activity and its putative role in information processing and learning. Annu. Rev. Physiol. 1993, 55:349-374.
88. Sirota A., Montgomery S., Fujisawa S., Isomura Y., Zugaro M., Buzsáki G. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 2008, 60:683-697.
89. Srinath R., Ray S. Effect of amplitude correlations on coherence in the local field potential. J.Neurophysiol. 2014, 112:741-751.
90. Stark E., Roux L., Eichler R., Senzai Y., Royer S., Buzsáki G. Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations. Neuron 2014, 83:467-480.
91. Stewart M., Quirk G.J., Barry M., Fox S.E. Firing relations of medial entorhinal neurons to the hippocampal theta rhythm in urethane anesthetized and walking rats. Exp. Brain Res. 1992, 90:21-28.
92. Sullivan D., Csicsvari J., Mizuseki K., Montgomery S., Diba K., Buzsáki G. Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity. J.Neurosci. 2011, 31:8605-8616.
93. Takahashi H., Magee J.C. Pathway interactions and synaptic plasticity in the dendritic tuft regions of CA1 pyramidal neurons. Neuron 2009, 62:102-111.
94. Tort A.B.L., 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 2009, 106:20942-20947.
95. Tort A.B.L., Komorowski R., Eichenbaum H., Kopell N. Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. J.Neurophysiol. 2010, 104:1195-1210.
96. Vaidya S.P., Johnston D. Temporal synchrony and gamma-to-theta power conversion in the dendrites of CA1 pyramidal neurons. Nat. Neurosci. 2013, 16:1812-1820.
97. Varga C., Golshani P., Soltesz I. Frequency-invariant temporal ordering of interneuronal discharges during hippocampal oscillations in awake mice. Proc. Natl. Acad. Sci. USA 2012, 109:E2726-E2734.
98. Vertes R.P., Hoover W.B., Szigeti-Buck K., Leranth C. Nucleus reuniens of the midline thalamus: link between the medial prefrontal cortex and the hippocampus. Brain Res. Bull. 2007, 71:601-609.
99. Witter M.P., Groenewegen H.J., Lopes da Silva F.H., Lohman A.H. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol. 1989, 33:161-253.
100. Wood E.R., Dudchenko P.A., Robitsek R.J., Eichenbaum H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 2000, 27:623-633.
101. Yamamoto J., Suh J., Takeuchi D., Tonegawa S. Successful execution of working memory linked to synchronized high-frequency gamma oscillations. Cell 2014, 157:845-857.
102. Yeckel M.F., Berger T.W. Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the roleof the trisynaptic pathway. Proc. Natl. Acad. Sci. USA 1990, 87:5832-5836.
103. Zador A.M., Agmon-Snir H., Segev I. The morphoelectrotonic transform: a graphical approach to dendritic function. J.Neurosci. 1995, 15:1669-1682.
104. Zanos T.P., Mineault P.J., Pack C.C. Removal of spurious correlations between spikes and local field potentials. J.Neurophysiol. 2011, 105:474-486.
105. Zemankovics R., Veres J.M., Oren I., Hájos N. Feedforward inhibition underlies the propagation of cholinergically induced gamma oscillations from hippocampal CA3 to CA1. J.Neurosci. 2013, 33:12337-12351.