A computational model for preplay in the hippocampus

Frontiers in Computational Neuroscience

Volumn , Issue NOV, 2013, Pages

  Azizi, Amir H ^a   Wiskott, Laurenz ^a   Cheng, Sen ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Continuous attractor neural networks; Multi chart structure; Preplay; Sequential activity; Spike frequency adaptation

Indexed keywords

ASYMMETRIC PATTERNS; COMPUTATIONAL MODEL; CONTINUOUS ATTRACTOR; CONTINUOUS ATTRACTOR NEURAL NETWORKS; PREPLAY; RANDOM CORRELATIONS; SEQUENTIAL ACTIVITIES; SPIKE-FREQUENCY-ADAPTATION;

BRAIN; NEURAL NETWORKS; NEURONS;

TIME VARYING NETWORKS;

ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONNECTOME; CORRELATION ANALYSIS; FEEDBACK SYSTEM; HIPPOCAMPUS; LEARNING; MATHEMATICAL MODEL; NERVE CELL NETWORK; PLAY; PREDICTION; PREPLAY; SIMULATION;

EID: 84887928035     PISSN: 16625188     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncom.2013.00161     Document Type: Article

References (58)

1. Battaglia, F. P., and Treves, A. (1998). Attractor neural networks storing multiple space representations: a model for hippocampal place fields. Phys. Rev. E 58, 7738-7753. doi: 10.1103/PhysRevE.58.7738
2. Ben-Yishai, R., Bar-Or, R. L., and Sompolinsky, H. (1995). Theory of orientation tuning in visual cortex. Proc. Natl. Acad. Sci. U.S.A. 92, 3844-3848. doi: 10.1073/pnas.92.9.3844
3. Blumenfeld, B., Preminger, S., Sagi, D., and Tsodyks, M. (2006). Dynamics of memory representations in networks with novelty-facilitated synaptic plasticity. Neuron 52, 383-394. doi: 10.1016/j.neuron.2006.08.016
4. Buhmann, J., and Schulten, K. (1987). Noise-Driven temporal association in neural networks. Europhys. Lett. 4, 1205-1209. doi: 10.1209/0295-5075/4/10/021
5. Buhry, L., Azizi, A. H., and Cheng, S. (2011). Reactivation, replay, and preplay: how it might all fit together. Neural Plastic. 2011, 1-11. doi: 10.1155/2011/203462
6. Burak, Y., and Fiete, I. R. (2009). Accurate path integration in continuous attractor network models of grid cells. PLoS Comput. Biol. 5:e1000291. doi: 10.1371/journal.pcbi.1000291
7. Buzsáki, G. (1996). The Hippocampo-Neocortical dialogue. Cereb. Cortex 6, 81-92. doi: 10.1093/cercor/6.2.81
8. Cheng, S. (2013). The CRISP theory of hippocampal function in episodic memory. Front. Neural Circ. 7:88. doi: 10.3389/fncir.2013.00088
9. Cheng, S., and Frank, L. M. (2008). New experiences enhance coordinated neural activity in the hippocampus. Neuron 57, 303-313. doi: 10.1016/j.neuron.2007.11.035
10. Colgin, L. L., Leutgeb, S., Jezek, K., Leutgeb, J. K., Moser, E. I., McNaughton, B. L., et al. (2010). Attractor-Map versus autoassociation based attractor dynamics in the hippocampal network. J. Neurophysiol. 104, 35-50. doi: 10.1152/jn.00202.2010
11. Dehaene, S., Changeux, J. P., and Nadal, J. P. (1987). Neural networks that learn temporal sequences by selection. Proc. Natl. Acad. Sci. U.S.A. 84, 2727-2731. doi: 10.1073/pnas.84.9.2727
12. Dragoi, G., and Tonegawa, S. (2011). Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469, 397-401. doi: 10.1038/nature09633
13. Dragoi, G., and Tonegawa, S. (2013). Distinct preplay of multiple novel spatial experiences in the rat. Proc. Natl. Acad. Sci. U.S.A. 110, 9100-9105. doi: 10.1073/pnas.1306031110
14. Epsztein, J., Brecht, M., and Lee, A. K. (2011). Intracellular determinants of hippocampal CA1 place and silent cell activity in a novel environment. Neuron 70, 109-120. doi: 10.1016/j.neuron.2011.03.006
15. 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. doi: 10.1038/nature04587
16. Foster, D. J., and Wilson, M. A. (2007). Hippocampal theta sequences. Hippocampus17, 1093-1099. doi: 10.1002/hipo.20345
17. Ghorbani, M., Mehta, M., Bruinsma, R., and Levine, A. J. (2012). Nonlinear-dynamics theory of up-down transitions in neocortical neural networks. Phys. Rev. E85:021908. doi: 10.1103/PhysRevE.85.021908
