Comparison of Properties of Medial Entorhinal Cortex Layer II Neurons in Two Anatomical Dimensions with and without Cholinergic Activation

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Yoshida, Motoharu ^a,b   Jochems, Arthur ^a   Hasselmo, Michael E ^b  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBACHOL; CHOLINERGIC RECEPTOR;

ANIMAL CELL; ARTICLE; CHOLINERGIC STIMULATION; CONTROLLED STUDY; ENTORHINAL CORTEX; EVOKED RESPONSE; FUNCTIONAL ANATOMY; HYPERPOLARIZATION; IN VITRO STUDY; INTRACELLULAR RECORDING; MEMBRANE POTENTIAL; NERVE CONDUCTION; NEUROANATOMY; NONHUMAN; OSCILLATION; PATCH CLAMP; RAT; SPIKE WAVE;

ACTION POTENTIALS; ANIMALS; CHOLINERGIC NEURONS; ENTORHINAL CORTEX; FEMALE; MALE; MEMBRANE POTENTIALS; NEURONS; RATS;

EID: 84884185077     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073904     Document Type: Article

References (40)

1. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI, (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436: 801-806.
2. Burgess N, Barry C, O'Keefe J, (2007) An oscillatory interference model of grid cell firing. Hippocampus 17: 801-812.
3. Hasselmo ME, Giocomo LM, Zilli EA, (2007) Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus 17: 1252-1271.
4. Fuhs MC, Touretzky DS, (2006) A spin glass model of path integration in rat medial entorhinal cortex. Journal of Neuroscience 26: 4266-4276.
5. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB, (2006) Path integration and the neural basis of the 'cognitive map'. Nature Reviews Neuroscience 7: 663-678.
6. 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.
7. Canto CB, Witter MP, (2012) Cellular properties of principal neurons in the rat entorhinal cortex. I. The lateral entorhinal cortex. Hippocampus 22: 1256-1276.
8. 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.
9. Garden DLF, Dodson PD, O'Donnell C, White MD, Nolan MF, (2008) Tuning of Synaptic Integration in the Medial Entorhinal Cortex to the Organization of Grid Cell Firing Fields. Neuron 60: 875-889.
10. Kropff E, Treves A, (2008) The Emergence of Grid Cells: Intelligent Design or Just Adaptation? Hippocampus 18: 1256-1269.
11. Hasselmo ME, (2008) Grid Cell Mechanisms and Function: Contributions of Entorhinal Persistent Spiking and Phase Resetting. Hippocampus 18: 1213-1229.
12. Giocomo LM, Hasselmo ME, (2008) Time constants of h current in layer II stellate cells differ along the dorsal to ventral axis of medial Entorhinal cortex. Journal of Neuroscience 28: 9414-9425.
13. Boehlen A, Heinemann U, Erchova I, (2010) The Range of Intrinsic Frequencies Represented by Medial Entorhinal Cortex Stellate Cells Extends with Age. Journal of Neuroscience 30: 4585-4589.
14. Giocomo LM, Hussaini SA, Zheng F, Kandel ER, Moser MB, et al. (2011) Grid Cells Use HCN1 Channels for Spatial Scaling. Cell 147: 1159-1170.
15. Schmidt-Hieber C, Hausser M, (2013) Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nature Neuroscience 16: 325-331.
16. Hasselmo ME, Brandon MP (2012) A model combining oscillations and attractor dynamics for generation of grid cell firing. Frontiers in Neural Circuits 6.
17. Couey JJ, Witoelar A, Zhang SJ, Zheng K, Ye J, et al. (2013) Recurrent inhibitory circuitry as a mechanism for grid formation. Nature Neuroscience 16: 318-324.
18. Dhillon A, Jones RSG, (2000) Laminar differences in recurrent excitatory transmission in the rat entorhinal cortex in vitro. Neuroscience 99: 413-422.
19. Pastoll H, Ramsden HL, Nolan MF (2012) Intrinsic electrophysiological properties of entorhinal cortex stellate cells and their contribution to grid cell firing fields. Frontiers in Neural Circuits 6.
