Neuronal rebound spiking, resonance frequency and theta cycle skipping may contribute to grid cell firing in medial entorhinal cortex

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1635, 2014, Pages

  Hasselmo, Michael E ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

Entorhinal cortex; Grid cells; Head direction; Place cells; Rat; Theta rhythm

Indexed keywords

BRAIN; EXPERIMENTAL STUDY; FREQUENCY ANALYSIS; NEUROLOGY; NUMERICAL MODEL; PERIODICITY; RESONANCE;

ACETYLCHOLINE;

ACTION POTENTIAL; ANIMAL; ARTICLE; BIOLOGICAL MODEL; COMPUTER SIMULATION; CYTOLOGY; DEPTH PERCEPTION; ENTORHINAL CORTEX; GRID CELLS; HEAD DIRECTION; NERVE CELL; PHYSIOLOGY; PLACE CELLS; RAT; THETA RHYTHM;

ENTORHINAL CORTEX; GRID CELLS; HEAD DIRECTION; PLACE CELLS; RAT; THETA RHYTHM;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; COMPUTER SIMULATION; ENTORHINAL CORTEX; MODELS, NEUROLOGICAL; NEURONS; SPACE PERCEPTION; THETA RHYTHM;

EID: 84906921296     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0523     Document Type: Article

References (78)

