The role of neuron–glia interactions in the emergence of ultra-slow oscillations

Abstract

Ultra-slow cortical oscillatory activity of 1-100 mHz has been recorded in human by electroencephalography and in dissociated cultures of cortical rat neurons, but the underlying mechanisms remain to be elucidated. This study presents a computational model of ultra-slow oscillatory activity based on the interaction between neurons and astrocytes. We predict that the frequency of these oscillations closely depends on activation of astrocytes in the network, which is reflected by oscillations of their intracellular calcium concentrations with periods between tens of seconds and minutes. An increase of intracellular calcium in astrocytes triggers the release of adenosine triphosphate from these cells which may alter transmission at nearby synapses by increasing or decreasing neurotransmitter release. These results provide theoretical support for the emerging awareness of astrocytes as active players in the regulation of neural activity and identify neuron-astrocyte interactions as a potential primary mechanism for the emergence of ultra-slow cortical oscillations.

Computational Models for Calcium-Mediated Astrocyte Functions

“…Half of the neuron-astrocyte network models were so-called generic models. Others, however, were specified to model neuron-astrocyte interactions in the cortex (Allegrini et al, 2009 ; Liu and Li, 2013a ; Chan et al, 2017 ; Tang et al, 2017 ; Yao et al, 2018 ), hippocampus (Amiri et al, 2012a , 2013a ; Mesiti et al, 2015a ; Li et al, 2016c ), spinal cord (Yang and Yeo, 2015 ), or thalamocortical networks (Amiri et al, 2012b , c ).…”

“…Three of the studied publications utilized Hodgkin and Huxley ( 1952 ) model (Liu and Li, 2013b ; Li et al, 2016c ; Yao et al, 2018 ) and one utilized Traub et al ( 1991 ) model's derivative Pinsky and Rinzel ( 1994 ) model (Mesiti et al, 2015a ). Simpler phenomenological models used in the studied publications were the FitzHugh-Nagumo (FitzHugh, 1961 ) model (Postnov et al, 2009 ; Hayati et al, 2016 ), LIF (Gerstner and Kistler, 2002 ) model (Liu and Li, 2013a ; Naeem et al, 2015 ), Izhikevich ( 2007 ) model (Allegrini et al, 2009 ; Haghiri et al, 2016 , 2017 ; Tang et al, 2017 ), Morris and Lecar ( 1981 ) model or its derivatives (Amiri et al, 2012a , 2013a ; Chan et al, 2017 ), and Suffczynski et al ( 2004 ) neuronal population model (Amiri et al, 2012b , c ). The released neurotransmitter was modeled explicitly by Amiri et al ( 2012a , 2013a ), Liu and Li ( 2013a ), Yang and Yeo ( 2015 ), Li et al ( 2016c ), and Yao et al ( 2018 ).…”

“…One of the newest models was the model by Chan et al ( 2017 ). Their neuron-astrocyte network model was able to generate ultra-slow neuronal oscillatory activity patterns with frequencies less than 0.01 Hz, recorded by high-density microelectrode arrays and examined using methods reflecting conventional EEG analysis rather than conventional microelectrode array analysis.…”

“…Most of the astrocyte models presented here are based on ordinary differential equations (ODEs), modeling well-stirred astrocytes (see e.g., Nadkarni and Jung, 2003 ; Ullah et al, 2006 ; Volman et al, 2007 ; De Pittà et al, 2009a ; Goldberg et al, 2010 ; Dupont et al, 2011 ; Valenza et al, 2011 ; Amiri et al, 2012a ; Wade et al, 2012 ; Hadfield et al, 2013 ; Tang et al, 2013 ; Lallouette et al, 2014 ; Wallach et al, 2014 ; Li et al, 2016a ; Chan et al, 2017 ; Guo et al, 2017 ; Handy et al, 2017 ; Taheri et al, 2017 ). These models make the assumption that chemical species have the same concentrations throughout the entire volume of the astrocyte, which can also be called as average concentrations.…”

The effects of different frequencies of repetitive transcranial magnetic stimulation (rTMS) on intracranial neurotransmitters in patients with swallowing disorders after cerebral infarction

“…S. Y. MOK first reported that network-wide ultra-slow oscillations aggregate the firing rates of cortical cultures [9]. Siow-Cheng Chan's results provided theoretical support for astrocytes as active players in the regulation of neural activity and identified neuron-astrocyte interactions as a potential primary mechanism for the emergence of ultra-slow cortical oscillations [10].Therefore, ultra-slow oscillations are very important in the study of the brain.…”