Democracy-independence trade-off in oscillating dendrites and its implications for grid cells

Neuron

Volumn 66, Issue 3, 2010, Pages 429-437

  Remme, Michiel W H ^a   Lengyel, Máté ^b   Gutkin, Boris S ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

SYSNEURO

Indexed keywords

ARTICLE; COMPARTMENT MODEL; CONTROLLED STUDY; DENDRITE; ENTORHINAL CORTEX; MEMBRANE POTENTIAL; OSCILLATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SIMULATION; SOMATIC CELL; STELLATE CELL; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL CLOCKS; DENDRITES; EXPLORATORY BEHAVIOR; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; RATS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 77952715714     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2010.04.027     Document Type: Article

References (51)

1. Alonso A., Klink R. Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J. Neurophysiol. 1993, 70:128-143.
2. Alonso A., Llinás R.R. Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 1989, 342:175-177.
3. Bernander O., Douglas R.J., Martin K.A., Koch C. Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc. Natl. Acad. Sci. USA 1991, 88:11569-11573.
4. Burgess N., Barry C., O'Keefe J. An oscillatory interference model of grid cell firing. Hippocampus 2007, 17:801-812.
5. Carnevale N.T., Johnston D. Electrophysiological characterization of remote chemical synapses. J. Neurophysiol. 1982, 47:606-621.
6. Chapman C.A., Lacaille J.C. Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare. J. Neurophysiol. 1999, 81:1296-1307.
7. DeFelipe J., Fariñas I. The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol. 1992, 39:563-607.
8. Dickson C.T., Magistretti J., Shalinsky M.H., Fransén E., Hasselmo M.E., Alonso A.A. Properties and role of I(h) in the pacing of subthreshold oscillations in entorhinal cortex layer II neurons. J. Neurophysiol. 2000, 83:2562-2579.
9. Fransén E., Alonso A.A., Dickson C.T., Magistretti J., Hasselmo M.E. Ionic mechanisms in the generation of subthreshold oscillations and action potential clustering in entorhinal layer II stellate neurons. Hippocampus 2004, 14:368-384.
10. Fuhs M.C., Touretzky D.S. A spin glass model of path integration in rat medial entorhinal cortex. J. Neurosci. 2006, 26:4266-4276.
11. Fyhn M., Hafting T., Treves A., Moser M.B., Moser E.I. Hippocampal remapping and grid realignment in entorhinal cortex. Nature 2007, 446:190-194.
12. Gasparini S., Migliore M., Magee J.C. On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J. Neurosci. 2004, 24:11046-11056.
13. Giocomo L.M., Zilli E.A., Fransén E., Hasselmo M.E. Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 2007, 315:1719-1722.
14. Goldberg J.A., Deister C.A., Wilson C.J. Response properties and synchronization of rhythmically firing dendritic neurons. J. Neurophysiol. 2007, 97:208-219.
15. Golding N.L., Spruston N. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 1998, 21:1189-1200.
16. Gutfreund Y., yarom Y., Segev I. Subthreshold oscillations and resonant frequency in guinea-pig cortical neurons: physiology and modelling. J. Physiol. 1995, 483:621-640.
17. Hafting T., Fyhn M., Molden S., Moser M.B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
18. Hafting T., Fyhn M., Bonnevie T., Moser M.B., Moser E.I. Hippocampus-independent phase precession in entorhinal grid cells. Nature 2008, 453:1248-1252.
19. Hasselmo M.E. Arc length coding by interference of theta frequency oscillations may underlie context-dependent hippocampal unit data and episodic memory function. Learn. Mem. 2007, 14:782-794.
20. Hasselmo M.E., Giocomo L.M., Zilli E.A. Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus 2007, 17:1252-1271.
21. Häusser M. Synaptic function: dendritic democracy. Curr. Biol. 2001, 11:R10-R12.
22. Hines M.L., Carnevale N.T. The NEURON simulation environment. Neural Comput. 1997, 9:1179-1209.
23. Hopfield J.J. Neural networks and physical systems with emergent collective computational abilities. Proc. Natl. Acad. Sci. USA 1982, 79:2554-2558.
