Independence of the unimodal tuning of firing rate from theta phase precession in hippocampal place cells

Biological Cybernetics

Volumn 102, Issue 2, 2010, Pages 95-107

  Wu, Zhihua ^a   Yamaguchi, Yoko ^b  

^a INSTITUTE OF BIOPHYSICS   (China)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Dynamical coupling; Place cell; Theta phase precession; Two compartment model; Unimodal profile of firing rate tuning

Indexed keywords

DYNAMICAL COUPLING; FIRING RATES; PLACE CELL; THETA PHASE PRECESSION; TWO-COMPARTMENT MODELS; UNIMODAL;

ANIMALS; DENDRIMERS; TUNING;

CELLS;

ANIMALIA; RATTUS;

ACTION POTENTIAL; ANIMAL; ARTICLE; BIOLOGICAL MODEL; HIPPOCAMPUS; PHYSIOLOGY; PYRAMIDAL NERVE CELL; RAT; THETA RHYTHM;

ACTION POTENTIALS; ANIMALS; HIPPOCAMPUS; MODELS, NEUROLOGICAL; PYRAMIDAL CELLS; RATS; THETA RHYTHM;

EID: 77949274506     PISSN: 03401200     EISSN: 14320770     Source Type: Journal    
DOI: 10.1007/s00422-009-0359-9     Document Type: Article

References (54)

