Preconfigured, skewed distribution of firing rates in the hippocampus and entorhinal cortex

Cell Reports

Volumn 4, Issue 5, 2013, Pages 1010-1021

  Mizuseki, Kenji ^a,b   Buzsáki, György ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENTORHINAL CORTEX; HIPPOCAMPUS; INTERNEURON; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RAT; SYNAPTIC POTENTIAL;

ACTION POTENTIALS; ANIMALS; CA1 REGION, HIPPOCAMPAL; ELECTROPHYSIOLOGY; ENTORHINAL CORTEX; HIPPOCAMPUS; INTERNEURONS; MALE; MICE; NEURONS; RATS; RATS, LONG-EVANS; SYNAPTIC TRANSMISSION;

EID: 84884143038     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.07.039     Document Type: Article

References (62)

1. Arellano J.I., Benavides-Piccione R., Defelipe J., Yuste R. Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front. Neurosci. 2007, 1:131-143.
2. Barth A.L., Poulet J.F. Experimental evidence for sparse firing in the neocortex. Trends Neurosci. 2012, 35:345-355.
3. Barthó P., Hirase H., Monconduit L., Zugaro M., Harris K.D., Buzsáki G. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J.Neurophysiol. 2004, 92:600-608.
4. Battaglia F.P., Sutherland G.R., Cowen S.L., Mc Naughton B.L., Harris K.D. Firing rate modulation: a simple statistical view of memory trace reactivation. Neural Netw 2005, 18:1280-1291.
5. Buzsáki G., Horváth Z., Urioste R., Hetke J., Wise K. High-frequency network oscillation in the hippocampus. Science 1992, 256:1025-1027.
6. Csicsvari J., Hirase H., Czurkó A., Mamiya A., Buzsáki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat. J.Neurosci. 1999, 19:274-287.
7. Csicsvari J., Hirase H., Mamiya A., Buzsáki G. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 2000, 28:585-594.
8. Diba K., Buzsáki G. Hippocampal network dynamics constrain the time lag between pyramidal cells across modified environments. J.Neurosci. 2008, 28:13448-13456.
9. Dragoi G., Tonegawa S. Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 2011, 469:397-401.
10. Dragoi G., Harris K.D., Buzsáki G. Place representation within hippocampal networks is modified by long-term potentiation. Neuron 2003, 39:843-853.
11. Dupret D., O'Neill J., Csicsvari J. Dynamic reconfiguration of hippocampal interneuron circuits during spatial learning. Neuron 2013, 78:166-180.
12. Feldmeyer D., Lübke J., Silver R.A., Sakmann B. Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. J.Physiol. 2002, 538:803-822.
13. Fujisawa S., Amarasingham A., Harrison M.T., Buzsáki G. Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex. Nat. Neurosci. 2008, 11:823-833.
14. Grosmark A.D., Mizuseki K., Pastalkova E., Diba K., Buzsáki G. REM sleep reorganizes hippocampal excitability. Neuron 2012, 75:1001-1007.
15. Hafting T., Fyhn M., Molden S., Moser M.B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
16. Hafting T., Fyhn M., Bonnevie T., Moser M.B., Moser E.I. Hippocampus-independent phase precession in entorhinal grid cells. Nature 2008, 453:1248-1252.
17. Harris K.D., Henze D.A., Csicsvari J., Hirase H., Buzsáki G. Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J.Neurophysiol. 2000, 84:401-414.
18. 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 2001, 32:141-149.
19. Hirase H., Leinekugel X., Czurkó A., Csicsvari J., Buzsáki G. Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experience. Proc. Natl. Acad. Sci. USA 2001, 98:9386-9390.
20. Hromádka T., Deweese M.R., Zador A.M. Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol. 2008, 6:e16.
21. Ikegaya Y., Sasaki T., Ishikawa D., Honma N., Tao K., Takahashi N., Minamisawa G., Ujita S., Matsuki N. Interpyramid spike transmission stabilizes the sparseness of recurrent network activity. Cereb. Cortex 2012.
22. Izhikevich E.M., Gally J.A., Edelman G.M. Spike-timing dynamics of neuronal groups. Cereb. Cortex 2004, 14:933-944.
23. Jarsky T., Mady R., Kennedy B., Spruston N. Distribution of bursting neurons in the CA1 region and the subiculum of the rat hippocampus. J.Comp. Neurol. 2008, 506:535-547.
24. Koulakov A.A., Hromádka T., Zador A.M. Correlated connectivity and the distribution of firing rates in the neocortex. J.Neurosci. 2009, 29:3685-3694.
25. Krupic J., Burgess N., O'Keefe J. Neural representations of location composed of spatially periodic bands. Science 2012, 337:853-857.
26. Lee D., Lin B.J., Lee A.K. Hippocampal place fields emerge upon single-cell manipulation of excitability during behavior. Science 2012, 337:849-853.
27. Leutgeb S., Leutgeb J.K., Barnes C.A., Moser E.I., McNaughton B.L., Moser M.B. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 2005, 309:619-623.
28. Levy W.B., Baxter R.A. Energy efficient neural codes. Neural Comput. 1996, 8:531-543.
29. Lisman J.E. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci. 1997, 20:38-43.
30. Loewenstein Y., Kuras A., Rumpel S. Multiplicative dynamics underlie the emergence of the log-normal distribution of spine sizes in the neocortex invivo. J.Neurosci. 2011, 31:9481-9488.
