Abstract
Brain cortex activity, as variously recorded by scalp or cortical electrodes in the electroencephalography (EEG) frequency range, probably reflects the basic strategy of brain information processing. Various hypotheses have been advanced to interpret this phenomenon, the most popular of which is that suitable combinations of excitatory and inhibitory neurons behave as assemblies of oscillators susceptible to synchronization and desynchronization. Implicit in this view is the assumption that EEG potentials are epiphenomena of action potentials, which is consistent with the argument that voltage variations in dendritic membranes reproduce the postsynaptic effects of targeting neurons. However, this classic argument does not really fit the discovery that firing synchronization over extended brain areas often appears to be established in about 1 ms, which is a small fraction of any EEG frequency component period. This is in contrast with the fact that all computational models of dynamic systems formed by more or less weakly interacting oscillators of near frequencies take more than one period to reach synchronization. The discovery that the somatodendritic membranes of specialized populations of neurons exhibit intrinsic subthreshold oscillations (ISOs) in the EEG frequency range, together with experimental evidence that short inhibitory stimuli are capable of resetting ISO phases, radically changes the scheme described above and paves the way to a novel view. This paper aims to elucidate the nature of ISO generation mechanisms, to explain the reasons for their reliability in starting and stopping synchronized firing, and to indicate their potential in brain information processing. The need for a repertoire of extraneuronal regulation mechanisms, putatively mediated by astrocytes, is also inferred. Lastly, the importance of ISOs for the brain as a parallel recursive machine is briefly discussed.
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Varela, F., Lachaux, J.-P., Rodriguez, E., Martinerie, J.: The brainweb: phase synchronization and large-scale integration. Nat. Rev. Neurosci. 2, 229–239 (2001). doi:10.1038/35067550
König, P., Engel, A.K., Singer, W.: Relation between oscillatory activity and long-range synchronization in cat visual cortex. Proc. Natl. Acad. Sci. U. S. A. 92, 290–294 (1995). doi:10.1073/pnas.92.1.290
Singer, W.: Neural synchrony: a versatile code for the definitions of relations? Neuron 24, 49–65 (1999). doi:10.1016/S0896-6273(00)80821-1
Engel, A.K., Fries, P., Singer, W.: Dynamic predictions: oscillations and synchrony in top-down processing. Nat. Rev. Neurosci. 2, 704–716 (2001). doi:10.1038/35094565
Desmaisons, D., Vincent, J.-D., Lledo, P.-M.: Control of action potential timing by intrinsic subthreshold oscillations in olfactory bulb output neurons. J. Neurosci. 19, 10727–10737 (1999)
Freeman, W., Schneider, W.: Changes in spatial patterns of rabbit olfactory EEG with conditioning to odors. Psychophysiology 19, 44–56 (1982). doi:10.1111/j.1469-8986.1982.tb02598.x
Barrie, M.J., Freeman, W.J., Lenhart, M.D.: Spatiotemporal analysis of prepyriform, visual, auditory, and somesthetic surface EEGs in trained rabbits. J. Neurophysiol. 76, 520–539 (1996)
Key, M.L., Freeman, W.: Bidirectional processing in the olfactory-limbic axis during olfactory behavior. Behav. Neurosci. 112, 541–553 (1998). doi:10.1037/0735-7044.112.3.541
Freeman, W.: Mesoscopic neurodynamics: from neuron to brain. J. Physiol. 94, 303–322 (2000)
Llinás, R.R., Grace, A.A., Yarom, J.: In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. Proc. Natl. Acad. Sci. U. S. A. 88, 879–901 (1991). doi:10.1073/pnas.88.3.897
Gutfreund, Y., Yarom, Y., Segev, I.: Subthreshold oscillations and resonant frequency in guinea-pig cortical neuron: physiology and modeling. J. Physiol. 483, 621–640 (1995)
Richardson, M.J.E., Brunel, N., Hakim, V.: From subthreshold to firing-rate resonance. J. Neurophysiol. 89, 2538–2554 (2003). doi:10.1152/jn.00955.2002
White, J.A., Budde, T., Kay, A.R.: A bifurcation analysis of neuronal subthreshold oscillations. Biophys. J. 69, 1203–1217 (1995). doi:10.1016/S0006-3495(95)79995-7
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 14, 368–384 (2004). doi:10.1002/hipo.10198
Rotstein, H.G., Oppermann, T., White, J.A., Koppell, N.: The dynamic structure underlying subthreshold oscillatory activity and the onset of spikes in a model of medial entorhinal cortex stellate cells. J. Comput. Neurosci. 21, 271–292 (2006). doi:10.1007/s10827-006-8096-8
Mauro, A., Conti, F., Dodge, F., Schor, R.: Subthreshold behavior and phenomenological impedance of the squid giant axon. J. Gen. Physiol. 55, 497–523 (1970). doi:10.1085/jgp.55.4.497
DeFelice, L.J.: Introduction to Membrane Noise. Plenum, New York (1981)
Mittman, T., Linton, S.M., Schwindt, P., Crill, W.: Evidence for persistent Na + current in apical dendrites of rat neocortical neurons from imaging of Na + -sensitive dye. Proc. Natl. Acad. Sci. U. S. A. 94, 724–728 (1997). doi:10.1073/pnas.94.2.724
Magistretti, J., Ragsdale, D.S., Alonso, A.: Direct demonstration of persistent Na + channel activity in dendritic processes of mammalian cortical neurons. J. Physiol. 521, 629–636 (1999). doi:10.1111/j.1469-7793.1999.00629.x
Selyanko, A.A., Brown, D.A.: M-channel gating and simulation. Biophys. J. 77, 701–713 (1999). doi:10.1016/S0006-3495(99)76925-0
Cooper, E.C., Harrington, E., Jan, Y.N., Jan, L.Y.: M channel KCNQ2 subunits are localized to key sites for control of neuronal network oscillations and synchronization in mouse brain. J. Neurosci. 21, 9529–9540 (2001)
Freeman, W.: How Brains Make Up Their Minds. Weidenfeld & Nicolson, London (1999)
Nobili, R., Vetešník, A., Turicchia, L., Mammano, F.: Otoacoustic emissions from residual oscillations of the cochlear basilar membrane in a human ear model. J. Assoc. Res. Otolaryngol. 4, 478–494 (2003). doi:10.1007/s10162-002-3055-1
Vetešník, A., Nobili, R.: The approximate scaling law of the cochlea box model. Hear. Res. 222, 43–53 (2006). doi:10.1016/j.heares.2006.08.012
Carmignoto, G., Fellin, T.: Glutamate release from astrocytes as a non-synaptic mechanism for neuronal synchronization in the hippocampus. J. Physiol. 99, 98–102 (2006)
Turing, A.M.: (1936) On computable numbers, with an application to the Entscheidungsproblem. In: Proceedings of the London Mathematical Society (Ser. 2, 42)
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Nobili, R. New perspectives in brain information processing. J Biol Phys 35, 347–360 (2009). https://doi.org/10.1007/s10867-009-9163-y
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DOI: https://doi.org/10.1007/s10867-009-9163-y