Theta modulation in the medial and the lateral entorhinal cortices

Journal of Neurophysiology

Volumn 104, Issue 2, 2010, Pages 994-1006

  Deshmukh, Sachin S ^a,b   Yoganarasimha, D ^a,d   Voicu, Horatiu ^a,e   Knierim, James J ^a,b,c  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL BRAIN RESEARCH CENTRE   (India)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTRIC POTENTIAL; HIPPOCAMPUS; LATERAL ETORHINAL CORTEX; MALE; MEDIAL ETORHINAL CORTEX; NERVE CONDUCTION; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RAT;

ACTION POTENTIALS; ANIMALS; BRAIN MAPPING; DELTA RHYTHM; ENTORHINAL CORTEX; HIPPOCAMPUS; MALE; PERIODICITY; RATS; RATS, LONG-EVANS; STATISTICS, NONPARAMETRIC; THETA RHYTHM; TIME FACTORS;

EID: 77955939518     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01141.2009     Document Type: Article

References (59)

1. Adey WR, Dunlop CW, Hendrix CE. Hippocampal slow waves. Distribution and phase relationships in the course of approach learning. Arch Neurol 3: 74-90, 1960.
2. Alonso A, Garcia-Austt E. 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, 1987a.
3. Alonso A, Garcia-Austt E. Neuronal sources of theta rhythm in the entorhinal cortex of the rat. II. Phase relations between unit discharges and theta field potentials. Exp Brain Res 67: 502-509, 1987b.
4. Alonso A, Klink R. Differential electroresponsiveness of stellate and pyramidal- like cells of medial entorhinal cortex layer II. J Neurophysiol 70: 128-143, 1993. (Pubitemid 23220304)
5. +-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342: 175-177, 1989.
6. Bi GQ, Poo MM. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18: 10464-10472, 1998.
7. Blair HT, Gupta K, Zhang K. 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, 2008.
8. Brun VH, Solstad T, Kjelstrup KB, Fyhn M, Witter MP, Moser EI, Moser MB. Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus 18: 1200-1212, 2008.
9. Burgess N, Barry C, O'Keefe J. An oscillatory interference model of grid cell firing. Hippocampus 17: 801-812, 2007. (Pubitemid 47493460)
10. Burwell RD, Amaral DG. Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. J Comp Neurol 398: 179-205, 1998.
11. Buzsáki G. Theta oscillations in the hippocampus. Neuron 33: 325-340, 2002.
12. Collins DR, Lang EJ, Paré D. Spontaneous activity of the perirhinal cortex in behaving cats. Neuroscience 89: 1025-1039, 1999.
13. Deacon TW, Eichenbaum H, Rosenberg P, Eckmann KW. Afferent connections of the perirhinal cortex in the rat. J Comp Neurol 220: 168-190, 1983.
14. Frank LM, Brown EN, Wilson MA. A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. J Neurophysiol 86: 2029-2040, 2001.
15. Fujisawa S, Buzsáki G. A novel (4 Hz) oscillation of prefrontal and hippocampal neurons in the waking rat. Program No. 192.12. 2009 Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience, 2009. Online.
16. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB. Spatial representation in the entorhinal cortex. Science 305: 1258-1264, 2004.
17. Giocomo LM, Hasselmo ME. Computation by oscillations: implications of experimental data for theoretical models of grid cells. Hippocampus 18: 1186-1199, 2008.
18. Giocomo LM, Zilli EA, Fransen E, Hasselmo ME. Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 315: 1719-1722, 2007. (Pubitemid 46515627)
19. Hafting T, Fyhn M, Bonnevie T, Moser MB, Moser EI. Hippocampus- independent phase precession in entorhinal grid cells. Nature 453: 1248-1252, 2008.
20. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. Microstructure of a spatial map in the entorhinal cortex. Nature 436: 801-806, 2005.
21. Hargreaves EL, Rao G, Lee I, Knierim JJ. Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308: 1792-1794, 2005.
22. Harris KD, Henze DA, Hirase H, Leinekugel X, Dragoi G, Czurko A, Buzsáki G. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417: 738-741, 2002.
23. Hasselmo ME, Giocomo LM, Zilli EA. Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus 17: 1252-1271, 2007.
24. Holmes JE, Adey WR. Electrical activity of the entorhinal cortex during conditioned behavior. Am J Physiol 199: 741-744, 1960.
25. Huxter J, Burgess N, O'Keefe J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425: 828-832, 2003. (Pubitemid 37351465)
26. Insausti R, Herrero MT, Witter MP. Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7: 146-183, 1997.
27. Jung MW, Wiener SI, McNaughton BL. Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J Neurosci 14: 7347-7356, 1994.
