Artificial synaptic conductances reduce subthreshold oscillations and periodic firing in stellate cells of the entorhinal cortex

Journal of Neuroscience

Volumn 28, Issue 14, 2008, Pages 3790-3803

  Fernandez, Fernando R ^a,b   White, John A ^a,b  

^a Boston University   (United States)

^b Department of Electrical and Computer Engineering   (United States)

Author keywords

AHP; Dynamic clamp; Medial entorhinal cortex; Membrane conductance; Oscillations; Theta

Indexed keywords

AFTERHYPERPOLARIZATION; ANIMAL TISSUE; ARTICLE; CONDUCTANCE; CONTROLLED STUDY; ENTORHINAL CORTEX; MEMBRANE CURRENT; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RAT; SPIKE; STELLATE CELL; SYNAPTIC TRANSMISSION; ACTION POTENTIAL; ANALYSIS OF VARIANCE; ANIMAL; ARTIFACT; BIOLOGICAL MODEL; CYTOLOGY; ELECTRIC CONDUCTIVITY; ELECTROSTIMULATION; IN VITRO STUDY; LONG EVANS RAT; METHODOLOGY; NERVE CELL; NERVE CELL INHIBITION; NEWBORN; NONLINEAR SYSTEM; PATCH CLAMP; PERIODICITY; PHYSIOLOGY; RADIATION EXPOSURE; SYNAPSE;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ARTIFACTS; ELECTRIC CONDUCTIVITY; ELECTRIC STIMULATION; ENTORHINAL CORTEX; MODELS, NEUROLOGICAL; NEURAL INHIBITION; NEURONS; NONLINEAR DYNAMICS; PATCH-CLAMP TECHNIQUES; PERIODICITY; RATS; RATS, LONG-EVANS; SYNAPSES;

EID: 43649101300     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5658-07.2008     Document Type: Article

References (47)

