Cosine directional tuning of theta cell burst frequencies: Evidence for spatial coding by oscillatory interference

Journal of Neuroscience

Volumn 31, Issue 45, 2011, Pages 16157-16176

  Welday, Adam C ^a   Shlifer, I Gary ^a   Bloom, Matthew L ^a   Zhang, Kechen ^b   Blair, Hugh T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; COMPUTER SIMULATION; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; MALE; MATHEMATICAL ANALYSIS; NERVE CELL NETWORK; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; OSCILLATION; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; RAT; SEPTOHIPPOCAMPAL SYSTEM; SIGNAL TRANSDUCTION; SPATIAL MEMORY; THETA CELL; THETA CELL BURST FREQUENCY;

ACTION POTENTIALS; ANIMALS; BIOPHYSICS; BRAIN; COMPUTER SIMULATION; CUES; EXPLORATORY BEHAVIOR; MALE; MODELS, NEUROLOGICAL; MOVEMENT; NEURONS; ORIENTATION; RATS; RATS, LONG-EVANS; SPACE PERCEPTION; THETA RHYTHM; VIDEO RECORDING; WAKEFULNESS;

EID: 80755127310     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0712-11.2011     Document Type: Article

References (88)

1. Bissiere S, Zelikowsky M, Ponnusamy R, Jacobs N, Blair HT, Fanselow MS (2011) Electrical synapses control hippocampal contributions to fear learning and memory. Science 331:87-91.
2. Blair HT, Sharp PE (1995) Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction. J Neurosci 15:6260-6270.
3. Blair HT, Welday AC, Zhang K (2007) Scale-invariant memory representations emerge from moire ́ interference between grid fields that produce theta oscillations: a computational model. J Neurosci 27:3211-3229.
4. Blair HT, Gupta K, Zhang K (2008) Conversion of a phase- to a rate-coded position signal by a three-stage model of theta cells, grid cells, and place cells. Hippocampus 18:1239-1255.
5. 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.
6. Brun VH, Leutgeb S, Wu HQ, Schwarcz R, Witter MP, Moser EI, Moser MB (2008a) Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron 57:290-302.
7. Brun VH, Solstad T, Kjelstrup KB, Fyhn M, Witter MP, Moser EI, Moser M-B (2008b) Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus 18:1200-1212.
8. Burgess N (2008) Grid cells and theta as oscillatory interference: theory and predictions. Hippocampus 18:1157-1174.
9. Burgess N, Barry C, O'Keefe J (2007) An oscillatory interference model of grid cell firing. Hippocampus 17:801-812.
10. Burgess N, Barry C, Jeffery KJ, O'Keefe J (2005) A grid and place cell model of path integration utilizing phase precession versus theta. Paper presented 1st Annual conference on Computational Cognitive Neuroscience, November 10-11, Washington, DC.
11. Buzsáki G (2006) Rhythms of the brain. New York: Oxford UP.
12. Carnevale NT, Hines ML (2006) The NEURON book. Cambridge, UK: Cambridge UP.
13. Destexhe A, Mainen ZF, Sejnowski TJ (1994) An efficient method for computing synaptic conductances based on a kinetic model of receptor binding. Neural Comput 6:10-14.
14. Düzel E, Penny WD, Burgess N (2010) Brain oscillations and memory. Curr Opin Neurobiol 20:143-149.
15. Eichenbaum H, Cohen NJ (1992) The hippocampus-what does it do? Behav Neural Biol 57:2-36.
16. Etienne AS, Jeffery KJ (2004) Path integration. Hippocampus 14:180-192.
17. Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170-173.
18. Geisler C, Robbe D, Zugaro M, Sirota A, Buzsáki G (2007) Hippocampal place cell assemblies are speed-controlled oscillators. Proc Natl Acad Sci U S A 104:8149-8154.
19. Geisler C, Diba K, Pastalkova E, Mizuseki K, Royer S, Buzsáki G (2010) Temporal delays among place cells determine the frequency of population theta oscillations in the hippocampus. Proc Natl Acad Sci U S A 107:7957-7962.
20. Giocomo LM, Zilli EA, Fransén E, Hasselmo ME (2007) Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 315:1719-1722.
21. Gogolák G, Petsche H, Sterc J, Stumpf C (1967) Septum cell activity in the rabbit under reticular stimulation. Brain Res 5:508-510.
22. Gorchetchnikov A, Grossberg S (2007) Space, time and learning in the hippocampus: how fine spatial and temporal scales are expanded into population codes for behavioral control. Neural Netw 20:182-193.
23. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801-806.
24. Hartley T, Burgess N, Lever C, Cacucci F, O'Keefe J (2000) Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 10:369-379.
25. Hartmann WM (1998) Signals, sound, and sensation. New York: Springer.