1. Moser EI, Moser MB. 2008 A metric for space. Hippocampus 18, 1142-1156. (doi:10.1002/ hipo.20483)
2. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB. 2004 Spatial representation in the entorhinal cortex. Science 305, 1258-1264. (doi:10.1126/science. 1099901)
3. Burgess N, Barry C, Jeffery KJ, O'Keefe J. 2005 A grid and place cell model of path integration utilizing phase precession versus theta. Poster presented at the Computational Cognitive Neuroscience Conference, Washington DC, 10-11 November 2005. See http://cdn.f1000.com/posters/ docs/225.
4. Burgess N, Barry C, O'Keefe J. 2007 An oscillatory interference model of grid cell firing. Hippocampus 17, 801-812. (doi:10.1002/hipo.20327)
5. Burgess N. 2008 Grid cells and theta as oscillatory interference: theory and predictions. Hippocampus 18, 1157-1174. (doi:10.1002/hipo.20518)
6. Blair HT, Gupta K, Zhang K. 2008 Conversion of a phaseto a rate-coded position signal by a three-stage model of theta cells, grid cells, and place cells. Hippocampus 18, 1239-1255. (doi:10.1002/hipo.20509)
7. Hasselmo ME. 2008 Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting. Hippocampus 18, 1213-1229. (doi:10.1002/hipo.20512)
8. Hafting T, Fyhn M, Bonnevie T, Moser MB, Moser EI. 2008 Hippocampus-independent phase precession in entorhinal grid cells. Nature 453, 1248-1252. (doi:10.1038/nature06957)
9. Jeewajee A, Barry C, O'Keefe J, Burgess N. 2008 Grid cells and theta as oscillatory interference: electrophysiological data from freely moving rats. Hippocampus 18, 1175-1185. (doi:10.1002/hipo.20510)
10. Brandon MP, Bogaard AR, Libby CP, Connerney MA, Gupta K, Hasselmo ME. 2011 Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 332, 595-599. (doi:10. 1126/science.1201652)
11. Koenig J, Linder AN, Leutgeb JK, Leutgeb S. 2011 The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332, 592-595. (doi:10.1126/science.1201685)
12. Stensola H, Stensola T, Solstad T, Froland K, Moser MB, Moser EI. 2012 The entorhinal grid map is discretized. Nature 492, 72-78. (doi:10.1038/ nature11649)
13. Climer JR, Newman EL, Hasselmo ME. 2013 Phase coding by grid cells in unconstrained environments: two-dimensional phase precession. Eur. J. Neurosci. 38, 2526-2541. (doi:10.1111/ejn.12256)
14. Mitchell SJ, Ranck Jr JB. 1980 Generation of theta rhythm in medial entorhinal cortex of freely moving rats. Brain Res. 189, 49-66. (doi:10.1016/0006-8993(80)90006-2)
15. Mitchell SJ, Rawlins JN, Steward O, Olton DS. 1982 Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats. J. Neurosci. 2, 292-302.
16. Alonso A, Garcia-Austt E. 1987 Neuronal sources of theta rhythm in the entorhinal cortex of the rat. I. Laminar distribution of theta field potentials. Exp. Brain Res. 67, 493-501. (doi:10.1007/ BF00247282)
17. Jeffery KJ, Donnett JG, O'Keefe J. 1995 Medial septal control of theta-correlated unit firing in the entorhinal cortex of awake rats. Neuroreport 6, 2166-2170. (doi:10.1097/00001756-1995 11000-00017)
18. Fuhs MC, Touretzky DS. 2006 A spin glass model of path integration in rat medial entorhinal cortex. J. Neurosci. 26, 4266-4276. (doi:10.1523/ JNEUROSCI.4353-05.2006)
19. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB. 2006 Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 7, 663-678. (doi:10.1038/nrn1932)
20. Guanella A, Kiper D, Verschure P. 2007 A model of grid cells based on a twisted torus topology. Int. J. Neural Syst. 17, 231-240. (doi:10.1142/ S0129065707001093)
21. Burak Y, Fiete IR. 2009 Accurate path integration in continuous attractor network models of grid cells. PLoS Comput. Biol. 5, e1000291. (doi:10.1371/ journal.pcbi.1000291)
22. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser MB, Moser EI. 2006 Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312, 758-762. (doi:10.1126/science.1125572)
23. Barry C, Hayman R, Burgess N, Jeffery KJ. 2007 Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 10, 682-684. (doi:10.1038/nn1905)
24. Kropff E, Treves A. 2008 The emergence of grid cells: intelligent design or just adaptation? Hippocampus 18, 1256-1269. (doi:10.1002/ hipo.20520)
25. Mhatre H, Gorchetchnikov A, Grossberg S. 2010 Grid cell hexagonal patterns formed by fast self-organized learning within entorhinal cortex. Hippocampus 22, 320-334. (doi:10.1002/hipo.20901)
26. Si B, Kropff E, Treves A. 2012 Grid alignment in entorhinal cortex. Biol. Cybern. 106, 483-506. (doi:10.1007/s00422-012-0513-7)
27. Bonnevie T, Dunn B, Fyhn M, Hafting T, Derdikman D, Kubie JL, Roudi Y, Moser EI, Moser M-B. 2013 Grid cells require excitatory drive from the hippocampus. Nat. Neurosci. 16, 309-317. (doi:10.1038/nn.3311)
28. Welday AC, Shlifer IG, Bloom ML, Zhang K, Blair HT. 2011 Cosine directional tuning of theta cell burst frequencies: evidence for spatial coding by oscillatory interference. J. Neurosci. 31, 16 157-16 176. (doi:10.1523/JNEUROSCI.0712-11.2011)
