A Signature of Attractor Dynamics in the CA3 Region of the Hippocampus

PLoS Computational Biology

Volumn 10, Issue 5, 2014, Pages

  Rennó Costa, César ^a,b   Lisman, John E ^c   Verschure, Paul F M J ^a,d  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

^c BRANDEIS UNIVERSITY   (United States)

^d INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ASSOCIATIVE STORAGE;

ACTIVITY PATTERNS; ANATOMICAL FEATURES; ASSOCIATIVE MEMORY; ATTRACTOR DYNAMICS; ATTRACTOR NETWORKS; EXPERIMENTAL EVIDENCE; EXTERNAL INPUT; FIRING PATTERNS; PATTERN COMPLETION; STORED PATTERN;

ASSOCIATIVE PROCESSING;

ARTICLE; ASSOCIATIVE MEMORY; ATTRACTOR NETWORK; CONTROLLED STUDY; DENTATE GYRUS; FUNCTIONAL ANATOMY; HIPPOCAMPAL CA3 REGION; LEARNING; MATHEMATICAL MODEL; NERVE CELL NETWORK; NEUROANATOMY; QUANTITATIVE ANALYSIS; RECALL; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; BIOLOGICAL RHYTHM; COMPUTER SIMULATION; HIPPOCAMPUS; HUMAN; MEMORY; NERVE CELL; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL CLOCKS; COMPUTER SIMULATION; HIPPOCAMPUS; HUMANS; MEMORY; MODELS, NEUROLOGICAL; NERVE NET; NEURONS;

EID: 84901660030     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003641     Document Type: Article

References (64)