31. Magee J.C., Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 1997, 275:209-213.
32. Mankin E.A., Sparks F.T., Slayyeh B., Sutherland R.J., Leutgeb S., Leutgeb J.K. Neuronal code for extended time in the hippocampus. Proc. Natl. Acad. Sci. USA 2012, 109:19462-19467.
33. Marshall L., Henze D.A., Hirase H., Leinekugel X., Dragoi G., Buzsáki G. Hippocampal pyramidal cell-interneuron spike transmission is frequency dependent and responsible for place modulation of interneuron discharge. J.Neurosci. 2002, 22:RC197.
34. 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. 2006, 26:13485-13492.
35. Mitra A., Mitra S.S., Tsien R.W. Heterogeneous reallocation of presynaptic efficacy in recurrent excitatory circuits adapting to inactivity. Nat. Neurosci. 2012, 15:250-257.
36. Mizuseki K., Sirota A., Pastalkova E., Buzsáki G. Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 2009, 64:267-280.
37. Mizuseki K., Diba K., Pastalkova E., Buzsáki G. Hippocampal CA1 pyramidal cells form functionally distinct sublayers. Nat. Neurosci. 2011, 14:1174-1181.
38. Mizuseki K., Royer S., Diba K., Buzsáki G. Activity dynamics and behavioral correlates of CA3 and CA1 hippocampal pyramidal neurons. Hippocampus 2012, 22:1659-1680.
39. Muller R.U., Kubie J.L. The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J.Neurosci. 1987, 7:1951-1968.
40. Muller R.U., Kubie J.L. The firing of hippocampal place cells predicts the future position of freely moving rats. J.Neurosci. 1989, 9:4101-4110.
41. Narayanan R., Johnston D. Functional maps within a single neuron. J.Neurophysiol. 2012, 108:2343-2351.
42. O'Connor D.H., Peron S.P., Huber D., Svoboda K. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 2010, 67:1048-1061.
43. Olshausen B.A., Field D.J. Sparse coding with an overcomplete basis set: a strategy employed by V1?. Vision Res. 1997, 37:3311-3325.
44. O'Keefe J., Nadel L. The Hippocampus as a Cognitive Map 1978, Oxford University Press, Oxford.
45. O'Keefe J., Recce M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 1993, 3:317-330.
46. Pastalkova E., Itskov V., Amarasingham A., Buzsáki G. Internally generated cell assembly sequences in the rat hippocampus. Science 2008, 321:1322-1327.
47. Pike F.G., Meredith R.M., Olding A.W., Paulsen O. Rapid report: postsynaptic bursting is essential for 'Hebbian' induction of associative long-term potentiation at excitatory synapses in rat hippocampus. J.Physiol. 1999, 518:571-576.
48. Quilichini P., Sirota A., Buzsáki G. Intrinsic circuit organization and theta-gamma oscillation dynamics in the entorhinal cortex of the rat. J.Neurosci. 2010, 30:11128-11142.
49. Roxin A., Brunel N., Hansel D., Mongillo G., van Vreeswijk C. On the distribution of firing rates in networks of cortical neurons. J.Neurosci. 2011, 31:16217-16226.
50. Samsonovich A., McNaughton B.L. Path integration and cognitive mapping in a continuous attractor neural network model. J.Neurosci. 1997, 17:5900-5920.
51. Sayer R.J., Friedlander M.J., Redman S.J. The time course and amplitude of EPSPs evoked at synapses between pairs of CA3/CA1 neurons in the hippocampal slice. J.Neurosci. 1990, 10:826-836.
52. Shadlen M.N., Newsome W.T. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J.Neurosci. 1998, 18:3870-3896.
53. Skaggs W.E., McNaughton B.L., Gothard K.M., Markus E.J. An information-theoretic approach to deciphering the hippocampal code. Advances in Neural Information Processing Systems 1993, Volume 5:1030-1037. Morgan Kaufmann, Burlington, MA. S.J. Hanson, J.D. Cowan, C.L. Giles (Eds.).
54. Song S., Sjöström P.J., Reigl M., Nelson S., Chklovskii D.B. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 2005, 3:e68.
55. Stark E., Koos T., Buzsáki G. Diode probes for spatiotemporal optical control of multiple neurons in freely moving animals. J.Neurophysiol. 2012, 108:349-363.
56. Thomas M.J., Watabe A.M., Moody T.D., Makhinson M., O'Dell T.J. Postsynaptic complex spike bursting enables the induction of LTP by theta frequency synaptic stimulation. J.Neurosci. 1998, 18:7118-7126.
57. Thompson L.T., Best P.J. Place cells and silent cells in the hippocampus of freely-behaving rats. J.Neurosci. 1989, 9:2382-2390.
58. Thomson A.M. Facilitation, augmentation and potentiation at central synapses. Trends Neurosci. 2000, 23:305-312.
59. Tononi G., Cirelli C. Sleep function and synaptic homeostasis. Sleep Med. Rev. 2006, 10:49-62.
60. Wolfe J., Houweling A.R., Brecht M. Sparse and powerful cortical spikes. Curr. Opin. Neurobiol. 2010, 20:306-312.
61. Yassin L., Benedetti B.L., Jouhanneau J.S., Wen J.A., Poulet J.F., Barth A.L. An embedded subnetwork of highly active neurons in the neocortex. Neuron 2010, 68:1043-1050.
62. Ziv Y., Burns L.D., Cocker E.D., Hamel E.O., Ghosh K.K., Kitch L.J., El Gamal A., Schnitzer M.J. Long-term dynamics of CA1 hippocampal place codes. Nat. Neurosci. 2013, 16:264-266.