29. Haas JS, White JA. 2002 Frequency selectivity of layer II stellate cells in the medial entorhinal cortex. J. Neurophysiol. 88, 2422-2429. (doi:10.1152/jn. 00598.2002)
30. Erchova I, Kreck G, Heinemann U, Herz AV. 2004 Dynamics of rat entorhinal cortex layer II and III cells: characteristics of membrane potential resonance at rest predict oscillation properties near threshold. J. Physiol. 560, 89-110. (doi:10. 1113/jphysiol.2004.069930)
31. Giocomo LM, Zilli EA, Fransen E, Hasselmo ME. 2007 Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 315, 1719-1722. (doi:10.1126/science.1139207)
32. Giocomo LM, Hasselmo ME. 2008 Computation by oscillations: implications of experimental data for theoretical models of grid cells. Hippocampus 18, 1186-1199. (doi:10.1002/hipo.20501)
33. Boehlen A, Heinemann U, Erchova I. 2010 The range of intrinsic frequencies represented by medial entorhinal cortex stellate cells extends with age. J. Neurosci. 30, 4585-4589. (doi:10.1523/ JNEUROSCI.4939-09.2010)
34. Pastoll H, Ramsden HL, Nolan MF. 2012 Intrinsic electrophysiological properties of entorhinal cortex stellate cells and their contribution to grid cell firing fields. Front. Neural Circuits 6, 17. (doi:10.3389/ fncir.2012.00017)
35. Canto CB, Witter MP. 2012 Cellular properties of principal neurons in the rat entorhinal cortex. II. The medial entorhinal cortex. Hippocampus 22, 1277-1299. (doi:10.1002/hipo.20993)
36. Canto CB, Witter MP. 2012 Cellular properties of principal neurons in the rat entorhinal cortex. I. The lateral entorhinal cortex. Hippocampus 22, 1256-1276. (doi:10.1002/hipo.20997)
37. Shay CF, Boardman IS, James NM, Hasselmo ME. 2012 Voltage dependence of subthreshold resonance frequency in layer II of medial entorhinal cortex. Hippocampus 22, 1733-1749. (doi:10.1002/ hipo.22008)
38. Alonso A, Klink R. 1993 Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J. Neurophysiol. 70, 128-143.
39. Alonso A, Llinas RR. 1989 Subthreshold Nadependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342, 175-177. (doi:10.1038/342175a0)
40. Deshmukh SS, Yoganarasimha D, Voicu H, Knierim JJ. 2010 Theta modulation in the medial and the lateral entorhinal cortices. J. Neurophysiol. 104, 994-1006. (doi:10.1152/jn.01141.2009)
41. Brandon MP, Bogaard AR, Schultheiss NW, Hasselmo ME. 2013 Segregation of cortical head direction cell assemblies on alternating theta cycles. Nat. Neurosci. 16, 739-748. (doi:10.1038/nn.3383)
42. King C, Reece M, O'Keefe J. 1998 The rhythmicity of cells of the medial septum/diagonal band of Broca in the awake freely moving rat: relationships with behaviour and hippocampal theta. Eur. J. Neurosci. 10, 464-477. (doi:10.1046/j.1460-9568.1998.00026.x)
43. Varga V, Hangya B, Kranitz K, Ludanyi A, Zemankovics R, Katona I, Shigemoto R, Freund TF, Borhegyi Z. 2008 The presence of pacemaker HCN channels identifies theta rhythmic GABAergic neurons in the medial septum. J. Physiol. 586, 3893-3915. (doi:10.1113/jphysiol.2008.155242)
44. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. 2005 Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801-806. (doi:10.1038/nature03721)
45. Hargreaves EL, Rao G, Lee I, Knierim JJ. 2005 Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308, 1792-1794. (doi:10.1126/science.1110449)
46. Heys JG, Giocomo LM, Hasselmo ME. 2010 Cholinergic modulation of the resonance properties of stellate cells in layer II of medial entorhinal cortex. J. Neurophysiol. 104, 258-270. (doi:10.1152/jn.00492.2009)
47. Acquas E, Wilson C, Fibiger HC. 1996 Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation, and fear. J. Neurosci. 16, 3089-3096.
48. Barry C, Ginzberg LL, O'Keefe J, Burgess N. 2012 Grid cell firing patterns signal environmental novelty by expansion. Proc. Natl Acad. Sci. USA 109, 17 687-17 692. (doi:10.1073/pnas.1209918109)
49. Barry C, Heys JG, Hasselmo ME. 2012 Possible role of acetylcholine in regulating spatial novelty effects on theta rhythm and grid cells. Front. Neural Circuits 6, 5. (doi:10.3389/fncir.2012.00005)
50. Giocomo LM, Hasselmo ME. 2009 Knock-out of HCN1 subunit flattens dorsal-ventral frequency gradient of medial entorhinal neurons in adult mice. J. Neurosci. 29, 7625-7630. (doi:10.1523/ JNEUROSCI.0609-09.2009)
51. Giocomo LM, Hussaini SA, Zheng F, Kandel ER, Moser MB, Moser EI. 2011 Grid cells use HCN1 channels for spatial scaling. Cell 147, 1159-1170. (doi:10.1016/j.cell.2011.08.051)
52. Heys JG, MacLeod KM, Moss CF, Hasselmo ME. 2013 Bat and rat neurons differ in theta-frequency resonance despite similar coding of space. Science 340, 363-367. (doi:10.1126/science.1233831)
53. Yartsev MM, Witter MP, Ulanovsky N. 2011 Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479, 103-107. (doi:10.1038/ nature10583)
54. Guanella A, Verschure PF. 2007 Prediction of the position of an animal based on populations of grid and place cells: a comparative simulation study. J. Integr. Neurosci. 6, 433-446. (doi:10.1142/ S0219635207001556)
