A physical neural mass model framework for the analysis of oscillatory generators from laminar electrophysiological recordings
Authors: Sanchez-Todo Roser , Bastos André M. , Sola Edmundo Lopez , Mercadal Borja , Santarnecchi Emiliano , Miller Earl K. , Deco Gustavo , Ruffini Giulio 
Published: July 2022

Cortical function emerges from the interactions of multi-scale networks that may be studied at a high level using neural mass models (NMM), representing the mean activity of large numbers of neurons. In order to properly reproduce experimental data, these models require the addition of further elements. Here we provide a framework integrating conduction physics that can be used to simulate cortical electrophysiology measurements, particularly those obtained from multi-contact laminar electrodes. This is achieved by endowing NMMs with basic physical properties, such as the average laminar location of the apical and basal dendrites of pyramidal cell populations. We call this framework laminar NMM, or LaNMM for short. We then employ this framework to infer the location of oscillatory generators from laminar-resolved data collected from the prefrontal cortex in the macaque monkey. Based on the literature on columnar connectivity, we define a minimal neural mass model capable of generating amplitude and phase coupled slow (alpha/beta, 4–22 Hz) and fast (gamma, 30–250 Hz) oscillations. The synapse layer locations of the two pyramidal cell populations are treated as optimization parameters, together with two more LaNMM-specific parameters, to compare the models with the multi-contact recordings. We rank the candidate models using an optimization function that evaluates the match between the functional connectivity (FC) of the model and data, where the FC is defined by the covariance between bipolar voltage measurements at different cortical depths. The family of best solutions reproduces the FC of the observed electrophysiology while selecting locations of pyramidal cells and their synapses that result in the generation of fast activity at superficial layers and slow activity across most depths, in line with recent literature proposals.

Highlights

We provide a neural mass modeling formalism that includes a physical layer to simulate electrophysiology measurements.

To analyze in-vivo data collected in the macaque monkey during a memory task, we propose a specific model with two coupled main circuits that can generate realistic electrophysiological signals in two important oscillatory regimes—the alpha/beta and the gamma bands.

Physical elements in the model shed light on the generation of oscillations in the two regimes and on the relative power distribution of fast and slow oscillatory signals across cortical depth, which we show can be altered by the choice of the reference location or method.

The model is contrasted with in-vivo data, with parameters adjusted by matching voltage statistics in the alpha/beta and gamma bands, leading to a solution with slow frequency components generated by synapses spanning most cortical layers and fast oscillations in superficial layers.

The resulting formalism provides useful tools and concepts to analyze and model data, with implications for understanding altered oscillatory EEG activity in dementia, Alzheimer’s disease and other disorders with oscillatory features.