1. A Adem M Jolkkonen N Bogdanovic A Islam E Karlsson 1997 Localization of M1 muscarinic receptors in rat brain using selective muscarinic toxin-1 Brain Res Bull 44 597 601 10.1016/S0361-9230(97)00281-5 1:CAS:528:DyaK2sXns1ektLw%3D 9365803 (Pubitemid 27494677)
2. DP Artemenko 1972 Role of hippocampal neurons in theta-wave generation Neurophysiologia 4 409 415 10.1007/BF01063013
3. V Booth A Bose 2001 Neural mechanisms for generating rate and temporal codes in model CA3 pyramidal cells J Neurophysiol 85 2432 2445 1:STN:280:DC%2BD3MzhsVartA%3D%3D 11387389
4. RM Booze EA Crisostomo JN Davis 1993 Beta-adrenergic receptors in the hippocampal and retrohippocampal regions of rats and guinea pigs: autoradiographic and immunohistochemical studies Synapse 13 206 214 10.1002/syn.890130303 1:CAS:528:DyaK3sXksVWnuro%3D 8098879
5. A Bose V Booth M Recce 2000 A temporal mechanism for generating the phase precession of hippocampal place cells J Comput Neurosci 9 5 30 10.1023/A:1008976210366 1:STN:280:DC%2BD3M%2FlvFeitQ%3D%3D 10946990 (Pubitemid 30468373)
6. A Bose M Recce 2001 Phase precession and phase-locking of hippocampal pyramidal cells Hippocampus 11 204 215 10.1002/hipo.1038 1:STN:280: DC%2BD38%2Fkt1Ojtg%3D%3D 11769305 (Pubitemid 32655282)
7. N Burgess A Jackson T Hartley J O'Keefe 2000 Predictions derived from modelling the hippocampal role in navigation Biol Cybern 83 301 312 10.1007/s004220000172 1:STN:280:DC%2BD3cvltFKitw%3D%3D 11007303
8. N Burgess C Barry J O'Keefe 2007 An oscillatory interference model of grid cell firing Hippocampus 17 801 812 10.1002/hipo.20327 17598147 (Pubitemid 47493460)
9. G Buzsáki 2002 Theta oscillations in the hippocampus Neuron 33 325 340 10.1016/S0896-6273(02)00586-X 11832222 (Pubitemid 34158839)
10. AD Ekstrom J Meltzer BL McNaughton CA Barnes 2001 NMDA receptor antagonism blocks experience-dependent expansion of hippocampal "place fields" Neuron 31 631 638 10.1016/S0896-6273(01)00401-9 1:CAS:528:DC%2BD3MXmvV2iurs%3D 11545721 (Pubitemid 32835117)
11. SE Fox 1989 Membrane potential and impedance changes in hippocampal pyramidal cells during theta rhythm Exp Brain Res 77 283 294 10.1007/BF00274985 1:STN:280:DyaK3c%2FgsFyjsA%3D%3D 2792276
12. G Gasparini M Migliore JC Magee 2004 On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons J Neurosci 24 11046 11056 10.1523/JNEUROSCI.2520-04.2004 1:CAS:528:DC%2BD2cXhtFagurbK 15590921 (Pubitemid 40012964)
13. NL Golding N Spruston 1998 Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons Neuron 21 1189 1200 10.1016/S0896-6273(00)80635-2 1:CAS:528:DyaK1cXotVWjur0%3D 9856473 (Pubitemid 29018087)
14. NL Golding W Kath N Spruston 2001 Dichotomy of action-potential backpropagation in CA1 pyramidal neuron dendrites J Neurophysiol 86 2998 3010 1:STN:280:DC%2BD38%2FivVOgtg%3D%3D 11731556
15. T Hafting M Fyhn T Bonnevie M Moser E Moser 2008 Hippocampus-independent phase precession in entorhinal grid cells Nature 453 1248 1253 10.1038/nature06957 1:CAS:528:DC%2BD1cXnslGks7Y%3D 18480753 (Pubitemid 351913591)
16. KD Harris DA Henze H Hirase X Leinekugel G Dragoi A Czurkó G Buzsáki 2002 Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells Nature 417 738 741 10.1038/nature00808 1:CAS:528:DC%2BD38XksVGjurY%3D 12066184 (Pubitemid 34640626)
17. T Hartley N Burgess C Lever F Cacucci J O'Keefe 2000 Modeling place fields in terms of the cortical inputs to the hippocampus Hippocampus 10 369 379 10.1002/1098-1063(2000)10:4<369::AID-HIPO3>3.0.CO;2-0 1:STN:280:DC%2BD3M%2FmsFCiuw%3D%3D 10985276 (Pubitemid 30696868)
18. CD Harvey F Collman DA Dombeck DW Tank 2009 Intracellular dynamics of hippocampal place cells during virtual navigation Nature 461 941 946 10.1038/nature08499 1:CAS:528:DC%2BD1MXhtlCqs73J 19829374
19. DA Hoffman D Johnston 1999 Neuromodulation of dendritic action potentials J Neurophysiol 81 408 411 1:CAS:528:DyaK1MXhtVersLc%3D 9914302
20. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons Nature 387 869 875 10.1038/42571 1:CAS:528:DyaK2sXkt1Glt7g%3D 9202119
21. H Hu K Vervaeke L Graham JF Storm 2009 Complementary theta resonance filtering by two spatially segregated mechanisms in CA1 hippocampal pyramidal neurons J Neurosci 29 14472 14483 10.1523/JNEUROSCI.0187-09.2009 1:CAS:528:DC%2BD1MXhsVOhsLnE 19923281
22. Z Huhn G Orbán P Érdi M Lengyel 2005 Theta oscillation-coupled dendritic spiking integrates inputs on a long time scale Hippocampus 15 950 962 10.1002/hipo.20112 16108010 (Pubitemid 41556424)
23. J Huxter N Burgess J O'Keefe 2003 Independent rate and temporal coding in hippocampal pyramidal cells Nature 425 828 832 10.1038/nature02058 1:CAS:528:DC%2BD3sXotlWqtrw%3D 14574410 (Pubitemid 37351465)
24. T Jarsky A Roxin WL Kath N Spruston 2005 Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons Nat Neurosci 8 1667 1676 10.1038/nn1599 1:CAS:528:DC%2BD2MXht1Gis7%2FO 16299501 (Pubitemid 41683193)
25. D Johnston DA Hoffman CM Colbert JC Magee 1999 Regulation of back-propagating action potentials in hippocampal neurons Curr Opin Neurobiol 9 288 292 10.1016/S0959-4388(99)80042-7 1:CAS:528:DyaK1MXktVylu7g%3D 10395568 (Pubitemid 29267598)
26. A Kamondi L Acsády X-J Wang G Buzsáki 1998 Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials Hippocampus 8 244 261 10.1002/(SICI)1098-1063(1998)8:3<244::AID-HIPO7>3.0.CO;2-J 1:STN:280:DyaK1czisVGitA%3D%3D 9662139 (Pubitemid 28288857)
