Spatial Memory Sequence Encoding and Replay During Modeled Theta and Ripple Oscillations

Cognitive Computation

Volumn 3, Issue 4, 2011, Pages 554-574

  Cutsuridis, Vassilis ^a,b   Hasselmo, Michael ^a  

^a BOSTON UNIVERSITY   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Calcium; Computational model; Hippocampus; Inhibitory interneurons; Medial septum; Region CA1; Ripples; Spike timing dependent plasticity; Theta

Indexed keywords

COMPUTATIONAL MODEL; HIPPOCAMPUS; INHIBITORY INTERNEURONS; MEDIAL SEPTUM; REGION CA1; RIPPLES; SPIKE-TIMING-DEPENDENT PLASTICITY; THETA;

CALCIUM; CELLS; COMPUTATIONAL METHODS; NEURAL NETWORKS; NEURONS;

BRAIN;

EID: 82555168323     PISSN: 18669956     EISSN: 18669964     Source Type: Journal    
DOI: 10.1007/s12559-011-9114-3     Document Type: Article

References (76)

1. Amit DJ. Modeling brain function: the world of attractor neural networks. New York: Cambridge University Press; 1989.
2. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barionuevo G, et al. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci. 2008; 9(7): 557-68.
3. Baude A, Bleasdale C, Dalezios Y, Somogyi P, Klausberger T. Immunoreactivity for the GABAA receptor alpha1 subunit, somatostatin and Connexin36 distinguishes axoaxonic, basket, and bistratified interneurons of the rat hippocampus. Cerebral Cortex. 2007; 17(9): 2094-107.
4. Borhegyi Z, Varga V, Szilagyi N, Fabo D, Freund TF. Phase segregation of medial septal GABAergic neurons during hippocampal theta activity. J Neurosci. 2004; 24(39): 8470-9.
5. Brun VH, Leutgeb S, Wu HQ, Schwarcz R, Witter MP, Moser EI, Moser MB. Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron. 2008; 57(2): 290-302.
6. Brun VH, Otnass MK, Molden S, Steffenach HA, Witter MP, Moser MB, Moser EI. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science. 2002; 296(5576): 2243-6.
7. Buzsaki G. Two stage model of memory trace formation: a role for "noisy" brain states. Neuroscience. 1989; 31(3): 551-70.
8. Buzsaki G. Theta oscillations in the hippocampus. Neuron. 2002; 33: 325-40.
9. Buzsaki G, Horvath Z, Urioste R, Hetke J, Wise K. High-frequency network oscillation in the hippocampus. Science. 1992; 25: 1025-7.
10. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature. 1995; 378(6552): 75-8.
11. 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. 2009; 462(19): 353-8.
12. Cutsuridis V, Cobb S, Graham BP. Encoding and retrieval in a CA1 microcircuit model of the hippocampus. In: Kurkova V, et al., editors. Lecture notes in computer science 5164. Berlin: Springer; 2008. p. 238-47.
13. Cutsuridis V, Cobb S, Graham BP. Encoding and retrieval in the hippocampal CA1 microcircuit model. Hippocampus. 2010; 20(3): 423-46.
14. Cutsuridis V, Graham BP, Cobb S, Vida I. Hippocampal microcircuits: a computational modeler's resource book. Springer; 2010.
15. Cutsuridis V, Hasselmo M. Dynamics and function of a CA1 model of the hippocampus during theta and ripples. In: Diamantaras K, Duch W, Iliadis LS, editors. ICANN 2010, part I, LNCS 6352. Berlin: Springer; 2010. p. 230-40.
16. Cutsuridis V, Kahramanoglou I, Smyrnis N, Evdokimidis I, Perantonis S. A neural variable integrator model of decision making in an antisaccade task. Neurocomputing. 2007; 70(7-9): 1390-402.
17. Cutsuridis V, Wennekers T. Hippocampus, microcircuits and associative memory. Neural Netw. 2009; 22(8): 1120-8.
18. Diba K, Buzsaki G. Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci. 2007; 10(10): 1241-2.
19. Dickson C, Magistretti J, Shalinsky M, Fransen E, Hasselmo M, Alonso A. Properties and role of I h in the pacing of sub-threshold oscillations in the entorhinal cortex layer II neurons. J Neurophysiol. 2000; 83: 2562-79.
20. Dragoi G, Carpi D, Recce M, Csicsvari J, Buzsaki G. Interactions between hippocampus and medial septum during sharp waves and theta oscillation in the behaving rat. J Neurosci. 1999; 19(14): 6191-9.
21. Dragoi G, Tonegawa S. Preplay of future place cell sequences by hippocampal cell assemblies. Nature. 2011; 469(7330): 397-401.
22. Ellender TJ, Nissen W, Colgin LL, Mann EO, Paulsen O. Priming of hippocampal population bursts by individual perisomatic-targeting interneurons. J Neurosci. 2010; 30(17): 5979-91.