28. Kjelstrup KB, Solstad T, Brun VH, Hafting T, Leutgeb S, Witter MP, Moser EI, Moser MB. Finite scale of spatial representation in the hippocampus. Science 321: 140-143, 2008.
29. Knierim JJ. Dynamic interactions between local surface cues, distal landmarks, and intrinsic circuitry in hippocampal place cells. J Neurosci 22: 6254-6264, 2002.
30. Komorowski RW, Manns JR, Eichenbaum H. Robust conjunctive item-place coding by hippocampal neurons parallels learning what happens where. J Neurosci 29: 9918-9929, 2009.
31. Leutgeb JK, Henriksen EJ, Leutgeb S, Witter M, Moser MB, Moser EI. Hippocampal rate coding depends on input from the lateral entorhinal cortex. Program No. 94.6. 2008 Neuroscience Meeting Planner. Washington, DC: Society for Neuroscience, 2008. Online.
32. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser MB. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309: 619-623, 2005.
33. Manns JR, Eichenbaum H. A cognitive map for object memory in the hippocampus. Learn Mem 16: 616-624, 2009.
34. McNaughton BL, Barnes CA, O'Keefe J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 52: 41-49, 1983. (Pubitemid 13019617)
35. Mehta MR, Lee AK, Wilson MA. Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417: 741-746, 2002.
36. Mitchell SJ, Ranck JB Jr. Generation of theta rhythm in medial entorhinal cortex of freely moving rats. Brain Res 189: 49-66, 1980.
37. Moita MA, Rosis S, Zhou Y, LeDoux JE, Blair HT. Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37: 485-497, 2003.
38. Muir GM, Bilkey DK. Synchronous modulation of perirhinal cortex neuronal activity during cholinergically mediated (type II) hippocampal theta. Hippocampus 8: 526-532, 1998.
39. O'Keefe J. Place units in the hippocampus of the freely moving rat. Exp Neurol 51: 78-109, 1976.
40. O'Keefe J, Burgess N. Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus 15: 853-866, 2005.
41. O'Keefe J, Dostrovsky J. The hippocampus as a spatial map: preliminary evidence from unit activity in the freely-moving rat. Brain Res 34: 171-175, 1971.
42. O'Keefe J, Nadel L. The Hippocampus as a Cognitive Map. Oxford, UK: Clarendon Press, 1978.
43. O'Keefe J, Recce ML. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3: 317-330, 1993. (Pubitemid 23231466)
44. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates (4th ed.). San Diego, CA: Academic Press, 1998.
45. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates (6th ed.). Burlington, MA: Elsevier/Academic Press, 2007.
46. Quirk GJ, Muller RU, Kubie JL, Ranck JB Jr. The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J Neurosci 12: 1945-1963, 1992.
47. Ranck JB Jr. Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp Neurol 41: 461-531, 1973.
48. Royer S, Sirota A, Patel J, Buzsáki G. Distinct representations and theta dynamics in dorsal and ventral hippocampus. J Neurosci 30: 1777-1787, 2010.
49. Savelli F, Yoganarasimha D, Knierim JJ. Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18: 1270-1282, 2008.
50. Schmidt R, Diba K, Leibold C, Schmitz D, Buzsáki G, Kempter R. Single-trial phase precession in the hippocampus. J Neurosci 29: 13232-13241, 2009.
51. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6: 149-172, 1996.
52. Stafekhina VS, Karanov AM. Background activity of neurons of the cortical portions of the limbic system of the rabbit brain. Neirofiziologiia 16: 753-760, 1984.
53. Stewart M, Quirk GJ, Barry M, Fox SE. Firing relations of medial entorhinal neurons to the hippocampal theta rhythm in urethane anesthetized and walking rats. Exp Brain Res 90: 21-28, 1992.
54. Tahvildari B, Fransen E, Alonso AA, Hasselmo ME. Switching between "on" and "off" states of persistent activity in lateral entorhinal layer III neurons. Hippocampus 17: 257-263, 2007.
55. Vinogradova OS. Expression, control, and probable functional significance of the neuronal theta-rhythm. Prog Neurobiol 45: 523-583, 1995.
56. Wiener SI, Paul CA, Eichenbaum H. Spatial and behavioral correlates of hippocampal neuronal activity. J Neurosci 9: 2737-2763, 1989.
57. Wilson MA, McNaughton BL. Dynamics of the hippocampal ensemble code for space. Science 261: 1055-1058, 1993.
58. Witter MP, Amaral DG. Hippocampal formation. In: The Rat Nervous System (3rd ed.), edited by Paxinos G. Amsterdam: Elsevier, 2004, p. 635-704.
59. Wood ER, Dudchenko PA, Eichenbaum H. The global record of memory in hippocampal neuronal activity. Nature 397: 613-616, 1999. (Pubitemid 129613566)