Influence of slow oscillation on hippocampal activity and ripples through cortico-hippocampal synaptic interactions, analyzed by a cortical-CA3-CA1 network model

Frontiers in Computational Neuroscience

Volumn , Issue JAN, 2013, Pages

  Taxidis, Jiannis ^a,b   Mizuseki, Kenji ^c,d   Mason, Robert ^a   Owen, Markus R ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c RUTGERS UNIVERSITY   (United States)

^d ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPUTATIONAL NETWORKS; CORTICAL NETWORK; COUPLING MECHANISM; FEED-BACK LOOP; HIPPOCAMPAL ACTIVITY; IN-VIVO; LONG-TERM STORAGE; MEMORY CONSOLIDATION; MOSSY FIBERS; NETWORK MODELS; PYRAMIDAL CELL; SCHAFFER COLLATERALS; SLOW OSCILLATIONS; SYNAPTIC INTERACTIONS; SYNCHRONOUS DISCHARGE;

EXCITED STATES; SLEEP RESEARCH;

BRAIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; MALE; MEMORY CONSOLIDATION; NEUROPHYSIOLOGY; NONHUMAN; OSCILLATION; PYRAMIDAL NERVE CELL; RAT; SIMULATION; SLOW OSCILLATION; SYNAPSE;

EID: 84873192983     PISSN: 16625188     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncom.2013.00003     Document Type: Article

References (94)