18. Girardeau, G., Benchenane, K., Wiener, S. I., Buzsaki, G., and Zugaro, M. B. (2009). Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 12, 1222-1223. doi: 10.1038/nn.2384
19. Gupta, A. S., van der Meer, M. A. A., Touretzky, D. S., and Redish, A. D. (2010). Hippocampal replay is not a simple function of experience. Neuron 65, 695-705. doi: 10.1016/j.neuron.2010.01.034
20. Gupta, A. S., van der Meer, M. A., Touretzky, D. S., and Redish, A. D. (2012). Segmentation of spatial experience by hippocampal sequences. Nat. Neurosci. 15, 1032-1039. doi: 10.1038/nn.3138
21. Hemond, P., Epstein, D., Boley, A., Migliore, M., Ascoli, G. A., and Jaffe, D. B. (2008). Distinct classes of pyramidal cells exhibit mutually exclusive firing patterns in hippocampal area CA3b. Hippocampus 18, 411-424. doi: 10.1002/hipo.20404
22. Herz, A. V., Li, Z., and van Hemmen, J. L. (1991). Statistical mechanics of temporal association in neural networks with transmission delays. Phys. Rev. Lett. 66, 1370-1373. doi: 10.1103/PhysRevLett.66.1370
23. Hopfield, J. J. (2010). Neurodynamics of mental exploration. Proc. Natl. Acad. Sci. U.S.A. 107, 1648-1653. doi: 10.1073/pnas.0913991107
24. Itskov, V., Curto, C., Pastalkova, E., and Buzsáki, G. (2011a). Cell assembly sequences arising from spike threshold adaptation keep track of time in the hippocampus. J. Neurosci. 31, 2828-2834. doi: 10.1523/JNEUROSCI.3773-10.2011
25. Itskov, V., Hansel, D., and Tsodyks, M. (2011b). Short-Term facilitation may stabilize parametric working memory trace. Front. Comput. Neurosci. 5:40. doi: 10.3389/fncom.2011.00040
26. Jadhav, S. P., Kemere, C., German, P. W., and Frank, L. M. (2012). Awake hippocampal Sharp-Wave ripples support spatial memory. Science 336, 1454-1458. doi: 10.1126/science.1217230
27. Jezek, K., Henriksen, E. J., Treves, A., Moser, E. I., and Moser, M.-B. (2011). Theta-paced flickering between place-cell maps in the hippocampus. Nature 478, 246-249. doi: 10.1038/nature10439
28. Johnson, A., and Redish, A. D. (2007). Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27, 12176-12189. doi: 10.1523/JNEUROSCI.3761-07.2007
29. Kammerer, A., Tejero-Cantero, A., and Leibold, C. (2012). Inhibition enhances memory capacity: optimal feedback, transient replay and oscillations. J. Comput. Neurosci. 34, 125-136. doi: 10.1007/s10827-012-0410-z
30. Lee, A. K., and Wilson, M. A. (2002). Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183-1194. doi: 10.1016/S0896-6273(02)01096-6
31. Leibold, C., and Kempter, R. (2006). Memory capacity for sequences in a recurrent network with biological constraints. Neural Comput. 18, 904-941. doi: 10.1162/neco.2006.18.4.904
32. Leutgeb, J. K., Leutgeb, S., Treves, A., Meyer, R., Barnes, C. A., McNaughton, B. L., et al. (2005). Progressive transformation of hippocampal neuronal representations in "morphed" environments. Neuron 48, 345-358. doi: 10.1016/j.neuron.2005.09.007
33. MacDonald, C. J., Lepage, K. Q., Eden, U. T., and Eichenbaum, H. (2011). Hippocampal time cellsİbridge the gap in memory for discontiguous events. Neuron 71, 737-749. doi: 10.1016/j.neuron.2011.07.012
34. McClelland, J. L., McNaughton, B. L., and O'Reilly, R. C. (1995). Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 102, 419-457. doi: 10.1037/0033-295X.102.3.419
35. McNaughton, B. L., Barnes, C. A., Meltzer, J., and Sutherland, R. J. (1989). Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge. Exp. Brain Res. 76, 485-496. doi: 10.1007/BF00248904
36. McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I., and Moser, M.-B. (2006). Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 7, 663-678. doi: 10.1038/nrn1932
