Reversed theta sequences of hippocampal cell assemblies during backward travel

Nature Neuroscience

Volumn 17, Issue 5, 2014, Pages 719-724

  Cei, Anne ^a,b   Girardeau, Gabrielle ^a,b   Drieu, Céline ^a,b   Kanbi, Karim El ^a,b   Zugaro, Michaël ^a,b  

^a PSL RESEARCH UNIVERSITY   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; CELL ACTIVITY; ENTORHINAL CORTEX; HIPPOCAMPUS; LOCOMOTION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAILWAY; THEORETICAL MODEL; THETA RHYTHM; TRAVEL;

ACTION POTENTIALS; ANIMALS; BAYES THEOREM; ELECTRODES, IMPLANTED; ENTORHINAL CORTEX; HIPPOCAMPUS; LOCOMOTION; MALE; MODELS, NEUROLOGICAL; NEURONS; ORIENTATION; RATS; RATS, LONG-EVANS; SPACE PERCEPTION; THETA RHYTHM;

EID: 84899621224     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3698     Document Type: Article

References (55)

1. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Calendron Press, Oxford, 1978).
2. Skaggs, W.E., Mcnaughton, B.L., Wilson, M.A. & Barnes, C.A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149-172 (1996).
3. Dragoi, G. & Buzsáki, G. Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50, 145-157 (2006).
4. Maurer, A.P., Cowen, S.L., Burke, S.N. & Barnes, C.A. & McNaughton, B.L. Organization of hippocampal cell assemblies based on theta phase precession. Hippocampus 16, 785-794 (2006).
5. Foster, D.J. & Wilson, M.A. Hippocampal theta sequences. Hippocampus 17, 1093- 1099 (2007).
6. Itskov, V., Pastalkova, E., Mizuseki, K., Buzsaki, G. & Harris, K.D. Theta-mediated dynamics of spatial information in hippocampus. J. Neurosci. 28, 5959-5964 (2008).
7. Gupta, A.S. & Van Der Meer, M.A., Touretzky, D.S. & Redish, A.D. Segmentation of spatial experience by hippocampal theta sequences. Nat. Neurosci. 15, 1032-1039 (2012).
8. Robbe, D. & Buzsáki, G. Alteration of theta timescale dynamics of hippocampal place cells by a cannabinoid is associated with memory impairment. J. Neurosci. 29, 12597-12605 (2009).
9. Buzsáki, G. Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 31, 551-570 (1989).
10. Girardeau, G., Benchenane, K., Wiener, S.I., Buzsáki, G. & Zugaro, M.B. Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 12, 1222-1223 (2009).
11. Ego-Stengel, V. & Wilson, M.A. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 20, 1-10 (2010).
12. Jadhav, S.P., Kemere, C., German, P.W. & Frank, L.M. Awake hippocampal sharp-wave ripples support spatial memory. Science 336, 1454-1458 (2012).
13. O'Keefe, J. & Recce, M. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317-330 (1993).
14. Hafting, T., Fyhn, M., Bonnevie, T., Moser, M.-B. & Moser, E.I. Hippocampusindependent phase precession in entorhinal grid cells. Nature 453, 1248-1252 (2008).
15. Dupret, D., O'Neill, J., Pleydell-Bouverie, B. & Csicsvari, J. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat. Neurosci. 13, 995-1002 (2010).
16. Harvey, C.D., Collman, F. & Dombeck, D.A. & Tank, D.W. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461, 941-946 (2009).
17. Zugaro, M.B., Monconduit, L. & Buzsáki, G. Spike phase precession persists after transient intrahippocampal perturbation. Nat. Neurosci. 8, 67-71 (2005).
18. Geisler, C. et al. Temporal delays among place cells determine the frequency of population theta oscillations in the hippocampus. Proc. Natl. Acad. Sci. USA 107, 7957-7962 (2010).
19. Burgess, N. Grid cells and theta as oscillatory interference: theory and predictions. Hippocampus 18, 1157-1174 (2008).
20. Jensen, O. & Lisman, J.E. Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn. Mem. 3, 279-287 (1996).
21. Tsodyks, M.V., Skaggs, W.E., Sejnowski, T.J. & McNaughton, B.L. Population dynamics and theta rhythm phase precession of hippocampal place cell firing: a spiking neuron model. Hippocampus 6, 271-280 (1996).
22. Wallenstein, G.V. & Hasselmo, M.E. GABAergic modulation of hippocampal population activity: sequence learning, place field development, and the phase precession effect. J. Neurophysiol. 78, 393-408 (1997).
23. Losonczy, A., Zemelman, B.V., Vaziri, A. & Magee, J.C. Network mechanisms of theta related neuronal activity in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 13, 967-972 (2010).
24. Kamondi, A., Acsády, L., Wang, X.J. & Buzsáki, G. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 8, 244-261 (1998).
25. Harris, K.D. et al. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417, 738-741 (2002).
26. Mehta, M.R., Lee, A.K. & Wilson, M.A. Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417, 741-746 (2002).
