ReviewEphaptic Coupling of Cortical Neurons: Possible Contribution of Astroglial Magnetic Fields?
Graphical abstract
Introduction
In addition to chemical and electrical neurotransmission, other non-synaptic mechanisms such as extracellular ionic waves and changes in osmolarity have been considered critical for coupling and synchronization of neurons into the neocortex both, in physiological and pathological conditions (Rosen and Andrew, 1990, Syková, 2004, Durand et al., 2010). These other ways of neuronal modulation are known as ephaptic interaction (Katz and Schmitt, 1940, Arvanitaki, 1942), and, recently it has been recognized that this type of communication may play a central role in cognitive functions (Buzsáki et al., 2012, Reimann et al., 2013). On the other hand, ephaptic effects may help to explain, at least partially, the therapeutic actions of transcranial electric and magnetic field stimulation (Peterchev et al., 2012). The ephaptic effect in the neocortex is thought to be due to the summation of all sources that contribute to the extracellular field potential. This extracellular potential in a point of the neocortex results from the addition of synaptic currents, action potential currents as well as astroglial ionic currents around this point (Jefferys and Haas, 1982, Jefferys, 1995, Ray, 2015), and it is called the local field potential (LFP). Classically, the effects of the action potentials and astroglial ionic currents have been considered negligible in comparison to the contribution of synaptic currents (Creutzfeldt and Houchin, 1974, Mitzdorf, 1985). Therefore, the contribution of astroglial bio-electric and bio-magnetic fields to the LFPs into the neocortex has been scarcely studied. In the present paper, I conjecture that bio-electro-magnetic fields generated inside the astroglial syncytium around neurons may contribute to the so-called ephaptic effects in the neocortex, playing a role in the modulation and synchronization of neuronal behavior.
Section snippets
Architectural considerations of the mammalian neocortex
The recognition of the huge number and wide diversity of cell types, complex 3D organization, functional architecture and connectivity in the mammalian cerebral cortex, begun with the Cajal’s studies (Ramón y Cajal, 1897) and continue today with the Blue Brain Project (Markram et al., 2015). From a schematic point of view, the mammalian neocortex is composed of neuronal and glial cells organized fundamentally in two closely related 3D structures (Fig. 1). The neurocortex is organized in
Neuron-astroglial interplay: electrophysiological and ionic considerations
The close anatomical and functional relationship between neuronal circuits and the astroglial network in the neocortex has been demonstrated at several organization levels. For instance, many experiments have shown an exquisite electrophysiological interplay between neurons and astrocytes in the mammalian neocortex supporting the notion that neuron-astroglial crosstalk could play a central role in information processing (Amzica and Steriade, 2000, Araque et al., 2001, Araque et al., 2014,
Bio-electro-magnetic fields in the neocortex
Correlation between electroencephalography (EEG) and magnetoencephalography (MEG) is very high (Cuffin and Cohen, 1979), but MEG records rhythmic and coherent magnetic fields generated mainly in cortical pyramidal cells (Gallen et al., 1995). The recorded fields are the result of the coordinated firing of many thousands of these cells, mostly located in layers III and IV of the neocortex (Nunez, 1986, Hamalainen et al., 1993). The magnetic fields, recorded above the surface of the scalp, are in
Ephaptic neuronal coupling: astroglial magnetic field effects?
It is a fact, that neuronal behavior is affected by adjacent neuronal activities in the cerebral cortex via ephaptic interaction. Experiments in goldfish showed an ephaptic inhibitory action on the Mauthner cells (Furukawa and Furshpan, 1963), and electrical interactions have been demonstrated to excite many interneurons playing important roles in neuronal circuits (Faber and Korn, 1983, Hu et al., 2000, Weiss et al., 2008). In addition, it has been suggested that cells could communicate by
Ephaptic effects in transcranial field stimulation
Transcranial electric and magnetic field stimulation of the brain have shown a wide variety of therapeutic and cognitive effects, using different techniques, stimulus waveforms, and designs (Weiss and Faber, 2010, Peterchev et al., 2012). In the case of transcranial magnetic stimulation, a magnetic field is generated that induces an electric field and its corresponding current density field in the brain (Peterchev et al., 2012). However, the specific mechanisms that mediate their clinical and
Conclusion
In recent years, an increasing role of astrocytes in the mammalian neocortical structure and function has been demonstrated. In addition to the structural, metabolic and ionic homeostatic support to neurons, astroglia plays a central role in neuromodulation and computation, including fundamental roles in superior cognitive function in the mammalian neocortex. The contribution of the astroglial network to the synaptic communication and remodeling is now well recognized, but a widespread role of
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