37. Memmesheimer, R.-M. M. (2010). Quantitative prediction of intermittent high-frequency oscillations in neural networks with supralinear dendritic interactions. Proc. Natl. Acad. Sci. U.S.A. 107, 11092-11097. doi: 10.1073/pnas.0909615107
38. Muller, R. U., and Stead, M. (1996). Hippocampal place cells connected by hebbian synapses can solve spatial problems. Hippocampus 6, 709-719. doi: 10.1002/(SICI)1098-1063(1996)6:6<709::AID-HIPO13>3.0.CO;2-4
39. Nadal, J.-P. (1991). Associative memory: on the (puzzling) sparse coding limit. J. Phys. A Math. Gen. 24:1093. doi: 10.1088/0305-4470/24/5/023
40. Pastalkova, E., Itskov, V., Amarasingham, A., and Buzsáki, G. (2008). Internally generated cell assembly sequences in the rat hippocampus. Science 321, 1322-1327. doi: 10.1126/science.1159775
41. Pfeiffer, B. E., and Foster, D. J. (2013). Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497, 74-79. doi: 10.1038/nature12112
42. Pinto, D. J., and Ermentrout, G. B. (2001). Spatially structured activity in synaptically coupled neuronal networks: I. traveling fronts and pulses. SIAM J. Appl. Math62:2001. doi: 10.1137/S0036139900346453
43. Ponulak, F., and Hopfield, J. J. (2013). Rapid, parallel path planning by propagating wavefronts of spiking neural activity. Front. Comput. Neurosci. 7:98. doi: 10.3389/fncom.2013.00098
44. Press, W. H., Flannery, B. P., Teukolsky, S. A., and Vetterling, W. T. (1992). Numerical Recipes in C: The Art of Scientific Computing, 2nd Edition. Cambridge; New York, NY: Cambridge University Press.
45. Renart, A., Song, P., and Wang, X.-J. (2003). Robust spatial working memory through homeostatic synaptic scaling in heterogeneous cortical networks. Neuron 38, 473-485. doi: 10.1016/S0896-6273(03)00255-1
46. Richardson, K. A., Schiff, S. J., and Gluckman, B. J. (2005). Control of traveling waves in the mammalian cortex. Phys. Rev. Lett. 94:028103. doi: 10.1103/PhysRevLett.94.028103
47. Romani, S., and Tsodyks, M. (2010). Continuous attractors with morphed/correlated maps. PLoS Comput. Biol. 6:e1000869. doi: 10.1371/journal.pcbi.1000869
48. Roudi, Y., and Treves, A. (2008). Representing where along with what information in a model of a cortical patch. PLoS Comput. Biol. 4:e1000012. doi: 10.1371/journal.pcbi.1000012
49. Samsonovich, A., and McNaughton, B. L. (1997). Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17, 5900-5920.
50. Scoville, W. B., and Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11-21. doi: 10.1136/jnnp.20.1.11
51. 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. doi: 10.1002/hipo.20930
52. Tsodyks, M. (1999). Attractor neural network models of spatial maps in hippocampus. Hippocampus 9, 481-489. doi: 10.1002/(SICI)1098-1063(1999)9:4<481::AID-HIPO14>3.0.CO;2-S
53. Tsodyks, M. V., Skaggs, W. E., Sejnowski, T. J., and McNaughton, B. L. (1996). Population dynamics and theta rhythm phase precession of hippocampal place cell firing: a spiking neuron model. Hippocampus 6, 271-280. doi: 10.1002/(SICI)1098-1063(1996)6:3<271::AID-HIPO5>3.3.CO;2-Q
54. Vladimirov, N., Tu, Y., and Traub, R. D. (2013). Synaptic gating at axonal branches, and sharp-wave ripples with replay: a simulation study. Eur. J. Neurosci., Page n/a. doi: 10.1111/ejn.12342. [Epub ahead of print].
55. Wagatsuma, H., and Yamaguchi, Y. (2007). Neural dynamics of the cognitive map in the hippocampus. Cogn. Neurodyn. 1, 119-141. doi: 10.1007/s11571-006-9013-6
56. Wills, T. J., Lever, C., Cacucci, F., Burgess, N., and O'Keefe, J. (2005). Attractor dynamics in the hippocampal representation of the local environment. Science 308, 873-876. doi: 10.1126/science.1108905
57. Wiskott, L., and von der Malsburg, C. (1996). "Face recognition by dynamic link matching, " in Lateral Interactions in the Cortex: Structure and Function. Austin, TX: The UTCS Neural Networks Research Group.
58. Zhang, K. (1996). Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J. Neurosci. 16, 2112-2126.