Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks
Neurons in vitro connect to each other and form neural networks that display emergent electrophysiological activity. This activity begins as spontaneous uncorrelated firing in the early phase of development, and as functional excitatory and inhibitory synapses mature, the activity typically emerges...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-02-01
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| Series: | Frontiers in Neural Circuits |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fncir.2023.1020487/full |
| _version_ | 1797905126588940288 |
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| author | Janelle Shari Weir Nicholas Christiansen Axel Sandvig Axel Sandvig Axel Sandvig Axel Sandvig Ioanna Sandvig |
| author_facet | Janelle Shari Weir Nicholas Christiansen Axel Sandvig Axel Sandvig Axel Sandvig Axel Sandvig Ioanna Sandvig |
| author_sort | Janelle Shari Weir |
| collection | DOAJ |
| description | Neurons in vitro connect to each other and form neural networks that display emergent electrophysiological activity. This activity begins as spontaneous uncorrelated firing in the early phase of development, and as functional excitatory and inhibitory synapses mature, the activity typically emerges as spontaneous network bursts. Network bursts are events of coordinated global activation among many neurons interspersed with periods of silencing and are important for synaptic plasticity, neural information processing, and network computation. While bursting is the consequence of balanced excitatory-inhibitory (E/I) interactions, the functional mechanisms underlying their evolution from physiological to potentially pathophysiological states, such as decreasing or increasing in synchrony, are still poorly understood. Synaptic activity, especially that related to maturity of E/I synaptic transmission, is known to strongly influence these processes. In this study, we used selective chemogenetic inhibition to target and disrupt excitatory synaptic transmission in in vitro neural networks to study functional response and recovery of spontaneous network bursts over time. We found that over time, inhibition resulted in increases in both network burstiness and synchrony. Our results indicate that the disruption in excitatory synaptic transmission during early network development likely affected inhibitory synaptic maturity which resulted in an overall decrease in network inhibition at later stages. These findings lend support to the importance of E/I balance in maintaining physiological bursting dynamics and, conceivably, information processing capacity in neural networks. |
| first_indexed | 2024-04-10T10:00:05Z |
| format | Article |
| id | doaj.art-71f9b033f78647ff8d5e2919f3576db1 |
| institution | Directory Open Access Journal |
| issn | 1662-5110 |
| language | English |
| last_indexed | 2024-04-10T10:00:05Z |
| publishDate | 2023-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neural Circuits |
| spelling | doaj.art-71f9b033f78647ff8d5e2919f3576db12023-02-16T09:01:16ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102023-02-011710.3389/fncir.2023.10204871020487Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networksJanelle Shari Weir0Nicholas Christiansen1Axel Sandvig2Axel Sandvig3Axel Sandvig4Axel Sandvig5Ioanna Sandvig6Department of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, NorwayDepartment of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, NorwayDepartment of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, NorwayDepartment of Neurology and Clinical Neurophysiology, St. Olav’s University Hospital, Trondheim, NorwayDivision of Neuro, Head and Neck, Department of Pharmacology and Clinical Neurosciences, Umeå University Hospital, Umeå, SwedenDivision of Neuro, Head and Neck, Department of Community Medicine and Rehabilitation, Umeå University Hospital, Umeå, SwedenDepartment of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, NorwayNeurons in vitro connect to each other and form neural networks that display emergent electrophysiological activity. This activity begins as spontaneous uncorrelated firing in the early phase of development, and as functional excitatory and inhibitory synapses mature, the activity typically emerges as spontaneous network bursts. Network bursts are events of coordinated global activation among many neurons interspersed with periods of silencing and are important for synaptic plasticity, neural information processing, and network computation. While bursting is the consequence of balanced excitatory-inhibitory (E/I) interactions, the functional mechanisms underlying their evolution from physiological to potentially pathophysiological states, such as decreasing or increasing in synchrony, are still poorly understood. Synaptic activity, especially that related to maturity of E/I synaptic transmission, is known to strongly influence these processes. In this study, we used selective chemogenetic inhibition to target and disrupt excitatory synaptic transmission in in vitro neural networks to study functional response and recovery of spontaneous network bursts over time. We found that over time, inhibition resulted in increases in both network burstiness and synchrony. Our results indicate that the disruption in excitatory synaptic transmission during early network development likely affected inhibitory synaptic maturity which resulted in an overall decrease in network inhibition at later stages. These findings lend support to the importance of E/I balance in maintaining physiological bursting dynamics and, conceivably, information processing capacity in neural networks.https://www.frontiersin.org/articles/10.3389/fncir.2023.1020487/fullexcitatory-inhibitory balancenetwork burstselectrophysiologydesigner receptors exclusively activated by designer drugs (DREADDs)synchronychemogenetic approach |
| spellingShingle | Janelle Shari Weir Nicholas Christiansen Axel Sandvig Axel Sandvig Axel Sandvig Axel Sandvig Ioanna Sandvig Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks Frontiers in Neural Circuits excitatory-inhibitory balance network bursts electrophysiology designer receptors exclusively activated by designer drugs (DREADDs) synchrony chemogenetic approach |
| title | Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks |
| title_full | Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks |
| title_fullStr | Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks |
| title_full_unstemmed | Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks |
| title_short | Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks |
| title_sort | selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks |
| topic | excitatory-inhibitory balance network bursts electrophysiology designer receptors exclusively activated by designer drugs (DREADDs) synchrony chemogenetic approach |
| url | https://www.frontiersin.org/articles/10.3389/fncir.2023.1020487/full |
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