1. Alonso A, Garcia-Austt E (1987a) 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.
2. Alonso A, Garcia-Austt E (1987b) 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.
3. Alonso A, Klink R (1993) Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J Neurophysiol 70:128-143.
4. +-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342:175-177.
5. Anderson JS, Lampl I, Gillespie DC, Ferster D (2000) The contribution of noise to contrast invariance of orientation tuning in cat visual cortex. Science 290:1968-1972.
6. Bair W, Koch C, Newsome W, Britten K (1994) Power spectrum analysis of bursting cells in area MT in the behaving monkey. J Neurosci 14:2870-2892.
7. Barbi M, Chillemi S, Di Garbo A (2000) The leaky integrate-and-fire with noise: a useful tool to investigate SR. Chaos Solitons Fractals 11:1849-1853.
8. Berg RW, Alaburda A, Hounsgaard J (2007) Balanced inhibition and excitation drive spike activity in spinal half-centers. Science 315:390-393.
9. Bernander O, Douglas RJ, Martin KA, Koch C (1991) Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc Natl Acad Sci USA 88:11569-11573.
10. Berretta N, Jones RS (1996) A comparison of spontaneous EPSCs in layer II and layer IV-V neurons of the rat entorhinal cortex in vitro. J Neurophysiol 76:1089-1100.
11. Borg-Graham LJ, Monier C, Fregnac Y (1998) Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393:369-373.
12. Burgess N, Barry C, O'Keefe J (2007) An oscillatory interference model of grid cell firing. Hippocampus 17:801-812.
13. Chance FS, Abbott LF, Reyes AD (2002) Gain modulation from background synaptic input. Neuron 35:773-782.
14. Destexhe A, Pare D (1999) Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol 81:1531-1547.
15. Destexhe A, Rudolph M, Fellous JM, Sejnowski TJ (2001) Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons. Neuroscience 107:13-24.
16. Destexhe A, Rudolph M, Pare D (2003) The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4:739-751.
17. Dickson CT, Kirk IJ, Oddie SD, Bland BH (1995) Classification of theta-related cells in the entorhinal cortex: cell discharges are controlled by the ascending brainstem synchronizing pathway in parallel with hippocampal theta-related cells. Hippocampus 5:306-319.
18. Dorval Jr AD, White JA (2005) Channel noise is essential for perithreshold oscillations in entorhinal stellate neurons. J Neurosci 25:10025-10028.
19. Dorval AD, Christini DJ, White JA (2001) Real-time linux dynamic clamp: a fast and flexible way to construct virtual ion channels in living cells. Ann Biomed Eng 29:897-907.
20. 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 (Lond) 560:89-110.
21. Frank LM, Brown EN, Wilson MA (2001) A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. J Neurophysiol 86:2029-2040.
22. Fransen E, Alonso AA, Dickson CT, Magistretti J, Hasselmo ME (2004) Ionic mechanisms in the generation of subthreshold oscillations and action potential clustering in entorhinal layer II stellate neurons. Hippocampus 14:368-384.
23. 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.
24. Gloor P (1997) The temporal lobe and limbic system. New York: Oxford UP.
25. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801-806.
26. Harsch A, Robinson HP (2000) Postsynaptic variability of firing in rat cortical neurons: the roles of input synchronization and synaptic NMDA receptor conductance. J Neurosci 20:6181-6192.
27. Hutcheon B, Miura RM, Puil E (1996) Models of subthreshold membrane resonance in neocortical neurons. J Neurophysiol 76:698-714.
28. Jones RS (1994) Synaptic and intrinsic properties of neurons of origin of the perforant path in layer II of the rat entorhinal cortex in vitro. Hippocampus 4:335-353.
29. Jones RS, Woodhall GL (2005) Background synaptic activity in rat entorhinal cortical neurones: differential control of transmitter release by presynaptic receptors. J Physiol (Lond) 562:107-120.
30. + currents and spike-frequency adaptation in medial entorhinal cortex layer II stellate cells. Hippocampus 17:1143-1148.
31. Klink R, Alonso A (1993) Ionic mechanisms for the subthreshold oscillations and differential electroresponsiveness of medial entorhinal cortex layer II neurons. J Neurophysiol 70:144-157.
32. Klink R, Alonso A (1997) Morphological characteristics of layer II projection neurons in the rat medial entorhinal cortex. Hippocampus 7:571-583.
33. Koch C (1999) Biophysics of computation: information processing in single neurons. New York: Oxford UP.
34. Kohler C (1986) Intrinsic connections of the retrohippocampal region in the rat brain. II. The medial entorhinal area. J Comp Neurol 246:149-169.
35. Longtin A (2000) Effect of noise on the tuning properties of excitable systems. Chaos Solitons Fractals 11:1835-1848.
36. Miller KD, Troyer TW (2002) Neural noise can explain expansive, powerlaw nonlinearities in neural response functions. J Neurophysiol 87:653-659.
37. Mitchell SJ, Ranck Jr JB (1980) Generation of theta rhythm in medial entorhinal cortex of freely moving rats. Brain Res 189:49-66.
38. Netoff TI, Banks MI, Dorval AD, Acker CD, Haas JS, Kopell N, White JA (2005) Synchronization in hybrid neuronal networks of the hippocampal formation. J Neurophysiol 93:1197-1208.
39. Nolan MF, Dudman JT, Dodson PD, Santoro B (2007) HCN1 channels control resting and active integrative properties of stellate cells from layer II of the entorhinal cortex. J Neurosci 27:12440-12451.
40. 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.
41. Pare D, Shink E, Gaudreau H, Destexhe A, Lang EJ (1998) Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons In vivo. J Neurophysiol 79:1450-1460.
42. Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18:3870-3896.
43. Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13:334-350.
44. Swanson LW, Kohler C (1986) Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat. J Neurosci 6:3010-3023.
45. van Vreeswijk C, Sompolinsky H (1996) Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science 274:1724-1726.
46. White JA, Klink R, Alonso A, Kay AR (1998) Noise from voltage-gated ion channels may influence neuronal dynamics in the entorhinal cortex. J Neurophysiol 80:262-269.
47. Wolfart J, Debay D, Le Masson G, Destexhe A, Bal T (2005) Synaptic background activity controls spike transfer from thalamus to cortex. Nat Neurosci 8:1760-1767.