1. Acsady, L., Kamondi, A., Sik, A., Freund, T., and Buzsáki, G. (1998). GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J. Neurosci. 18, 3386-3403.
2. Amaral, D. G., Ishizuka, N., and Claiborne, B. (1990). Neurons, numbers and the hippocampal network. Prog. Brain Res. 83, 1-11.
3. Amaral, D. G., Witter, M. P. (1989). The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571-91.
4. Andersen, P., Morris, R., Amaral, D., Bliss, T., and O'Keefe, J. (2007). The hippocampus book. Oxford University Press, USA.
5. Baccalá, L. A., and Sameshima, K. (2001). Partial directed coherence: a new concept in neural structure determination. Biol. Cybern. 84, 463-474.
6. Bartos, M., Vida, I., and Jonas, P. (2007). Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 8, 45-56.
7. Battaglia, F. P., Sutherland, G. R., and McNaughton, B. L. (2004). Hippocampal sharp wave bursts coincide with neocortical "up-state" transitions. Learn. Mem. 11, 697-704.
8. Bazhenov, M., Timofeev, I., Steriade, M., and Sejnowski, T. J. (2002). Model of thalamocortical slow-wave sleep oscillations and transitions to activated states. J. Neurosci. 22, 8691-8704.
9. Berens, P. (2009). CircStat: A MATLAB Toolbox for Circular Statistics. J. Stat. Softw. 31, 1-21.
10. Bernard, C., and Wheal, H. V. (1994). Model of local connectivity patterns in CA3 and CA1 areas of the hippocampus. Hippocampus 4, 497-529.
11. Buhl, E. H., Halasy, K., and Somogyi, P. (1994). Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368, 823-828.
12. Buzsáki, G. (1989). Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 31, 551-570.
13. Buzsáki, G. (2006). Rhythms of the Brain. Oxford University Press, USA.
14. Buzsáki, G., Horvath, Z., Urioste, R., Hetke, J., and Wise, K. (1992). High-frequency network oscillation in the hippocampus. Science 256, 1025-1027.
15. Chrobak, J. J., and Buzsáki, G. (1996). High-frequency oscillations in the out-put networks of the hippocampal-entorhinal axis of the freely behaving rat. J. Neurosci. 16, 3056-3066.
16. Cobb, S. R., Buhl, E. H., Halasy, K., Paulsen, O., and Somogyi, P. (1995). Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75-78.
17. Colbert, C. M., and Levy, W. B. (1992). Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J. Neurophys. 68, 1-8.
18. Compte, A., Reig, R., Descalzo, V. F., Harvey, M. A., Puccini, G. D., and Sanchez-Vives, M. V. (2008). Spontaneous high-frequency (10-80 Hz) oscillations during up states in the cerebral cortex in vitro. J. Neurosci. 28, 13,828-13,844.
19. Compte, A., Sanchez-Vives, M. V., McCormick, D. A., and Wang, X. J. (2003). Cellular and network mechanisms of slow oscillatory activity (<1 Hz) and wave propagations in a cortical network model. J. Neurophys. 89, 2707-2725.
20. Csicsvari, J., Hirase, H., Czurko, A., Mamiya, A., and Buzsáki, G. (1999). Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J. Neurosci. 19, 274-287.
21. Csicsvari, J., Hirase, H., Mamiya, A., and Buzsáki, G. (2000). Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28, 585-594.
22. Cutsuridis, V., Graham, B., Cobb, S., and Vida, I. (2010). Hippocampal Microcircuits: A Computational Modeler's Resource Book. Springer Verlag.
23. Cutsuridis, V., and Hasselmo, M. (2010). Dynamics and function of a CA1 model of the hippocampus during theta and ripples. Artif. Neural Netw.-ICANN 2010, 230-240.
24. Cutsuridis, V., and Hasselmo, M. (2011). Spatial memory sequence encoding and replay during modeled theta and ripple oscillations. Cogn. Comput. 1-21.
25. Diba, K., and Buzsáki, G. (2007). Forward and reverse hippocampal place-cell sequences during ripples. Nat. Neurosci. 10, 1241-1242.
26. Dickson, C. T., Wolansky, T. D., and Kerber, J. W. (2005). Neocortical modulation of the hippocampal slow oscillation via the entorhinal cortex. Soc. Neurosci. Abstr. 31, 275-273.
27. Eichenbaum, H. (2000). A cortical-hippocampal system for declarative memory. Nat. Rev. Neurosci. 1, 41-50.
28. Ellender, T. J., Nissen, W., Colgin, L. L., Mann, E. O., and Paulsen, O. (2010). Priming of hippocampal population bursts by individual perisomatic-targeting interneurons. J. Neurosci. 30, 5979-5991.
29. Empson, R. M., and Heinemann, U. (1995). The perforant path projection to hippocampal area CA1 in the rat hippocampal-entorhinal cortex combined slice. J. Physiol. 484, 707-720.
30. Fernández-Ruiz, A., Makarov, V. A., Benito, N., and Herreras, O. (2012). Schaffer-specific local field potentials reflect discrete excitatory events at gamma frequency that may fire postsynaptic hippocampal CA1 units. J. Neurosci. 32, 5165-5176.
31. Foster, D. J., and Wilson, M. A. (2006). Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440, 680-683.
32. Freund, T. F., and Buzsáki, G. (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
33. Gabbott, P., Headlam, A., and Busby, S. (2002). Morphological evidence that CA1 hippocampal afferents monosynaptically innervate PV-containing neurons and NADPH-diaphorase reactive cells in the medial prefrontal cortex (Areas 25/32) of the rat. Brain. Res. 946, 314-322.