24. Huhn Z., Orbán G., Érdi P., Lengyel M. Theta oscillation-coupled dendritic spiking integrates inputs on a long time scale. Hippocampus 2005, 15:950-962.
25. Izhikevich E. Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting 2007, MIT Press, Cambridge.
26. Klink R., Alonso A.A. Morphological characteristics of layer II projection neurons in the rat medial entorhinal cortex. Hippocampus 1997, 7:571-583.
27. Kropff E., Treves A. The emergence of grid cells: Intelligent design or just adaptation?. Hippocampus 2008, 18:1256-1269.
28. Larkum M.E., Nevian T., Sandler M., Polsky A., Schiller J. Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science 2009, 325:756-760.
29. Lengyel M., Szatmáry Z., Érdi P. Dynamically detuned oscillations account for the coupled rate and temporal code of place cell firing. Hippocampus 2003, 13:700-714.
30. Leung L.W., Yim C.Y. Intrinsic membrane potential oscillations in hippocampal neurons in vitro. Brain Res. 1991, 553:261-274.
31. London M., Segev I. Synaptic scaling in vitro and in vivo. Nat. Neurosci. 2001, 4:853-855.
32. Losonczy A., Magee J.C. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 2006, 50:291-307.
33. McCulloch W.S., Pitts W. A logical calculus of the ideas immanent in nervous activity. Bull. Math. Biophys. 1943, 5:115-133.
34. McNaughton B.L., Battaglia F.P., Jensen O., Moser E.I., Moser M.B. Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 2006, 7:663-678.
35. Nevian T., Larkum M.E., Polsky A., Schiller J. Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study. Nat. Neurosci. 2007, 10:206-214.
36. O'Keefe J., Burgess N. Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus 2005, 15:853-866.
37. Pape H.C., Paré D., Driesang R.B. Two types of intrinsic oscillations in neurons of the lateral and basolateral nuclei of the amygdala. J. Neurophysiol. 1998, 79:205-216.
38. Poirazi P., Brannon T., Mel B.W. Pyramidal neuron as two-layer neural network. Neuron 2003, 37:989-999.
39. Polsky A., Mel B.W., Schiller J. Computational subunits in thin dendrites of pyramidal cells. Nat. Neurosci. 2004, 7:621-627.
40. Rall W., Rinzel J. Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model. Biophys. J. 1973, 13:648-687.
41. Remme M.W.H., Lengyel M., Gutkin B.S. The role of ongoing dendritic oscillations in single-neuron dynamics. PLoS Comput. Biol. 2009, 5:e1000493.
42. Rinzel J., Rall W. Transient response in a dendritic neuron model for current injected at one branch. Biophys. J. 1974, 14:759-790.
43. Rosenblatt F. The perceptron: a probabilistic model for information storage and organization in the brain. Psychol. Rev. 1958, 65:386-408.
44. Rotstein H.G., Oppermann T., White J.A., Kopell N.J. The dynamic structure underlying subthreshold oscillatory activity and the onset of spikes in a model of medial entorhinal cortex stellate cells. J. Comput. Neurosci. 2006, 21:271-292.
45. Rudolph M., Destexhe A. A fast-conducting, stochastic integrative mode for neocortical neurons in vivo. J. Neurosci. 2003, 23:2466-2476.
46. Rumelhart D.E., McClelland J.L. Parallel Distributed Processing: Explorations in the Microstructure of Cognition 1986, MIT Press, Cambridge.
47. Sanhueza M., Bacigalupo J. Intrinsic subthreshold oscillations of the membrane potential in pyramidal neurons of the olfactory amygdala. Eur. J. Neurosci. 2005, 22:1618-1626.
48. Sargolini F., Fyhn M., Hafting T., McNaughton B.L., Witter M.P., Moser M.B., Moser E.I. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 2006, 312:758-762.
49. Stuart G., Spruston N., Häusser M. Dendrites 2007, Oxford University Press, New York.
50. Wei D.S., Mei Y.A., Bagal A., Kao J.P., Thompson S.M., Tang C.M. Compartmentalized and binary behavior of terminal dendrites in hippocampal pyramidal neurons. Science 2001, 293:2272-2275.
51. White J.A., Budde T., Kay A.R. A bifurcation analysis of neuronal subthreshold oscillations. Biophys. J. 1995, 69:1203-1217.