1. Willshaw DJ, Buneman OP, Longuet-Higgins HC, (1969) Non-Holographic Associative Memory. Nature 222: 960-962.
2. Hopfield JJ, (1982) Neural Networks and Physical Systems with Emergent Collective Computational Abilities. Proc Natl Acad Sci 79: 2554-2558.
3. Amit DJ (1992) Modeling Brain Function: The World of Attractor Neural Networks. Cambridge: Cambridge University Press.
4. Rolls ET, Deco G (2010) The Noisy Brain: Stochastic Dynamics as a Principle of Brain Function. Oxford: Oxford University Press, USA.
5. Marr D, (1971) Simple Memory: A Theory for Archicortex. Philos Trans R Soc London Ser B. 262: 23-81.
6. McNaughton BL, Morris RGM, (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10: 408-415.
7. Wittner L, Henze DA, Záborszky L, Buzsáki G, (2007) Three-dimensional reconstruction of the axon arbor of a CA3 pyramidal cell recorded and filled in vivo. Brain Struct Funct 212: 75-83.
8. Ishizuka N, Weber J, Amaral DG, (1990) Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 295: 580-623.
9. Bains JS, Longacher JM, Staley KJ, (1999) Reciprocal interactions between CA3 network activity and strength of recurrent collateral synapses. Nat Neurosci 2: 720-726.
10. Pavlidis P, Montgomery J, Madison DV, (2000) Presynaptic protein kinase activity supports long-term potentiation at synapses between individual hippocampal neurons. J Neurosci 20: 4497-4505.
11. Tsodyks M, Sejnowski T, (1995) Associative memory and hippocampal place cells. Int J Neural Syst 6: 81-86.
12. Rolls ET, (2007) An attractor network in the hippocampus: theory and neurophysiology. Learn Mem 14: 714-731.
13. O'Reilly RC, McClelland JL, (1994) Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus 4: 661-682.
14. Rolls ET, (2013) A quantitative theory of the functions of the hippocampal CA3 network in memory. Front Cell Neurosci 7: 98.
15. Hasselmo ME, Schnell E, Barkai E, (1995) Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. J Neurosci 15: 5249-5262.
16. Rolls ET (1990) Functions of the primate hippocampus in spatial processing and memory. In: Olton DS, Kesner RP, editors. Neurobiology of comparative cognition. Hillsdale, NJ: L. Erlbaum. p. 339.
17. Knierim JJ, Zhang K, (2012) Attractor Dynamics of Spatially Correlated Neural Activity in the Limbic System. Annu Rev Neurosci 35: 267-285 doi:10.1146/annurev-neuro-062111-150351.
18. Leutgeb JK, Leutgeb S, Treves A, Meyer R, Barnes CA, et al. (2005) Progressive Transformation of Hippocampal Neuronal Representations in "'Morphed'" Environments. Neuron 48: 345-358.
19. Leutgeb JK, Leutgeb S, Moser M-B, Moser EI, (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315: 961-966.
20. Lu L, Leutgeb JK, Tsao A, Henriksen EJ, Leutgeb S, et al. (2013) Impaired hippocampal rate coding after lesions of the lateral entorhinal cortex. Nat Neurosci 16: 1085-1093.
21. Colgin LL, Leutgeb S, Jezek K, Leutgeb JK, Moser EI, et al. (2010) Attractor-map versus autoassociation based attractor dynamics in the hippocampal network. J Neurophysiol 104: 35-50.
22. Papp G, Witter MP, Treves A, (2007) The CA3 network as a memory store for spatial representations. Learn Mem 14: 732-744.
23. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA, (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6: 149-172.
24. O'Keefe J, Recce ML, (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3: 317-330.
25. De Almeida L, Idiart M, Lisman JE, (2007) Memory retrieval time and memory capacity of the CA3 network: role of gamma frequency oscillations. Learn Mem 14: 795-806.
26. Turner DA, Schwartzkroin PA, (1983) Electrical characteristics of dendrites and dendritic spines in intracellularly stained CA3 and dentate hippocampal neurons. J Neurosci 3: 2381-2394.
27. Storm JF, (1990) Potassium currents in hippocampal pyramidal cells. Prog Brain Res 83: 161-187.
28. Miles R, (1990) Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea-pig in vitro. J Physiol 428: 61-77.
29. De Almeida L, Idiart M, Lisman JE, (2009) A second function of gamma frequency oscillations: an E%-max winner-take-all mechanism selects which cells fire. J Neurosci 29: 7497-7503.
30. Trommald M, Hulleberg G, (1997) Dimensions and density of dendritic spines from rat dentate granule cells based on reconstructions from serial electron micrographs. J Comp Neurol 377: 15-28.
31. De Almeida L, Idiart M, Lisman JE, (2009) The input-output transformation of the hippocampal granule cells: from grid cells to place fields. J Neurosci 29: 7504-7512.
32. Johnston D, Amaral DG (1998) Hippocampus. In: Shepherd GM, editor. The synaptic organization of the brain. New York: Oxford UP. pp. 417-458.
33. Hama K, Arii T, Kosaka T, (1989) Three-dimensional morphometrical study of dendritic spines of the granule cell in the rat dentate gyrus with HVEM stereo images. J Electron Microsc Tech 12: 80-87 doi:10.1002/jemt.1060120203.