34. Girardeau, G., Benchenane, K., Wiener, S. I., Buzsáki, G., and Zugaro, M. B. (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 12, 1222-1223.
35. Goodman, D., and Brette, R. (2008). Brian: a simulator for spiking neural networks in Python. Front. Neuroinf. 2, 1-10.
36. Gulyás, A. I., Miles, R., Sik, A., Toth, K., Tamamaki, N., and Freund, T. F. (1993). Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366, 683-687.
37. Hahn, T. T. G., McFarland, J. M., Berberich, S., Sakmann, B., and Mehta, M. R. (2012). Spontaneous persistent activity in entorhinal cortex modulates cortico-hippocampal interaction in vivo. Nat. Neurosci. 15, 1531-1538.
38. Hahn, T. T. G., Sakmann, B., and Mehta, M. R. (2006). Phase-locking of hippocampal interneurons' membrane potential to neocortical up-down states. Nat. Neurosci. 9, 1359-1361.
39. Hahn, T. T. G., Sakmann, B., and Mehta, M. R. (2007). Differential responses of hippocampal subfields to cortical up-down states. Proc. Natl. Acad. Sci. 104, 5169-5174.
40. Halliday, D. M., and Rosenberg, J. R. (1999). Time and frequency domain analysis of spike train and time series data. In: Modern Techniques in Neuroscience Research, ed. Windhorst, U., Johansson, H., Springer-Verlag.
41. Harris, K. D., Henze, D. A., Csicsvari, J., Hirase, H., and Buzsáki, G. (2000) Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J. Neurophys. 84, 401-414.
42. Harris, K. D., Hirase, H., Leinekugel, X., Henze, D. A., and Buzsáki, G. (2001). Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron 32, 141-149.
43. Hazan, L., Zugaro, M., and Buzsáki, G. (2006). Klusters, NeuroScope, NDManager: a Free Software Suite for Neurophysiological Data Processing and Visualization. J. Neurosci. Methods 155, 207-216.
44. Henze, D. A., Wittner, L., and Buzsáki, G. (2002). Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat. Neurosci. 5, 790-795.
45. Hill, S., and Tononi, G. (2005). Modeling sleep and wakefulness in the thalamocortical system. J. Neurophys. 93, 1671-1698.
46. Holcman, D., and Tsodyks, M. (2006). The emergence of up and down states in cortical networks. PLoS Comput. Biol. 2, 174-181.
47. Isomura, Y., Sirota, A., Özen, S., Montgomery, S., Mizuseki, K., Henze D. A., and Buzsáki, G. (2006). Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 52, 871-882.
48. Jarsky, T., Roxin, A., Kath, W. L., and Spruston, N. (2005). Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat. Neurosci. 8, 1667-1676.
49. Jonas, P., Major, G., and Sakmann, B. (1993). Quantal components of unitary EPSCs at the mossy fiber synapse on CA3 pyramidal cells of rat hippocampus. J. Physiol. 472, 615-663.
50. Klausberger, T., Magill, P. J., Márton, L. F., Roberts, J. D. B., Cobden, P. M., Buzsáki, G., and Somogyi, P. (2003). Brain-state-and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421, 844-848.
51. Klausberger, T., and Somogyi, P. (2008). Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53-57.
52. Knowles, W. D., and Schwartzkroin, P. A. (1981). Local circuit synaptic interactions in hippocampal brain slices. J. Neurosci. 1, 318-322.
53. Lawrence, J. J., Grinspan, Z. M., and McBain, C. J. (2004). Quantal transmission at mossy fiber targets in the CA3 region of the rat hippocampus. J. Physiol. 554, 175-193.
54. 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., and Kullander, K. (2012). OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons. Nat. Neurosci. 15, 1524-1530.
55. Lee, A. K., and Wilson, M. A. (2002). Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183-1194.
56. Li, X. J., Somogyi, P., Ylinen, A., and Buzsáki, G. (1994). The hippocampal CA3 network: an in vivo intracellular labeling study. J. Comp. Neurol. 339, 181-208.
57. Lovett-Barron, M., Turi, G. F., Kaifosh, P., Lee, P. H., Bolze, F., Sun, X., Nicoud, J., Zemelman, B. V., Sternson S. M., and Losonczy, A. (2012). Regulation of neuronal input transformations by tunable dendritic inhibition. Nat. Neurosci. 15, 423-430.
58. Maier, N., Nimmrich, V., and Draguhn, A. (2003). Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices. J. Physiol. 550, 873-887.
59. Mehta, M. R. (2007). Cortico-hippocampal interaction during up-down states and memory consolidation. J. Neurosci. 10, 13-15.
60. Miles, R., Traub, R. D., and Wong, R. K. (1988). Spread of synchronous firing in longitudinal slices from the CA3 region of the hippocampus. J. Neurophysiol. 60, 1481-1496.
61. Mizuseki, K., Diba, K., Pastalkova, E., and Buzsáki, G. (2011). Hippocampal CA1 pyramidal cells form functionally distinct sublayers. Nat. Neurosci. 14, 1174-1181.
62. Mizuseki, K., Sirota, A., Pastalkova, E., and Buzsáki, G. (2009). Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 64, 267-280.
63. Mölle, M., Yeshenko, O., Marshall, L., Sara, S. J., and Born, J. (2006). Hippocampal sharp waveripples linked to slow oscillations in rat slow-wave sleep. J. Neurophys. 96, 62-70.
64. Mori, M., Abegg, M. H., Gähwiler, B. H., and Gerber, U. (2004). A frequency-dependent switch from inhibition to excitation in a hippocampal unitary circuit. Nature 431, 453-456.