27. Pastalkova, E., Itskov, V., Amarasingham, A. & Buzsáki, G. Internally generated cell assembly sequences in the rat hippocampus. Science 321, 1322-1327 (2008).
28. Huxter, J., Burgess, N. & O'Keefe, J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425, 828-832 (2003).
29. Terrazas, A. et al. Self-motion and the hippocampal spatial metric. J. Neurosci. 25, 8085-8096 (2005).
30. Burgess, N., Recce, M. & O'Keefe, J. A model of hippocampal function. Neural Netw. 7, 1065-1081 (1994).
31. Huxter, J.R., Senior, T.J., Allen, K. & Csicsvari, J. Theta phase-specific codes for twodimensional position, trajectory and heading in the hippocampus. Nat. Neurosci. 11, 587-594 (2008).
32. Sargolini, F. et al. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312, 758-762 (2006).
33. Maurer, A.P., Cowen, S.L., Burke, S.N. & Barnes, C.A. & McNaughton, B.L. Phase precession in hippocampal interneurons showing strong functional coupling to individual pyramidal cells. J. Neurosci. 26, 13485-13492 (2006).
34. Ego-Stengel, V. & Wilson, M.A. Spatial selectivity and theta phase precession in CA1 interneurons. Hippocampus 17, 161-174 (2007).
35. Kim, S.M., Ganguli, S. & Frank, L.M. Spatial information outflow from the hippocampal circuit: distributed spatial coding and phase precession in the subiculum. J. Neurosci. 32, 11539-11558 (2012).
36. Jones, M.W. & Wilson, M.A. Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus 15, 867-873 (2005).
37. Geisler, C., Robbe, D., Zugaro, M., Sirota, A. & Buzsáki, G. Hippocampal place cell assemblies are speed-controlled oscillators. Proc. Natl. Acad. Sci. USA 104, 8149- 8154 (2007).
38. Booth, V. & Bose, A. Neural mechanisms for generating rate and temporal codes in model CA3 pyramidal cells. J. Neurophysiol. 85, 2432-2445 (2001).
39. Yamaguchi, Y. A theory of hippocampal memory based on theta phase precession. Biol. Cybern. 89, 1-9 (2003).
40. Lengyel, M., Szatmáry, Z. & Erdi, P. Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing. Hippocampus 13, 700-714 (2003).
41. Sato, N. & Yamaguchi, Y. Memory encoding by theta phase precession in the hippocampal network. Neural Comput. 15, 2379-2397 (2003).
42. Burgess, N., O'Keefe, J. & Recce, M. Using hippocampal place cells' for navigation, exploiting phase coding. Adv. Neural Inf. Process. Syst. 5, 923-936 (1993).
43. Chance, F.S. Hippocampal phase precession from dual input components. J. Neurosci. 32, 16693-16703 (2012).
44. Castro, L. & Aguiar, P. Phase precession through acceleration of local theta rhythm: a biophysical model for the interaction between place cells and local inhibitory neurons. J. Comput. Neurosci. 33, 141-150 (2012).
45. Baker, J.L. & Olds, J.L. Theta phase precession emerges from a hybrid computational model of a CA3 place cell. Cogn. Neurodyn. 1, 237-248 (2007).
46. Navratilova, Z., Giocomo, L.M., Fellous, J.-M., Hasselmo, M.E. & McNaughton, B.L. Phase precession and variable spatial scaling in a periodic attractor map model of medial entorhinal grid cells with realistic after-spike dynamics. Hippocampus 22, 772-789 (2011).
47. Magee, J.C. Dendritic mechanisms of phase precession in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 86, 528-532 (2001).
48. Leung, L.S. A model of intracellular theta phase precession dependent on intrinsic subthreshold membrane currents. J. Neurosci. 31, 12282-12296 (2011).
49. Mehta, M.R. & Barnes, C. & McNaughton, B.L. Experience-dependent, asymmetric expansion of hippocampal place fields. Proc. Natl. Acad. Sci. USA 94, 8918-8921 (1997).
50. Fiore, L., Corsini, G. & Geppetti, L. Application of non-linear filters based on the median filter to experimental and simulated multiunit neural recordings. J. Neurosci. Methods 70, 177-184 (1996).
51. Quiroga, R.Q., Nadasdy, Z. & Ben-Shaul, Y. Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput. 16, 1661-1687 (2004).
52. Hazan, L., Zugaro, M. & Buzsáki, G. Klusters, NeuroScope, NDManager: a free software suite for neurophysiological data processing and visualization. J. Neurosci. Methods 155, 207-216 (2006).
53. Harris, K.D., Hirase, H., Leinekugel, X. & Henze, D.A. & Buzsáki, G. Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron 32, 141-149 (2001).
54. Mehta, M.R., Quirk, M.C. & Wilson, M.A. Experience-dependent asymmetric shape of hippocampal receptive fields. Neuron 25, 707-715 (2000).
55. Kempter, R., Leibold, C., Buzsáki, G., Diba, K. & Schmidt, R. Quantifying circular-linear associations: Hippocampal phase precession. J. Neurosci. Methods 207, 113-124 (2012).