Astroglial Isopotentiality and Calcium-Associated Biomagnetic Field Effects on Cortical Neuronal Coupling

Abstract

Synaptic neurotransmission is necessary but does not sufficiently explain superior cognitive faculties. Growing evidence has shown that neuron-astroglial chemical crosstalk plays a critical role in the processing of information, computation, and memory. In addition to chemical and electrical communication among neurons and between neurons and astrocytes, other nonsynaptic mechanisms called ephaptic interactions can contribute to the neuronal synchronization from different brain regions involved in the processing of information. New research on brain astrocytes has clearly shown that the membrane potential of these cells remains very stable among neighboring and distant astrocytes due to the marked bioelectric coupling between them through gap junctions. This finding raises the possibility that the neocortical astroglial network exerts a guiding template modulating the excitability and synchronization of trillions of neurons by astroglial Ca²⁺-associated bioelectromagnetic interactions. We propose that bioelectric and biomagnetic fields of the astroglial network equalize extracellular local field potentials (LFPs) and associated local magnetic field potentials (LMFPs) in the cortical layers of the brain areas involved in the processing of information, contributing to the adequate and coherent integration of external and internal signals. This article reviews the current knowledge of ephaptic interactions in the cerebral cortex and proposes that the isopotentiality of cortical astrocytes is a prerequisite for the maintenance of the bioelectromagnetic crosstalk between neurons and astrocytes in the neocortex.

Keywords: astrocyte; calcium; connexin; coupling; electric field; ephaptic; isopotentiality; magnetic field.

Figure 1

Three-dimensional (3D) organization of the human neocortex. Scanning imaging of the human brain (A). Histological section of the human cerebral cortex organized in layers (B). Astroglial matrix (hexagonal network) surrounding neuronal minicolumns and layers (C).

Figure 2

Histological section of the human neocortex (layers 2–3) parallel to the pial surface (scale bar, 50 μm). Astrocytes (red arrow) were immunolabeled with GFAP (glial fibrillary acidic protein). Body neurons (black arrow) were not labeled. Astroglial matrix is a sponge-like 3D-structure where neurons of the cortex are imbibed.

Figure 3

Schematic representation of the bioelectromagnetic field distribution in the neocortex and gliocortex. Schematic representation of a pyramidal neuron of the cerebral cortex (a). Bioelectric (E) and biomagnetic (B₀) fields generated following the dendritic–axonal direction (b and c, respectively). Cylinders represent neuronal minicolumns, and hexagons represent the astroglial matrix (d–g). Bioelectromagnetic fields associated with neuronal activities in minicolumns (d), which modulate local field potentials (LFPs) (e). Ca²⁺-associated bioelectromagnetic fields can modulate LMFPs (f). Neuron–astroglial biomagnetic crosstalk (g).

Figure 4

Schematic representation of neurons (N) and astrocytes (A) in layer 2–3 of the human neocortex. Astrocytes are stellated white cells connected by gap junctions. The astroglial matrix surrounds neuronal axons and dendrites. The interstitial space is near virtual (20 to 62 nm width) in physiological conditions. The addition of synaptic currents, action potential currents, and astroglial ionic currents generate local field potential (LFP) in the intercellular space with their corresponding local magnetic field potential (LMFP). Ca²⁺ waves generate current gradients into the astroglial network with their inherent bioelectric and biomagnetic fields that modulate adjacent neuronal behavior by influencing the LFPs and LMFPs.