Cytoarchitectonic and Dynamic Origins of Giant Positive Local Field Potentials in the Dentate Gyrus

Abstract

To determine why some pathways but not others produce sizable local field potentials (LFPs) and how far from the source can these be recorded, complementary experimental analyses and realistic modeling of specific brain structures are required. In the present study, we combined multiple in vivo linear recordings in rats and a tridimensional finite element model of the dentate gyrus, a curved structure displaying abnormally large positive LFPs. We demonstrate that the polarized dendritic arbour of granule cells (GCs), combined with the curved layered configuration of the population promote the spatial clustering of GC currents in the interposed hilus and project them through the open side at a distance from cell domains. LFPs grow up to 20 times larger than observed in synaptic sites. The dominant positive polarity of hilar LFPs was only produced by the synchronous activation of GCs in both blades by either somatic inhibition or dendritic excitation. Moreover, the corresponding anatomical pathways must project to both blades of the dentate gyrus as even a mild decrease in the spatial synchronization resulted in a dramatic reduction in LFP power in distant sites, yet not in the GC domains. It is concluded that the activation of layered structures may establish sharply delimited spatial domains where synaptic currents from one or another input appear to be segregated according to the topology of afferent pathways and the cytoarchitectonic features of the target population. These also determine preferred directions for volume conduction in the brain, of relevance for interpretation of surface EEG recordings.

Effect of Ionic Diffusion on Extracellular Potentials in Neural Tissue

“…Furthermore, the LFP is also likely to receive contributions from a large fraction of neurons that are not firing APs, but receiving synaptic input, so that they still participate in generating the low powers of the PSD [33]. In addition, different aspects of the LFP has been found to depend on neuronal morphology, subcellular distributions of membrane mechanisms, and the level of synchrony between neighboring neurons [18, 19, 33, 35, 94–96]. …”

Local Field Potentials: Myths and Misunderstandings

“…Furthermore, the dominant polarity does not reflect the active synaptic currents. For instance, in simple aggregates like the orderly population of hippocampal granule cells, both somatic inhibition and dendritic excitation produce positive FP transients with similar spatial distribution (Fernández-Ruiz et al, 2013), and they are undistinguishable in wide areas. In one case, the dominant positivity is created by the active inhibitory synaptic currents, while in the other it is generated by the passive share of the excitatory current loops (both outward in nature).…”

Mapping dynamical properties of cortical microcircuits using robotized TMS and EEG: Towards functional cytoarchitectonics

“…However, there is only few similar approaches based on electrophysiological recordings, although it has been proved that some of its characteristics are strongly modulated by topological and cytoarchitectural features, including the density of pyramidal cells (Fernández-Ruiz et al, 2013;Kajikawa and Schroeder, 2011;Murakami and Okada, 2006). Several studies using direct cortical electrical stimulation also showed that the properties of the neuronal responses depend a lot on the intrinsic cytoarchitecture or connectivity patterns of the stimulated area, in both animals (Luppino et al, 1991) and humans (Keller et al, 2014).…”