27. A Kepecs X-J Wang 2000 Analysis of complex bursting in cortical pyramidal neuron models Neurocomputing 32-33 181 187 10.1016/S0925-2312(00)00162-4 (Pubitemid 30459718)
28. A Kepecs X-J Wang J Lisman 2002 Bursting neurons signal input slope J Neurosci 22 9053 9062 1:CAS:528:DC%2BD38XosV2is74%3D 12388612
29. ME Larkum JJ Zhu B Sakmann 2001 Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons J Physiol 533 447 466 10.1111/j.1469-7793. 2001.0447a.x 1:CAS:528:DC%2BD3MXltVSktbo%3D 11389204 (Pubitemid 32520000)
30. M Lengyel Z Szatmáry P Érdi 2003 Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing Hippocampus 13 700 714 10.1002/hipo.10116 12962315 (Pubitemid 37098758)
31. LS Leung CY Yim 1986 Intracellular records of theta rhythm in hippocampal CA1 cells of the rat Brain Res 367 323 327 10.1016/0006-8993(86)91611-2 1:STN:280:DyaL287ovVyjtg%3D%3D 3008923
32. C Lever S Burton A Jeewajee J O'Keefe N Burgess 2009 Boundary vector cells in the subiculum of the hippocampal formation J Neurosci 29 9771 9777 10.1523/JNEUROSCI.1319-09.2009 1:CAS:528:DC%2BD1MXpvFOmur4%3D 19657030
33. JC Magee 1998 Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons J Neurosci 18 7613 7624 1:CAS:528:DyaK1cXmtleqt7k%3D 9742133
34. JC Magee 2001 Dendritic mechanisms of phase precession in hippocampal CA1 pyramidal neurons J Neurophysiol 86 528 532 1:STN:280:DC%2BD3MznsVyhsA%3D%3D 11431530
35. Z Mainen TJ Sejnowski 1996 Influence of dendritic structure on firing pattern in model neocortical neurons Nature 382 363 366 10.1038/382363a0 1:CAS:528:DyaK28Xks1Wnsr0%3D 8684467 (Pubitemid 26260465)
36. BL McNaughton CA Barnes J O'Keefe 1983 The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely moving rats Exp Brain Res 52 41 49 10.1007/BF00237147 1:STN:280: DyaL2c%2FivFSnsg%3D%3D 6628596
37. MR Mehta MC Quirk MA Wilson 2000 Experience-dependent asymmetric shape of hippocampal receptive fields Neuron 25 707 715 10.1016/S0896-6273(00)81072-7 1:CAS:528:DC%2BD3cXisFKrtbY%3D 10774737
38. MR Mehta AK Lee MA Wilson 2002 Role of experience and oscillations in transforming a rate code into a temporal code Nature 417 741 746 10.1038/nature00807 1:CAS:528:DC%2BD38XksVGjurg%3D 12066185 (Pubitemid 34640627)
39. M Migliore M Ferrante GA Ascoli 2005 Signal propagation in oblique dendrites of CA1 pyramidal cells J Neurophysiol 94 4145 4155 10.1152/jn.00521.2005 16293591 (Pubitemid 41691775)
40. J O'Keefe ML Recce 1993 Phase relationship between hippocampal place units and the EEG theta rhythm Hippocampus 3 317 330 10.1002/hipo.450030307 8353611
41. J O'Keefe N Burgess 2005 Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells Hippocampus 15 853 866 10.1002/hipo.20115 16145693 (Pubitemid 41556415)
42. + channels supports the activity-dependent enhancement of back-propagating action potentials in hippocampal CA1 pyramidal neurons J Neurophysiol 85 1013 1016 1:CAS:528:DC%2BD3MXktVaqtLk%3D 11160533
43. PF Pinsky J Rinzel 1994 Intrinsic and network rhythmogenesis in a reduced traub model for CA3 neurons J Comput Neurosci 1 39 60 10.1007/BF00962717 1:STN:280:DyaK28zosVegtA%3D%3D 8792224
44. MC Quirk KI Blum MA Wilson 2001 Experience-dependent changes in extracellular spike amplitude may reflect regulation of dendritic action potential back-propagation in rat hippocampal pyramidal cells J Neurosci 21 240 248 1:CAS:528:DC%2BD3MXmtVOnsA%3D%3D 11150341
45. WE Skaggs BL McNaughton MA Wilson CA Barnes 1996 Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences Hippocampus 6 149 172 10.1002/(SICI)1098-1063(1996)6:2<149::AID-HIPO6>3.0. CO;2-K 1:STN:280:DyaK28zovF2hsA%3D%3D 8797016 (Pubitemid 26232443)
46. T Solstad CN Boccara E Kropff MB Moser EI Moser 2008 Representation of geometric borders in the entorhinal cortex Science 322 1865 1868 10.1126/science.1166466 1:CAS:528:DC%2BD1cXhsFSmtrbJ 19095945
47. WA Spencer ER Kandel 1961 Electrophysiology of hippocampal neurons J Neurophysiol 24 272 288
48. N Spruston 2008 Pyramidal neurons: dendritic structure and synaptic integration Nat Rev Neurosci 9 206 221 10.1038/nrn2286 1:CAS:528: DC%2BD1cXitFKntbo%3D 18270515 (Pubitemid 351272663)
49. Y Yamaguchi 2003 A theory of hippocampal memory based on theta phase precession Biol Cybern 89 1 9 12836028
50. Y Yamaguchi Y Aota BL McNaughton P Lipa 2002 Bimodality of theta phase precession in hippocampal place cells in freely running rats J Neurophysiol 87 2629 2642 12037166
51. Y Yamaguchi N Sato H Wagatsuma Z Wu C Molter Y Aota 2007 A unified view of theta-phase coding in the entorhinal-hippocampal system Curr Opin Neurobiol 17 197 204 10.1016/j.conb.2007.03.007 1:CAS:528:DC%2BD2sXksFeht74%3D 17379502 (Pubitemid 46584801)
52. A Ylinen I Soltész A Bragin M Penttonen A Sik G Buzsáki 1995 Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells and basket cells Hippocampus 5 78 90 10.1002/hipo.450050110 1:STN:280:DyaK2MzgslKksw%3D%3D 7787949
53. 2+ accumulations in dendrites of neocortical pyramidal neurons: an apical band and evidence for two functional compartments Neuron 13 23 43 10.1016/0896-6273(94) 90457-X 1:CAS:528:DyaK2cXmsFajtbY%3D 8043278
54. M Zugaro L Monconduit G Buzsáki 2005 Spike phase precession persists after transient intrahippocampal perturbation Nat Neurosci 8 67 71 10.1038/nn1369 1:CAS:528:DC%2BD2MXhtFWntg%3D%3D 15592464 (Pubitemid 41236733)