23. Ermentrout B. Simulating, analyzing, and animating dynamical systems: a guide to XPPAUT for researchers and students. Philadelphia: SIAM; 2002.
24. Foster DJ, Wilson MA. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature. 2006; 440: 680-3.
25. Fransen E, Alonso A, Dickson C, Magistretti J, Hasselmo M. Ionic mechanisms in the generation of subthreshold oscillations and action potential clustering in entorhinal layer II stellate neurons. Hippocampus. 2004; 14: 368-84.
26. Fransen E, Alonso A, Hasselmo M. Simulations of the role of the muscarinic-activated calcium-sensitive nonspecific cation current INCM in entorhinal neuronal activity during delayed matching tasks. J Neurosci. 2002; 22: 1081-97.
27. Freund TF. GABAergic septohippocampal neurons contain parvalbumin. Brain Res. 1989; 478: 375-81.
28. Freund TF, Antal M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature. 1988; 336: 170-3.
29. Fuentealba P, Begum R, Capogna M, Jinno S, Márton LF, Csicsvari J, Thomson A, Somogyi P, Klausberger T. Ivy cells: a population of nitric-oxide-producing, slow-spiking GABAergic neurons and their involvement in hippocampal network activity. Neuron. 2008; 57(6): 917-29.
30. Fuentealba P, Klausberger T, Karayannis T, Suen WY, Huck J, Tomioka R, Rockland K, Capogna M, Studer M, Morales M, Somogyi P. Expression of COUP-TFII nuclear receptor in restricted GABAergic neuronal populations in the adult rat hippocampus. J Neurosci. 2010; 30(5): 1595-609.
31. Gillies MJ, Traub RD, LeBeau FEN, Davies CH, Gloveli T, Buhl EH, Whittington MA. A model of atropine-resistant theta oscillations in rat hippocampal area CA1. J Physiol. 2002; 543: 779-93.
32. Graham BP. Dynamics of storage and recall in hippocampal associative memory networks. In: Erdi P, Esposito A, Marinaro M, Scarpetta S, editors. Computational neuroscience: cortical dynamics. Berlin: Springer; 2003. p. 1-23.
33. Graham BP, Cutsuridis V, Hunter R. Associative memory models of hippocampal areas CA1 and CA3. In: Cutsuridis V, et al., editors. Hippocampal microcircuits: a computational modeller's resource book. USA: Springer; 2010. p. 461-94.
34. Harris KD, Henze DA, Hirase H, Leinekugel Z, Dragoi G, Czurko A, Buzsaki G. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature. 2002; 417: 738-41.
35. Hasselmo M, Bodelon C, Wyble B. A proposed function of the hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput. 2002; 14: 793-817.
36. Hasselmo ME, McClelland JL. Neural models of memory. Curr Opinion Neurobiol. 1999; 9: 184-8.
37. Hasselmo M, Schnell E. Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modelling and brain slice physiology. J Neurosci. 1994; 14: 3898-914.
38. Hasselmo ME, Wyble BP. Simulation of the effects of scopolamine on free recall and recognition in a network model of the hippocampus. Behav Brain Res. 1997; 89: 1-34.
39. Hoang L, Kesner RP. Dorsal hippocampus, CA3 and CA1 lesions disrupt temporal sequence completion. Behav Neurosci. 2008; 122: 9-15.
40. Houser CR. Interneurons of the dentate gyrus: an overview of cell types, terminal fields and neurochemical identity. Prog Brain Res. 2007; 163: 217-32.
41. Hunsaker M, Mooy GG, Swift JS, Kesner RP. Dissociation of the medial and lateral perforant path projections into dorsal DG, CA3, and CA1 for spatial and nonspatial (visual object) information processing. Behav Neurosci. 2007; 121: 742-50.
42. Jarsky T, Roxin A, Kath WL, Spruston N. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat Neurosci. 2005; 8(12): 1667-76.
43. Kamondi A, Acsady L, Wang XJ, Buzsaki G. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase precession of action potentials. Hippocampus. 1998; 8: 244-61.
44. Klausberger T, Magill PJ, Marton LF, David J, Roberts B, Cobden PM, Buzsaki G, Somogyi P. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature. 2003; 421: 844-8.
45. Klausberger T, Marton LF, Baude A, Roberts JD, Magill PJ, Somogyi P. Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat Neurosci. 2004; 7(1): 41-7.
46. Klausberger T, Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science. 2008; 321: 53-7.
