Inhibition determines membrane potential dynamics and controls action potential generation in awake and sleeping cat cortex

Journal of Neuroscience

Volumn 27, Issue 20, 2007, Pages 5280-5290

  Rudolph, Michelle ^a   Pospischil, Martin ^a   Timofeev, Igor ^b   Destexhe, Alain ^a  

^a CNRS   (France)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Cerebral cortex; Computational models; Conductance analysis; GABAergic conductances; Intracellular recordings; Spike triggered average

Indexed keywords

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CAT; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE POTENTIAL; HYPERPOLARIZATION; MATHEMATICAL MODEL; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; SLEEP WAKING CYCLE; SPIKE WAVE; SYNAPTIC TRANSMISSION; WAKEFULNESS;

ACTION POTENTIALS; ANIMALS; CATS; CEREBRAL CORTEX; MEMBRANE POTENTIALS; NEURAL INHIBITION; SLEEP; WAKEFULNESS;

EID: 34249044194     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4652-06.2007     Document Type: Article

References (36)

1. Anderson JS, Carandini M, Ferster D (2000) Orientation tuning of input conductance, excitation and inhibition in cat primary visual cortex. J Neurophysiol 84:909-926.
2. Baranyi A, Szente MB, Woody CD (1993) Electrophysiological characterization of different types of neurons recorded in vivo in the motor cortex of the cat. II. Membrane parameters, action potentials, current-induced voltage responses and electrotonic structures. J Neurophysiol 69:1865-1879.
3. Borg-Graham LJ, Monier C, Frégnac Y (1998) Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393:369-373.
4. Brecht M, Schneider M, Sakmann B, Margrie TW (2004) Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427:704-710.
5. Destexhe A, Paré D (1999) Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol 81:1531-1547.
6. Destexhe A, Rudolph M, Fellous JM, Sejnowski TJ (2001) Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons. Neuroscience 107:13-24.
7. Destexhe A, Rudolph M, Paré D (2003) The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4:739-751.
8. Destexhe A, Timofeev I, Rudolph M (2005) Combining stochastic models with intracellular recordings reveals dominant inhibitory conductances in cortical neurons of awake and naturally-sleeping animals. Paper presented at COSYNE Conference, Salt Lake City, March.
9. Haider B, Duque A, Hasenstaub AR, McCormick DA (2006) Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci 26:4535-4545.
10. Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, McCormick DA (2005) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47:423-435.
11. Hines ML, Carnevale NT (1997) The Neuron simulation environment. Neural Comput 9:1179-1209.
12. Hirsch JA, Alonso JM, Clay Reid R, Martinez LM (1998) Synaptic integration in striate cortical simple cells. J Neurosci 18: 9517-9528.
13. Kuhn A, Aertsen A, Rotter S (2004) Neuronal integration of synaptic input in the fluctuation-driven regime. J Neurosci 24:2345-2356.
14. Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science 268:1503-1506.
15. Matsumura M, Cope T, Fetz EE (1988) Sustained excitatory synaptic input to motor cortex neurons in awake animals revealed by intracellular recording of membrane potentials. Exp Brain Res 70:463-469.
16. McCormick DA (1992) Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuro-modulation of thalamocortical activity. Prog Neurobiol 39:337-388.
17. Metherate R, Ashe JH (1993) Ionic flux contributions to neocortical slow waves and nucleus basalis-mediated activation: whole-cell recordings in vivo. J Neurosci 13:5312-5323.
18. Monier C, Chavane F, Baudot P, Graham LJ, Frégnac Y (2003) Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron 37:663-680.
19. Paré D, Shink E, Gaudreau H, Destexhe A, Lang EJ (1998) Impact of spontaneous synaptic activity on the resting properties of cat neocortical neurons in vivo. J Neurophysiol 79:1450-1460.
20. Pospischil M, Rudolph M, Shulz D, Timofeev I, Destexhe A (2005) Are we inhibited when we are awake? A combined intracellular and computational analysis of membrane potential dynamics in cortical neurons of awake and naturally sleeping animals. Soc Neurosci Abstr 31: 276.15.
21. Pospischil M, Piwkowska Z, Rudolph M, Bal T, Destexhe A (2007) Calculating event-triggered average synaptic conductances from the membrane potential. J Neurophysiol 97:2544-2552.
22. Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1986) Numerical recipes. The art of scientific computing. Cambridge, MA: Cambridge UP.
23. Priebe NJ, Ferster D (2005) Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex. Neuron 45:133-145.
24. Rudolph M, Destexhe A (2003) Characterization of subthreshold voltage fluctuations in neuronal membranes. Neural Comput 15:2577-2618.
25. Rudolph M, Destexhe A (2005) An extended analytic expression for the membrane potential distribution of conductance-based synaptic noise. Neural Comput 17:2301-2315.
26. Rudolph M, Destexhe A (2006) Multichannel shot noise approach to describe synaptic background activity in neurons. Eur Phys J B 52:125-132.
27. Rudolph M, Piwkowska Z, Badoual M, Bal T, Destexhe A (2004) A method to estimate synaptic conductances from membrane potential fluctuations. J Neurophysiol 91: 2884-2896.
28. Rudolph M, Pelletier JG, Paré D, Destexhe A (2005) Characterization of synaptic conductances and integrative properties during electrically-induced EEG-activated states in neocortical neurons in vivo. J Neurophysiol 94: 2805-2821.
29. Shu Y, Hasenstaub A, McCormick DA (2003) Turning on and off recurrent balanced cortical activity. Nature 423:288-293.
30. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85:1969-1985.
31. Stuart G, Spruston N, Sakmann B, Hausser M (1997) Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci 20:125-131.
32. Timofeev I, Grenier F, Steriade M (2001) Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. Proc Natl Acad Sci USA 98:1924-1929.
33. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442-446.
34. Xiang Z, Huguenard JR, Prince DA (1998) Cholinergic switching within neocortical inhibitory networks. Science 281:985-988.
35. Waters J, Helmchen F (2006) Background synaptic activity is sparse in neocortex. J Neurosci 26:8267-8277.
36. Zou Q, Rudolph M, Roy N, Sanchez-Vives M, Contreras D, Destexhe A (2005) Reconstructing synaptic background activity from conductance measurements in vivo. Neurocomputing 65:673-678.