26. Harvey CD, Collman F, Dombeck DA, Tank DW (2009) Intracellular dynamic of hippocampal place cells during virtual navigation. Nature 461:941-946.
27. Hasselmo ME (2008) Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting. Hippocampus 18:1213-1229.
28. Hasselmo ME, Giocomo LA, Zilli EA (2007) Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus 17:1252-1271.
29. Hasselmo ME, Giocomo LM, Brandon MP, Yoshida M (2010) Cellular dynamical mechanisms for encoding the time and place of events along spatiotemporal trajectories in episodic memory. Behav Brain Res 215:261-274.
30. Hines ML, Morse T, Migliore M, Carnevale NT, Shepherd GM (2004) ModelDB: a database to support computational neuroscience. J. Comput. Neurosci 17:7-11.
31. Hopfield JJ, Brody CD (2001) What s a moment? Transient synchrony as a collective mechanism for spatiotemporal integration. Proc Natl Acad U S A 98:128207.
32. Jeewajee A, Barry C, O'Keefe J, Burgess N (2008a) Grid cells and theta as oscillatory interference: electrophysiological data from freely moving rats. Hippocampus 18:1175-1185.
33. Jeewajee A, Lever C, Burton S, O'Keefe J, Burgess N (2008b) Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus 18:340-348.
34. Jones EG (1985) The thalamus. New York: Plenum.
35. Kamondi A, Acsády L, Wang XJ, Buzsáki G (1998) Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity dependent phase precession of action potentials. Hippocampus 8:244-261.
36. King C, Recce 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 behavior and hippocampal theta. Eur J Neurosci 10:464-477.
37. Knierim JJ, Kudrimoti HS, McNaughton BL (1995) Place cells, head direction cells, and the learning of landmark stability. J Neurosci 15:1648-1659.
38. Knierim JJ, Kudrimoti HS, McNaughton BL (1998) Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J Neurophysiol 80:425-446.
39. 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.
40. Koepsell K, Wang X, Hirsch JA, Sommer FT (2010) Exploring the function of neural oscillations in early sensory systems. Front Neurosci 4:53.
41. Laurent G, Stopfer M, Friedrich RW, Rabinovich MI, Volkovskii A, Abarbanel HD (2001) Odor encoding as an active, dynamical process: experiments, computation, and theory. Ann Rev Neurosci 24:263-297.
42. Lengyel M, Szatmáry Z, Erdi P (2003) Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing. Hippocampus 13:700-714.
43. Leutgeb JK, Leutgeb S, Moser MB, Moser EI (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961-966.
44. Lever C, Burton S, Jeewajee A, O'Keefe J, Burgess N (2009) Boundary vector cells in the subiculum of the hippocampal formation. J Neurosci 29:9771-9777.
45. Losonczy A, Zemelman BV, Vaziri A, Magee JC (2010) Network mechanisms of theta related neuronal activity in hippocampal CA1 pyramidal neurons. Nat Neurosci 13:967-972.
46. Lubenov EV, Siapas AG (2009) Hippocampal theta oscillations are traveling waves. Nature 459:534-539.
47. Matell MS, Meck WH (2004) Cortico-striatal circuits and interval timing: coincidence detection of oscillatory processes. Brain Res Cogn Brain Res 21:139-170.
48. McNaughton BL, Barnes CA, Gerrard JL, Gothard K, Jung MW, Knierim JJ, Kudrimoti H, Qin Y, Skaggs WE, Suster M, Weaver KL (1996) Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol 199:173-185.
49. 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.
50. Mhatre H, Gorchetchnikov A, Grossberg S (2010) Grid cell hexagonal patterns formed by fast self-organized learning within entorhinal cortex. Hippocampus. Advance online publication. doi:10.1002/hipo.20901.
51. Miall C (1989) The storage of time intervals using oscillating neurons. Neural Comput 1:359-371.
52. Mizumori SJ, McNaughton BL, Barnes CA, Fox KB (1989) Preserved spatial coding in hippocampal CA1 pyramidal cells during reversible suppression of CA3c output: evidence for pattern completion in hippocampus. J Neurosci 9:3915-3928.
53. Monaco JD, Abbott LR (2011) Modular realignment of entorhinal grid cell activity as a basis for hippocampal remapping. J Neurosci 31:9414-9425.
54. Muller RU, Kubie JL (1987) The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 7:1951-1968.
55. O'Keefe J, Burgess N (2005) Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus 15:853-866.
56. O'Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171-175.