47. Koene RA, Hasselmo ME. Reversed and forward buffering of behavioral spike sequences enables retrospective and prospective retrieval in hippocampal regions CA3 and CA1. Neural Netw. 2007; 21: 276-88.
48. 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 Brain Res. 1975; 49(1 Pt 1): 58-85.
49. Kunec S, Hasselmo ME, Kopell N. Encoding and retrieval in the CA3 region of the hippocampus: a model of theta-phase separation. J Neurophysiol. 2005; 94(1): 70-82.
50. Lee I, Kesner RP. Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory. Nat Neurosci. 2002; 5: 162-8.
51. Lee I, Kesner RP. Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual-fear conditioning. Hippocampus. 2004; 14: 301-10.
52. Levy W. A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal-like tasks. Hippocampus. 1996; 6: 579-90.
53. Manns JR, Zilli EA, Ong KC, Hasselmo ME, Eichenbaum H. Hippocampal CA1 spiking during encoding and retrieval: relation to theta phase. Neurobiol Learn Mem. 2007; 87(1): 9-20.
54. Mehta MR, Lee AK, Wilson MA. Role of experience and oscillations in transforming a rate code into a temporal code. Nature. 2002; 417: 741-6.
55. Mizuseki K, Sirota A, Pastalkova E, Buzsaki G. Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron. 2009; 64: 267-80.
56. B presynaptic inhibition has an in vivo time constant sufficiently rapid to allow modulation at theta frequency. J Neurophys. 2002; 87(3): 1196-205.
57. O'Keefe J, Nadel L. The hippocampus as a cognitive map. Oxford: Oxford University Press; 1978.
58. O'Keefe J, Recce ML. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus. 1993; 3(3): 317-30.
59. Orbán G, Kiss T, Érdi P. Intrinsic and synaptic mechanisms determining the timing of neuron population activity during hippocampal theta oscillation. J Neurophysiol. 2006; 96(6): 2889-904.
60. O'Reilly R, McClelland JL. Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus. 1994; 4: 661-82.
61. Poirazi P, Brannon T, Mel BW. Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron. 2003; 37: 977-87.
62. Rizzuto DS, Madsen JR, Bromfield EB, Schulze-Bonhage A, Kahana MJ. Human neocortical oscillations exhibit theta phase differences between encoding and retrieval. Neuroimage. 2006; 31(3): 1352-8.
63. Rolls ET. Spatial view cells and the representation of place in the primate hippocampus. Hippocampus. 1999; 9(4): 467-80.
64. Rolls ET, Treves A. Neural networks in the brain involved in memory and recall. Prog Brain Res. 1994; 102: 335-41.
65. Rotstein HG, Pervouchine DD, Acker CD, Gillies MJ, White JA, Buhl EH, Whittington MA, Kopell N. Slow and fast inhibition and an h-current interact to create a theta rhythm in a model of CA1 interneuron network. J Neurophysiol. 2005; 94: 1509-18.
66. Rubin JE, Gerkin RC, Bi GQ, Chow CC. Calcium time course as signal for spike-timing-dependent plasticity. J Neurophysiol. 2005; 93: 2600-13.
67. Skaggs WE, McNaughton BL. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science. 1996; 271: 1870-3.
68. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus. 1996; 6: 149-72.
69. Toth K, Borhegyi Z, Freund TF. Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of Broca complex. J Neurosci. 1993; 13: 3712-24.
70. Traub RD, Draguhn A, Whittington MA, Baldeweg T, Bibbig A, Buhl EH, Schmitz D. Axonal gap junctions between principal neurons: a novel source of network oscillations, and perhaps epileptogenesis. Rev Neurosci. 2002; 13: 1-30.
71. Traub RD, Jefferys JG, Miles R, Whittington MA, Toth K. A branching dendritic model of a rodent CA3 pyramidal neurone. J Physiol. 1994; 481: 79-95.
72. Treves A. Computational constraints between retrieving the past and predicting the future, and the CA3-CA1 differentiation. Hippocampus. 2004; 14: 539-56.
73. Vanderwolf CH. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol. 1969; 26: 407-18.
74. Vida I. Morphology of hippocampal neurons. In: Cutsuridis V, et al., editors. Hippocampal microcircuits: a computational modeler's resource book. USA: Springer; 2010. p. 27-67.
75. Vinogradova O. Hippocampus as a comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus. 2001; 11: 578-98.
76. White J, Klink R, Alonso A, Kay A. Noise from voltage-gated ion channels may influence neuronal dynamics in the entorhinal cortex. J Neurophysiol. 1998; 80: 262-9.