20. Brandon MP, Bogaard AR, Libby CP, Connerney MA, Gupta K, et al. (2011) Reduction of Theta Rhythm Dissociates Grid Cell Spatial Periodicity from Directional Tuning. Science 332: 595-599.
21. 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.
22. Hamlin AS, Windels F, Boskovic Z, Sah P, Coulson EJ (2013) Lesions of the Basal Forebrain Cholinergic System in Mice Disrupt Idiothetic Navigation. Plos One 8.
23. Heys JG, Giocomo LM, Hasselmo ME, (2010) Cholinergic Modulation of the Resonance Properties of Stellate Cells in Layer II of Medial Entorhinal Cortex. Journal of Neurophysiology 104: 258-270.
24. Storm JF, (1987) Action-Potential Repolarization and A Fast After-Hyperpolarization in Rat Hippocampal Pyramidal Cells. Journal of Physiology-London 385: 733-759.
25. Storm JF, (1989) An After-Hyperpolarization of Medium Duration in Rat Hippocampal Pyramidal Cells. Journal of Physiology-London 409: 171-190.
26. 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. Journal of Neuroscience 31: 12683-12694.
27. Zhang L, Weiner JL, Valiante TA, Velumian AA, Watson PL, et al. (1994) Whole-Cell Recording of the Ca2+-Dependent Slow Afterhyperpolarization in Hippocampal-Neurons- Effects of Internally Applied Anions. Pflugers Archiv-European Journal of Physiology 426: 247-253.
28. Klink R, Alonso A, (1997) Morphological characteristics of layer II projection neurons in the rat medial entorhinal cortex. Hippocampus 7: 571-583.
29. Klink R, Alonso A, (1997) Muscarinic modulation of the oscillatory and repetitive firing properties of entorhinal cortex layer II neurons. Journal of Neurophysiology 77: 1813-1828.
30. Madison DV, Nicoll RA, (1984) Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J Physiol 354: 319-331.
31. Barkai E, Hasselmo ME, (1994) Modulation of the Input/Output Function of Rat Piriform Cortex Pyramidal Cells. Journal of Neurophysiology 72: 644-658.
32. Gu N, Vervaeke K, Hu H, Storm JF, (2005) Kv7/KCNQ/M and HCN/h, but not K(Ca)2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. Journal of Physiology-London 566: 689-715.
33. Khawaja FA, Alonso AA, Bourque CW, (2007) Ca2+-dependent K+ currents and spike-frequency adaptation in medial entorhinal cortex layer II stellate cells. Hippocampus 17: 1143-1148.
34. Gu N, Hu H, Vervaeke K, Storm JF, (2008) SK (KCa2) channels do not control somatic excitability in CA1 pyramidal neurons but can be activated by dendritic excitatory synapses and regulate their impact. J Neurophysiol 100: 2589-2604.
35. 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.
36. Dodson PD, Pastoll H, Nolan MF, (2011) Dorsal-ventral organization of theta-like activity intrinsic to entorhinal stellate neurons is mediated by differences in stochastic current fluctuations. Journal of Physiology-London 589: 2993-3008.
37. Canto CB, Witter MP, (2012) Cellular properties of principal neurons in the rat entorhinal cortex. II. The medial entorhinal cortex. Hippocampus 22: 1277-1299.
38. Magistretti J, Ma L, Shalinsky MH, Lin W, Klink R, et al. (2004) Spike patterning by Ca2+-dependent regulation of a muscarinic cation current in entorhinal cortex layer II neurons. Journal of Neurophysiology 92: 1644-1657.
39. Giocomo LM, Hasselmo ME, (2009) Knock-Out of HCN1 Subunit Flattens Dorsal-Ventral Frequency Gradient of Medial Entorhinal Neurons in Adult Mice. Journal of Neuroscience 29: 7625-7630.
40. Burak Y, Fiete IR (2009) Accurate Path Integration in Continuous Attractor Network Models of Grid Cells. Plos Computational Biology 5.