Non-zero mean alpha oscillations revealed with computational model and empirical data

Member Authors
Authors
Alina A Studenova, Arno Villringer, Vadim Nikulin
Journal
PLoS Comput Biol.

Abstract

Ongoing oscillations and evoked responses are two main types of neuronal activity obtained with diverse electrophysiological recordings (EEG/MEG/iEEG/LFP). Although typically studied separately, they might in fact be closely related. One possibility to unite them is to demonstrate that neuronal oscillations have non-zero mean which predicts that stimulus- or task-triggered amplitude modulation of oscillations can contribute to the generation of evoked responses. We validated this mechanism using computational modelling and analysis of a large EEG data set. With a biophysical model, we indeed demonstrated that intracellular currents in the neuron are asymmetric and, consequently, the mean of alpha oscillations is non-zero. To understand the effect that neuronal currents exert on oscillatory mean, we varied several biophysical and morphological properties of neurons in the network, such as voltage-gated channel densities, length of dendrites, and intensity of incoming stimuli. For a very large range of model parameters, we observed evidence for non-zero mean of oscillations. Complimentary, we analysed empirical rest EEG recordings of 90 participants (50 young, 40 elderly) and, with spatio-spectral decomposition, detected at least one spatially-filtred oscillatory component of non-zero mean alpha oscillations in 93% of participants. In order to explain a complex relationship between the dynamics of amplitude-envelope and corresponding baseline shifts, we performed additional simulations with simple oscillators coupled with different time delays. We demonstrated that the extent of spatial synchronisation may obscure macroscopic estimation of alpha rhythm modulation while leaving baseline shifts unchanged. Overall, our results predict that amplitude modulation of neural oscillations should at least partially explain the generation of evoked responses. Therefore, inference about changes in evoked responses with respect to cognitive conditions, age or neuropathologies should be constructed while taking into account oscillatory neuronal dynamics.

Published: 2022 Jul

Figure 1

Schematic representation of a pyramidal neuron as it was modelled in Human Neocortical Neurosolver (HNN) [32].

a. Parameters of the model that were subjected to change: strength of incoming inputs via synaptic weights on AMPA and NMDA synaptic receptors, the density of voltage-gated sodium and potassium ion channels, and the length of apical dendrites. b. A schematic illustration of the effect that incoming inputs exert on the dendritic currents. The proximal drive is a simulation of thalamic activity coming to the granular layer of the cortex, which is later relayed to layer II/III and layer V. Distal drive is excitatory input from non-lemniscal thalamic sources and/or other cortical areas. Proximal connections terminate on the basal dendrites of pyramidal neurons, while distal input is reaching apical dendrites. Therefore, currents that are generated in the neuron as a response to proximal stimulation flow predominantly in the upward direction (with respect to the surface of the cortex), and distal drive creates downward currents [32]. Spontaneous alpha rhythm emerges when the delay between proximal and distal inputs is 50 ms, and both are delivered to the network with a frequency of 10 Hz [324041]. However, simultaneous presence of both proximal and distal inputs is not essential for the emergence of the alpha rhythm (see Results/Asymmetric currents lead to non-zero mean oscillations). The current figure demonstrates the most biologically plausible layout of inputs’ allocation.

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