57. O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map. New York: Oxford UP.
58. O'Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317-330.
59. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates. Sydney: Academic.
60. Petsche H, Gogolak G, Vanzwieten PA (1965) Rhythmicity of septal cell discharges at various levels of reticular excitation. Electroencephalogr Clin Neurophysiol 19:25-33.
61. Ranck JB Jr (1973) Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp Neurol 41:461-531.
62. Redish AD, Elga AN, Touretzky DS (1996) A coupled attractor model of the rodent head-direction system. Network 7:671-685.
63. Remme MW, Lengyel M, Gutkin BS (2010) Democracy-independence trade-off in oscillating dendrites and its implications for grid cells. Neuron 66:429-437.
64. Rivas J, Gatztelu JM, García-Austt E (1996) Changes in hippocampal cell discharge patterns and theta rhythm spectral properties as a function of walking velocity in the guinea pig. Exp Brain Res 108:113-118.
65. Rutishauser U, Ross IB, Mamelak AN, Schuman EM (2010) Human memory strength is predicted by theta-frequency phase locking of single neurons. Nature 464:903-907.
66. 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.
67. Savelli F, Knierim JJ (2010) Hebbian analysis of the transformation of medial entorhinal grid-cell inputs to hippocampal place fields. J. Neurophysiol 103:3167-3183.
68. Savelli F, Yoganarasimha D, Knierim JJ (2008) Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18:1270-1282.
69. Sharp PE, Koester K (2008) Lesions of the mammillary body region severely disrupt the cortical head direction, but not place cell signal. Hippocampus 18:766-784.
70. Skaggs WE, Knierim JJ, Kudrimoti HS, McNaughton BL (1995) A model of the neural basis of the rat's sense of direction. Adv Neural Inf Process Syst 7:173-180.
71. Skaggs WE, McNaughton BL, Gothard KM, Markus EJ (1993) An information-theoretic approach to deciphering the hippocampal code. Adv Neural Inf Process Syst 5:1030-1037.
72. Solstad T, Moser EI, Einevoll GT (2006) From grid cells to place cells: a mathematical model. Hippocampus 16:1026-1031.
73. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI (2008) Representation of geometric borders in the entorhinal cortex. Science 322: 1865-1868.
74. Song P, Wang XJ (2005) Angular path integration by moving "hill of activity": a spiking neuron model without recurrent excitation of the headdirection system. J Neurosci 25:1002-1014.
75. Squire LR, Schacter DL, eds (2002) Neuropsychology of memory, Ed 3. New York: Guilford.
76. Taube JS (2007) The head direction signal: origins and sensorimotor integration. Annu Rev Neurosci 30:181-207.
77. Taube JS, Muller RU, Ranck JB Jr (1990) Head direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J Neurosci 10:436-437.
78. Tiesinga P, Fellous JM, Sejnowski TJ (2008) Regulation of spike timing in visual cortical circuits. Nat Rev Neurosci 9:97-107.
79. Tsanov M, Chah E, Vann SD, Reilly RB, Erichsen JT, Aggleton JP, O'Mara SM (2011a) Theta-modulated head direction cells in the rat anterior thalamus. J Neurosci 31:9489-9502.
80. Tsanov M, Chah E, Wright N, Vann SD, Reilly R, Erichsen JT, Aggleton JP, O'Mara SM (2011b) Oscillatory entrainment of thalamic neurons by theta rhythm in freely moving rats. J Neurophysiol 105:4-17.
81. Uebachs M, Opitz T, Royeck M, Dickhof G, Horstmann MT, Isom LL, Beck H (2010) Efficacy loss of the anticonvulsant carbamazepine in mice lacking sodium channel beta subunits via paradoxical effects on persistent sodium currents. J Neurosci 30:8489-8501.
82. Van Cauter T, Poucet B, Save E (2008) Unstable CA1 place cell representation in rats with entorhinal cortex lesions. Eur J Neurosci 27:1933-1946.
83. Vann SD, Aggleton JP (2004) The mammillary bodies: two memory systems in one? Nat Rev Neurosci 5:35-44.
84. Vertes RP, Kocsis B (1997) Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81:893-926.
85. Wills TJ, Cacucci F, Burgess N, O'Keefe J (2010) Development of the hippocampal cognitive map in preweanling rats. Science 328:1573-1576.
86. Zhang K (1996) Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J Neurosci 16:2112-2126.
87. Zilli EA, Hasselmo ME (2010) Coupled noisy spiking neurons as velocitycontrolled oscillators in a model of grid cell spatial firing. J Neurosci 30:13850-13860.
88. 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.