65. Parga, N., and Abbott, L. F. (2007). Network model of spontaneous activity exhibiting synchronous transitions between up and down states. Front. Neurosci. 1, 57-66.
66. Peyrache, A., Khamassi, M., Benchenane, K., Wiener, S. I., and Battaglia, F. P. (2009). Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat. Neurosci. 12, 919-926.
67. Phillips, K. G., Bartsch, U., McCarthy, A. P., Edgar, D. M., Tricklebank, M. D., Wafford, K. A., and Jones, M. W. (2012). Decoupling of sleep-dependent cortical and hippocampal interactions in a neurodevelopmental model of schizophrenia. Neuron, 76, 526-533.
68. Pinsky, P. F., and Rinzel, J. (1994). Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons. J. Comput. Neurosci. 1, 39-60.
69. Otmakhova, N. A., Otmakhov, N., and Lisman, J. E. (2002). Pathway-specific properties of AMPA and NMDA-mediated transmission in CA1 hippocampal pyramidal cells. J. Neurosci. 22, 1199-1207.
70. Remondes, M., and Schuman, E. M. (2002). Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature 416, 736-740.
71. Remondes, M., and Schuman, E. M. (2004). Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature 431, 699-703.
72. Royer, S., Zemelman, B. V., Losonczy, A., Kim, J., Chance, F., Magee, J. C., and Buzsáki, G. (2012). Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat. Neurosci. 15, 769-775.
73. Sanchez-Vives, M. V., and McCormick, D. A. (2000). Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027-1034.
74. Sayer, R. J., Friedlander, M. J., and Redman, S. J. (1990). The time course and amplitude of EPSPs evoked at synapses between pairs of CA3/CA1 neurons in the hippocampal slice. J. Neurosci. 10, 826-836.
75. Siapas, A. G., and Wilson, M. A. (1998). Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21, 1123-1128.
76. Sik, A., Tamamaki, N., and Freund, T. F. (1993). Complete axon arborization of a single CA3 pyramidal cell in the rat hippocampus, and its relationship with postsynaptic parvalbumincontaining interneurons. Eur. J. Neurosci. 5, 1719-1728.
77. Sirota, A., Montgomery, S., Fujisawa, S., Isomura, Y., Zugaro, M., and Buzsáki, G. (2008). Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60, 683-697.
78. Sirota, A., Csicsvari, J., Buhl, D., and Buzsáki, G. (2003). Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. 100, 2065-2069.
79. Skaggs, W. E., and McNaughton, B. L. (1996). Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271, 1870-1873.
80. Sorra, K. E., and Harris, K. M. (1993). Occurrence and three-dimensional structure of multiple synapses between individual radiatum axons and their target pyramidal cells in hippocampal area CA1. J. Neurosci. 13, 3736-3748.
81. Steriade, M. (2006). Grouping of brain rhythms in corticothalamic systems. Neuroscience 137, 1087-1106.
82. Suh, J., Rivest, A. J., Nakashiba, T., Tominaga, T., and Tonegawa, S. (2011). Entorhinal cortex layer III input to the hippocampus is crucial for temporal association memory. Science 334, 1415-1420.
83. Sullivan, D., Csicsvari, J., Mizuseki, K., Montgomery, S., Diba, K., and Buzsáki, G. (2011). Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: Influence of dentate and entorhinal cortical activity. J. Neurosci. 31, 8605-8616.
84. Takahashi, N., Kitamura, K., Matsuo, N., Mayford, M., Kano, M., Matsuki, N., and Ikegaya, Y. (2012). Locally synchronized synaptic inputs. Science 335, 353-356.
85. Taxidis, J., Coomber, B., Mason, R., and Owen, M. R. (2010). Assessing cortico-hippocampal functional connectivity under anesthesia and kainic acid using generalized partial directed coherence. Biol. Cybern. 102, 327-340.
86. Taxidis, J., Coombes, S., Mason, R., and Owen, M. R. (2012). Modeling sharp wave-ripple complexes through a CA3-CA1 network model with chemical synapses. Hippocampus, 22, 995-1017.
87. Timofeev, I., Grenier, F., Bazhenov, M., Sejnowski, T. J., and Steriade, M. (2000). Origin of slow cortical oscillations in deafferented cortical slabs. Cereb. Cortex 10, 1185-1199.
88. Timofeev, I., and Steriade, M. (1996). Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. J. Neurophys. 76, 4152-4168.
89. Traub, R. D., Jefferys, J. G., and Whittington, M. A. (1999). Fast oscillations in cortical circuits. The MIT Press, Cambridge, Messachusetts, USA.
90. Traub, R. D., and Miles, R. (1991). Neuronal networks of the hippocampus. Cambridge University, Press, New York, USA.
91. Wang, X. J., and Buzsáki, G. (1996). Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J. Neurosci. 16, 6402-6413.
92. Wolansky, T., Clement, E. A., Peters, S. R., Palczak, M. A., and Dickson, C. T. (2006). Hippocampal slow oscillation: a novel EEG state and its coordination with ongoing neocortical activity. J. Neurosci. 26, 6213-6229.
93. Yamamoto, C., D., Higashima, M., and Sawada, S. (1987). Quantal analysis of potentiating action of phorbolester on synaptic transmission in the hippocampus. Neurosci. Res. 5, 28-38.
94. Ylinen, A., Bragin, A., Nadasdy, Z., Jando, G., Szabo, I., Sik, A., and Buzsáki, G. (1995). Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15, 30-46.