34. Rennó-Costa C, Lisman JE, Verschure PFMJ, (2010) The mechanism of rate remapping in the dentate gyrus. Neuron 68: 1051-1058.
35. De Almeida L, Idiart M, Lisman JE, (2010) The single place fields of CA3 cells: A two-stage transformation from grid cells. Hippocampus 22: 200-208.
36. Polsky A, Mel BW, Schiller J, (2004) Computational subunits in thin dendrites of pyramidal cells. Nat Neurosci 7: 621-627.
37. Williams SH, Johnston D, (1991) Kinetic properties of two anatomically distinct excitatory synapses in hippocampal CA3 pyramidal neurons. J Neurophysiol 66: 1010-1020.
38. Hafting T, Fyhn M, Molden S, Moser M-B, Moser EI, (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436: 801-806.
39. Blair HT, Welday AC, Zhang K, (2007) Scale-invariant memory representations emerge from moiré interference between grid fields that produce theta oscillations: a computational model. J Neurosci 27: 3211-3229.
40. Fyhn M, Hafting T, Treves A, Moser M, Moser EI, (2007) Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446: 190-194.
41. Hargreaves EL, Rao G, Lee I, Knierim JJ, (2005) Major Dissociation Between Medial and Lateral Entorhinal Input to Dorsal Hippocampus. Science 1792: 1792-1794 doi:10.1126/science.1110449.
42. Yoganarasimha D, Rao G, Knierim JJ, (2011) Lateral entorhinal neurons are not spatially selective in cue-rich environments. Hippocampus 21: 1363-1374.
43. Deshmukh SS, Johnson JL, Knierim JJ, (2012) Perirhinal cortex represents nonspatial, but not spatial, information in rats foraging in the presence of objects: comparison with lateral entorhinal cortex. Hippocampus 22: 2045-2058.
44. McDonald AJ, Mascagni F, (1996) Cortico-cortical and cortico-amygdaloid projections of the rat occipital cortex: a Phaseolus vulgaris leucoagglutinin study. Neuroscience 71: 37-54.
45. Carlsen J, De Olmos J, Heimer L, (1982) Tracing of two-neuron pathways in the olfactory system by the aid of transneuronal degeneration: projections to the amygdaloid body and hippocampal formation. J Comp Neurol 208: 196-208.
46. Burwell RD, Amaral DG, (1998) Perirhinal and postrhinal cortices of the rat: interconnectivity and connections with the entorhinal cortex. J Comp Neurol 391: 293-321.
47. Chawla MK, Guzowski JF, Ramirez-Amaya V, Lipa P, Hoffman KL, et al. (2005) Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 15: 579-586.
48. Tashiro A, Makino H, Gage FH, (2007) Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J Neurosci 27: 3252-3259.
49. Rousseeuw PJ, (1987) Silhouettes: A graphical aid to the interpretation and validation of cluster analysis. J Comput Appl Math 20: 53-65.
50. Henze DA, Wittner L, Buzsáki G, (2002) Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat Neurosci 5: 790-795.
51. Bragin A, Jandó G, Nádasdy Z, Hetke J, Wise K, et al. (1995) Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15: 47-60.
52. Akam T, Oren I, Mantoan L, Ferenczi E, Kullmann DM, (2012) Oscillatory dynamics in the hippocampus support dentate gyrus-CA3 coupling. Nat Neurosci 15: 763-768.
53. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, et al. (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312: 758-762.
54. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, et al. (2005) Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309: 619-623.
55. Mankin EA, Sparks FT, Slayyeh B, Sutherland RJ, Leutgeb S, et al. (2012) Neuronal code for extended time in the hippocampus. Proc Natl Acad Sci 109: 19462-19467 doi:10.1073/pnas.1214107109.
56. Wills TJ, Lever C, Cacucci F, Burgess N, O'Keefe J, (2005) Attractor dynamics in the hippocampal representation of the local environment. Science 308: 873-876.
57. Neunuebel JP, Knierim JJ, (2014) CA3 Retrieves Coherent Representations from Degraded Input: Direct Evidence for CA3 Pattern Completion and Dentate Gyrus Pattern Separation. Neuron 81: 416-427.
58. Jackson MB, (2013) Recall of Spatial Patterns Stored in a Hippocampal Slice By Long-Term Potentiation. J Neurophysiol 110: 2511-2519.
59. Nakazawa K, Quirk MC, Chitwood RA, Watanabe M, Yeckel MF, et al. (2002) Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297: 211-218.
60. Mei B, Li F, Gu Y, Cui Z, Tsien JZ, (2011) NMDA receptors are not required for pattern completion during associative memory recall. PLoS One 6: e19326.
61. Verschure PFMJ, Voegtlin T, Douglas RJ, (2003) Environmentally mediated synergy between perception and behaviour in mobile robots. Nature 425: 620-624.
62. Sanches-Montanes MA, Verschure PFMJ, König P, (2000) Global and local gating of synaptic plasticity. Neural Comput 12: 543-552.
63. Grossberg S, (1980) How does a brain build a cognitive code? Psychol Rev 87: 1-51.
64. Gold AE, Kesner RP (2005) The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat. Hippocampus 15: 808-814. Available: http://www.ncbi.nlm.nih.gov/pubmed/16010664. Accessed 20 October 2012.