Impact of Network Topology on Neural Synchrony in a Model of the Subthalamic Nucleus-Globus Pallidus Circuit

Synchronous neural oscillations within the beta frequency range are observed across the parkinsonian basal ganglia network, including within the subthalamic nucleus (STN) - globus pallidus (GPe) subcircuit. The emergence of pathological synchrony in Parkinson’s disease is often attributed...

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Main Authors: Cathal McLoughlin, Madeleine Lowery
Format: Article
Language:English
Published: IEEE 2024-01-01
Series:IEEE Transactions on Neural Systems and Rehabilitation Engineering
Subjects:
Online Access:https://ieeexplore.ieee.org/document/10373090/
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author Cathal McLoughlin
Madeleine Lowery
author_facet Cathal McLoughlin
Madeleine Lowery
author_sort Cathal McLoughlin
collection DOAJ
description Synchronous neural oscillations within the beta frequency range are observed across the parkinsonian basal ganglia network, including within the subthalamic nucleus (STN) - globus pallidus (GPe) subcircuit. The emergence of pathological synchrony in Parkinson’s disease is often attributed to changes in neural properties or connection strength, and less often to the network topology, i.e. the structural arrangement of connections between neurons. This study investigates the relationship between network structure and neural synchrony in a model of the STN-GPe circuit comprised of conductance-based spiking neurons. Changes in net synaptic input were controlled for through a synaptic scaling rule, which facilitated separation of the effects of network structure from net synaptic input. Five topologies were examined as structures for the STN-GPe circuit: Watts-Strogatz, preferential attachment, spatial, stochastic block, k-regular random. Beta band synchrony generally increased as the number of connections increased, however the exact relationship was topology specific. Varying the wiring pattern while maintaining a constant number of connections caused network synchrony to be enhanced or suppressed, demonstrating the ability of purely structural changes to alter synchrony. This relationship was well-captured by the algebraic connectivity of the network, the second smallest eigenvalue of the network’s Laplacian matrix. The structure-synchrony relationship was further investigated in a network model designed to emulate the action selection role of the STN-GPe circuit. It was found that increasing the number of connections and/or the overlap of action selection channels could lead to a rapid transition to synchrony, which was also predicted by the algebraic connectivity.
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spelling doaj.art-49a97fcf92b748bcbc333440cb5bb5a32024-01-16T00:00:19ZengIEEEIEEE Transactions on Neural Systems and Rehabilitation Engineering1558-02102024-01-013228229210.1109/TNSRE.2023.334645610373090Impact of Network Topology on Neural Synchrony in a Model of the Subthalamic Nucleus-Globus Pallidus CircuitCathal McLoughlin0https://orcid.org/0000-0001-9086-6286Madeleine Lowery1https://orcid.org/0000-0001-6743-360XDepartment of Electrical and Electronic Engineering, University College Dublin, Dublin, IrelandDepartment of Electrical and Electronic Engineering, University College Dublin, Dublin, IrelandSynchronous neural oscillations within the beta frequency range are observed across the parkinsonian basal ganglia network, including within the subthalamic nucleus (STN) - globus pallidus (GPe) subcircuit. The emergence of pathological synchrony in Parkinson’s disease is often attributed to changes in neural properties or connection strength, and less often to the network topology, i.e. the structural arrangement of connections between neurons. This study investigates the relationship between network structure and neural synchrony in a model of the STN-GPe circuit comprised of conductance-based spiking neurons. Changes in net synaptic input were controlled for through a synaptic scaling rule, which facilitated separation of the effects of network structure from net synaptic input. Five topologies were examined as structures for the STN-GPe circuit: Watts-Strogatz, preferential attachment, spatial, stochastic block, k-regular random. Beta band synchrony generally increased as the number of connections increased, however the exact relationship was topology specific. Varying the wiring pattern while maintaining a constant number of connections caused network synchrony to be enhanced or suppressed, demonstrating the ability of purely structural changes to alter synchrony. This relationship was well-captured by the algebraic connectivity of the network, the second smallest eigenvalue of the network’s Laplacian matrix. The structure-synchrony relationship was further investigated in a network model designed to emulate the action selection role of the STN-GPe circuit. It was found that increasing the number of connections and/or the overlap of action selection channels could lead to a rapid transition to synchrony, which was also predicted by the algebraic connectivity.https://ieeexplore.ieee.org/document/10373090/Beta oscillationsParkinson’s diseasenetwork neurosciencecomputational modelingaction selection
spellingShingle Cathal McLoughlin
Madeleine Lowery
Impact of Network Topology on Neural Synchrony in a Model of the Subthalamic Nucleus-Globus Pallidus Circuit
IEEE Transactions on Neural Systems and Rehabilitation Engineering
Beta oscillations
Parkinson’s disease
network neuroscience
computational modeling
action selection
title Impact of Network Topology on Neural Synchrony in a Model of the Subthalamic Nucleus-Globus Pallidus Circuit
title_full Impact of Network Topology on Neural Synchrony in a Model of the Subthalamic Nucleus-Globus Pallidus Circuit
title_fullStr Impact of Network Topology on Neural Synchrony in a Model of the Subthalamic Nucleus-Globus Pallidus Circuit
title_full_unstemmed Impact of Network Topology on Neural Synchrony in a Model of the Subthalamic Nucleus-Globus Pallidus Circuit
title_short Impact of Network Topology on Neural Synchrony in a Model of the Subthalamic Nucleus-Globus Pallidus Circuit
title_sort impact of network topology on neural synchrony in a model of the subthalamic nucleus globus pallidus circuit
topic Beta oscillations
Parkinson’s disease
network neuroscience
computational modeling
action selection
url https://ieeexplore.ieee.org/document/10373090/
work_keys_str_mv AT cathalmcloughlin impactofnetworktopologyonneuralsynchronyinamodelofthesubthalamicnucleusglobuspalliduscircuit
AT madeleinelowery impactofnetworktopologyonneuralsynchronyinamodelofthesubthalamicnucleusglobuspalliduscircuit