What is measured by electroencephalograms and local field potentials?

Question

In the Scholarpedia article on local field potentials (2013), I read:

The current view is that EEG and LFPs are generated by synchronized synaptic currents arising on cortical neurons, possibly through the formation of dipoles (Niedermeyer and Lopes da Silva, 1998; Nunez and Srinivasan, 2005).

There are three things I do not understand:

1. What does "on neurons" mean? Why not "in" or "around neurons"?
2. I assume that what is measured is the electric potential in an electric field that is generated by charges (the ions). So only the changes of the measured potential are due to currents, the potential itself (at any given point in time) is only due to the distribution of charges. Is that view correct? Independent of the nature of the charges.
3. What exactly are the above mentioned dipoles? Of which are they formed and what is their size? (At least, the article says "possibly generated through the formation of dipoles".)

Does all this sum up to the picture that it is all and only about the ions that pass through the ligand-gated channels at a synapse and the electric field and potential generated by them, the contribution of all other charges being cancelled and filtered out?

Answer 1

[I give this as a sketchy answer being aware that it might be nonsense. So feel free to downvote in this case. I should have mentioned - thanks to Bryan for having remembered me - that this answer has been inspired by Buzsáki/Anastassiou/Koch's article on The origin of extracellular fields and currents and just tries to sketch the mental image this article evoked in me.]

I assume that what is actually measured by an EEG electrode is an effective dipole moment in the upper cortical layers underneath the electrode (which decays with $1/r^2$). The way this dipole moment is created by "brain currents" is the matter of this answer.

There seem to be some premises under which a measurable EEG signal (= a dipole) can be detected:

1. The presynaptic action potentials must arrive highly synchronized. (Additive superposition.).

2. The apic dendrites of the pyramidal neurons that give rise to the dipole must be vertically oriented (pointing to the skull, resp. the electrode). (Orientation of the dipole.)

3. The sodium potassium pumps trying to restore the rest potential are unevenly distributed, i.e. mainly located at the soma. (Breaking the symmetry.)

This is the situation for the neuron (gray) at rest:

The dipole then forms as follows in three steps:

Step 1: An presynaptic action potential releases neurotransmitters that open ligand-gated ion channels causing sodium ions to enter the neuron.

Step 2: The extra sodium ions wander quickly to the soma. This happens passively, i.e. driven by repulsion and diffusion. At the end of step 2, all ions inside the neuron are distributed approximately evenly (i.e. not giving rise to an inner dipole).

Step 3: At the soma sodium ions are pumped out of the neuron. During this step equidistribution of ions is maintained inside the neuron (still no dipole inside the neuron).

In the extracellular medium, we now have an observable dipole.

Summary: What is measured by an EEG are not directly "brain currents" but an effective dipole moment that results from three different currents on different time scales:

1. Ions passing the membrane of apic dendrites into the neuron. (Slow.)
2. A net flow of ions wandering from dendrite to soma (driven by repulsion and diffusion). (Fast.)
3. Ions leaving the soma, e.g. by sodium pottasium pumps. (Slow.)

Answer 2

1) Is on neurons because here neurons are considered as population, in this case the cortical neurons.

2) Yes this point of view is correct since the electric potential is generate by charges present outside and inside of the cell. Is the movement of this charge that could generate the electric field.

3)According to wikipedia

An electric dipole is a separation of positive and negative charges. The simplest example of this is a pair of electric charges of equal magnitude but opposite sign, separated by some (usually small) distance

In this case the cortical neurons have some zone where they are positive charges and other zone where they are negatively charged give to them the propriety to be considered as dipole.

The ability to generate a potential by neurons is due by the ions that pass through the channel that could be voltage-gate (open when a specific potential is reach) or ligand-gate (active in presence of a ligand). Depending on the concentration of a specific ions found inside and outside of neurons, this ion can exit or enter the cell if the correct channel is open.

Hope this could help you.

Answer 3

Even though this image is to depict the neuronal origins of the fMRI hemodynamic response, doesn't it also depict quite well the neural origins of the EEG response:

from Scott Huettel, Neuroimaging the Aging Mind, p. 14