55. Pastoll H, Solanka L, van Rossum MC, Nolan MF. 2013 Feedback inhibition enables theta-nested gamma oscillations and grid firing fields. Neuron 77, 141-154. (doi:10.1016/j.neuron.2012.11.032)
56. Navratilova Z, Giocomo LM, Fellous JM, Hasselmo ME, McNaughton BL. 2012 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. (doi:10.1002/hipo.20939)
57. Dickson CT, Mena AR, Alonso A. 1997 Electroresponsiveness of medial entorhinal cortex layer III neurons in vitro. Neuroscience 81, 937-950. (doi:10.1016/S0306-4522(97)00263-7)
58. Engel TA, Schimansky-Geier L, Herz AV, Schreiber S, Erchova I. 2008 Subthreshold membrane-potential resonances shape spike-train patterns in the entorhinal cortex. J. Neurophysiol. 100, 1576-1589. (doi:10.1152/jn.01282.2007)
59. Schreiber S, Erchova I, Heinemann U, Herz AV. 2004 Subthreshold resonance explains the frequencydependent integration of periodic as well as random stimuli in the entorhinal cortex. J. Neurophysiol. 92, 408-415. (doi:10.1152/ jn.01116.2003)
60. Izhikevich EM. 2007 Dynamical systems in neuroscience: the geometry of excitability and bursting, p. 315. Cambridge, MA: MIT Press.
61. Blair HT, Wu A, Cong J. 2014 Oscillatory neurocomputing with ring attractors: a network architecture for mapping locations in space onto patterns of neural synchrony. Phil. Trans. R. Soc. B 369, 20120526. (doi:10.1098/rstb.2012.0526)
62. Mizuseki K, Sirota A, Pastalkova E, Buzsaki G. 2009 Theta oscillations provide temporal windows for local circuit computation in the entorhinalhippocampal loop. Neuron 64, 267-280. (doi:10.1016/j.neuron.2009.08.037)
63. Couey JJ et al. 2013 Recurrent inhibitory circuitry as a mechanism for grid formation. Nat. Neurosci. 16, 318-324. (doi:10.1038/nn.3310)
64. Yoshida M, Giocomo LM, Boardman I, Hasselmo ME. 2011 Frequency of subthreshold oscillations at different membrane potential voltages in neurons at different anatomical positions on the dorsoventral axis in the rat medial entorhinal cortex. J. Neurosci. 31, 12 683-12 694. (doi:10.1523/JNEUROSCI.1654-11.2011)
65. Hinman JR, Penley SC, Long LL, Escabi MA, Chrobak JJ. 2010 Septotemporal variation in dynamics of theta: speed and habituation. J. Neurophysiol. 105, 2675-2686. (doi:10.1152/jn.00837.2010)
66. Beed P, Gundlfinger A, Schneiderbauer S, Song J, Bohm C, Burgalossi A, Brecht M, Vida I, Schmitz D. 2013 Inhibitory gradient along the dorsoventral axis in the medial entorhinal cortex. Neuron 79, 1197-1207. (doi:10.1016/j.neuron.2013.06.038)
67. Zilli EA, Hasselmo ME. 2010 Coupled noisy spiking neurons as velocity-controlled oscillators in a model of grid cell spatial firing. J. Neurosci. 30, 13 850-13 860. (doi:10.1523/JNEUROSCI.0547-10.2010)
68. Zilli EA, Yoshida M, Tahvildari B, Giocomo LM, Hasselmo ME. 2009 Evaluation of the oscillatory interference model of grid cell firing through analysis and measured period variance of some biological oscillators. PLoS Comput. Biol. 5, e1000573. (doi:10.1371/journal.pcbi.1000573)
69. Remme MW, Lengyel M, Gutkin BS. 2009 The role of ongoing dendritic oscillations in single-neuron dynamics. PLoS Comput. Biol. 5, e1000493. (doi:10.1371/journal.pcbi.1000493)
70. Remme MW, Lengyel M, Gutkin BS. 2010 Democracy-independence trade-off in oscillating dendrites and its implications for grid cells. Neuron 66, 429-437. (doi:10.1016/j.neuron. 2010.04.027)
71. Egorov AV, Hamam BN, Fransen E, Hasselmo ME, Alonso AA. 2002 Graded persistent activity in entorhinal cortex neurons. Nature 420, 173-178. (doi:10.1038/nature01171)
72. Fransén E, Tahvildari B, Egorov AV, Hasselmo ME, Alonso AA. 2006 Mechanism of graded persistent cellular activity of entorhinal cortex layer v neurons. Neuron 49, 735-746. (doi:10.1016/j.neuron.2006. 01.036)
73. Klink R, Alonso A. 1997 Muscarinic modulation of the oscillatory and repetitive firing properties of entorhinal cortex layer II neurons. J. Neurophysiol. 77, 1813-1828.
74. Klink R, Alonso A. 1997 Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J. Neurophysiol. 77, 1829-1843.
75. Hasselmo ME, Brandon MP. 2008 Linking cellular mechanisms to behavior: entorhinal persistent spiking and membrane potential oscillations may underlie path integration, grid cell firing, and episodic memory. Neural Plast. 2008, 658323. (doi:10.1155/2008/658323)
76. Hasselmo ME, Brandon MP. 2012 A model combining oscillations and attractor dynamics for generation of grid cell firing. Front. Neural Circuits 6, 30. (doi:10.3389/fncir.2012.00030)
77. Raudies F, Chapman GW, Brandon MP, Hasselmo ME. 2013 Movement direction is not coded by the firing of most entorhinal cells but is required by grid cell models. Soc. Neurosci. Abstr. 39, 696.11.
78. Milford MJ, Wiles J, Wyeth GF. 2010 Solving navigational uncertainty using grid cells on robots. PLoS Comput. Biol. 6, e1000995. (doi:10.1371/ journal.pcbi.1000995)