Theoretical considerations and supporting evidence for the primary role of source geometry on field potential amplitude and spatial extent

Abstract

Field potential (FP) recording is an accessible means to capture the shifts in the activity of neuron populations. However, the spatial and composite nature of these signals has largely been ignored, at least until it became technically possible to separate activities from co-activated sources in different structures or those that overlap in a volume. The pathway-specificity of mesoscopic sources has provided an anatomical reference that facilitates transcending from theoretical analysis to the exploration of real brain structures. We review computational and experimental findings that indicate how prioritizing the spatial geometry and density of sources, as opposed to the distance to the recording site, better defines the amplitudes and spatial reach of FPs. The role of geometry is enhanced by considering that zones of the active populations that act as sources or sinks of current may arrange differently with respect to each other, and have different geometry and densities. Thus, observations that seem counterintuitive in the scheme of distance-based logic alone can now be explained. For example, geometric factors explain why some structures produce FPs and others do not, why different FP motifs generated in the same structure extend far while others remain local, why factors like the size of an active population or the strong synchronicity of its neurons may fail to affect FPs, or why the rate of FP decay varies in different directions. These considerations are exemplified in large structures like the cortex and hippocampus, in which the role of geometrical elements and regional activation in shaping well-known FP oscillations generally go unnoticed. Discovering the geometry of the sources in play will decrease the risk of population or pathway misassignments based solely on the FP amplitude or temporal pattern.

Uncorrelated bilateral cortical input becomes timed across hippocampal subfields for long waves whereas gamma waves are largely ipsilateral

“…Actually, they belong to the few connections that contribute significantly to FPs. In former studies we showed that most pathways do not contribute to FPs, either due to the inadequate spatial geometry of microscopic currents ( Herreras et al, 2023 ) or because the low level of activity does not accumulate enough variance to be discriminated by the ICA ( Herreras et al, 2015 ). However, in these loose pieces of the map, we have several that are key and allow us to glimpse the overall flow of activity and some of its bilateral characteristics.…”

“…Methods to increase the temporal precision of separation have been advanced, but they may not achieve sufficient precision in some epochs ( Benito et al, 2014 , 2016 ). Without optimization measures, accurate extraction of gamma waves in strongly overlapping DG generators (e.g., Fernández-Ruiz et al, 2021 ) is highly susceptible to error, while being more reliable when applied to CA1 gamma sources (see Herreras et al, 2023 for a repertoire of gamma-related phenomena). In this study, we have opted for cautious use of correlation or spectral coherence tests, which are suitable for studying global flow and coherence between paired generators of bilateral circuits.…”

“…Unlike the poor performance of ICA algorithms on surface EEG recordings, their optimal performance on intracranial multisite FPs derives from the fact that different synaptic pathways raise distinct voltage gradients in space, which can be captured by high-density recording arrays placed in or near the source populations ( Figure 1C ). Such pathway-specific voltage gradients fade and equalize in the distance, and cannot be discriminated by remote recordings ( Herreras et al, 2023 ).…”

“…These two spatial and temporal features reflected, respectively, the stratified input of various synaptic pathways to major populations of pyramidal or GCs, and the wide variety of dynamics. According to previous research (Herreras et al, 2022(Herreras et al, , 2023, such variety of waveforms derived in part from the spatiotemporal mixtures of potentials contributed by various co-active sources that contaminate each other and distort the original time courses. Temporal distortion arose either from the overlapping of the spatial domains hosting different FP waves/motifs (Figure 1C, purple ovals) or due to their contamination by others generated at remote sites (waves outlined in brown).…”

“…While the links were not completely symmetrical, there were no significant differences between directions across subjects. CA1 gamma sources (see Herreras et al, 2023 for a repertoire of gamma-related phenomena). In this study, we have opted for cautious use of correlation or spectral coherence tests, which are suitable for studying global flow and coherence between paired generators of bilateral circuits.…”