Neuronal Degeneration Impairs Rhythms Between Connected Microcircuits
Synchronization of neural activity across brain regions is critical to processes that include perception, learning, and memory. After traumatic brain injury (TBI), neuronal degeneration is one possible effect and can alter communication between neural circuits. Consequently, synchronization between...
| Main Authors: | , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2020-03-01
|
| Series: | Frontiers in Computational Neuroscience |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fncom.2020.00018/full |
| _version_ | 1818486129937088512 |
|---|---|
| author | Samantha N. Schumm David Gabrieli David F. Meaney David F. Meaney |
| author_facet | Samantha N. Schumm David Gabrieli David F. Meaney David F. Meaney |
| author_sort | Samantha N. Schumm |
| collection | DOAJ |
| description | Synchronization of neural activity across brain regions is critical to processes that include perception, learning, and memory. After traumatic brain injury (TBI), neuronal degeneration is one possible effect and can alter communication between neural circuits. Consequently, synchronization between neurons may change and can contribute to both lasting changes in functional brain networks and cognitive impairment in patients. However, fundamental principles relating exactly how TBI at the cellular scale affects synchronization of mesoscale circuits are not well understood. In this work, we use computational networks of Izhikevich integrate-and-fire neurons to study synchronized, oscillatory activity between clusters of neurons, which also adapt according to spike-timing-dependent plasticity (STDP). We study how the connections within and between these neuronal clusters change as unidirectional connections form between the two neuronal populations. In turn, we examine how neuronal deletion, intended to mimic the temporary or permanent loss of neurons in the mesoscale circuit, affects these dynamics. We determine synchronization of two neuronal circuits requires very modest connectivity between these populations; approximately 10% of neurons projecting from one circuit to another circuit will result in high synchronization. In addition, we find that synchronization level inversely affects the strength of connection between neuronal microcircuits – moderately synchronized microcircuits develop stronger intercluster connections than do highly synchronized circuits. Finally, we find that highly synchronized circuits are largely protected against the effects of neuronal deletion but may display changes in frequency properties across circuits with targeted neuronal loss. Together, our results suggest that strongly and weakly connected regions differ in their inherent resilience to damage and may serve different roles in a larger network. |
| first_indexed | 2024-12-10T16:18:46Z |
| format | Article |
| id | doaj.art-0a6eaaac523141c59a678c4f4f419aae |
| institution | Directory Open Access Journal |
| issn | 1662-5188 |
| language | English |
| last_indexed | 2024-12-10T16:18:46Z |
| publishDate | 2020-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Computational Neuroscience |
| spelling | doaj.art-0a6eaaac523141c59a678c4f4f419aae2022-12-22T01:41:53ZengFrontiers Media S.A.Frontiers in Computational Neuroscience1662-51882020-03-011410.3389/fncom.2020.00018497860Neuronal Degeneration Impairs Rhythms Between Connected MicrocircuitsSamantha N. Schumm0David Gabrieli1David F. Meaney2David F. Meaney3Department of Bioengineering, School of Engineering and Applied Sciences, University of Pennsylvania, Philadelphia, PA, United StatesDepartment of Bioengineering, School of Engineering and Applied Sciences, University of Pennsylvania, Philadelphia, PA, United StatesDepartment of Bioengineering, School of Engineering and Applied Sciences, University of Pennsylvania, Philadelphia, PA, United StatesPenn Center for Brain Injury and Repair, Department of Neurosurgery, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, United StatesSynchronization of neural activity across brain regions is critical to processes that include perception, learning, and memory. After traumatic brain injury (TBI), neuronal degeneration is one possible effect and can alter communication between neural circuits. Consequently, synchronization between neurons may change and can contribute to both lasting changes in functional brain networks and cognitive impairment in patients. However, fundamental principles relating exactly how TBI at the cellular scale affects synchronization of mesoscale circuits are not well understood. In this work, we use computational networks of Izhikevich integrate-and-fire neurons to study synchronized, oscillatory activity between clusters of neurons, which also adapt according to spike-timing-dependent plasticity (STDP). We study how the connections within and between these neuronal clusters change as unidirectional connections form between the two neuronal populations. In turn, we examine how neuronal deletion, intended to mimic the temporary or permanent loss of neurons in the mesoscale circuit, affects these dynamics. We determine synchronization of two neuronal circuits requires very modest connectivity between these populations; approximately 10% of neurons projecting from one circuit to another circuit will result in high synchronization. In addition, we find that synchronization level inversely affects the strength of connection between neuronal microcircuits – moderately synchronized microcircuits develop stronger intercluster connections than do highly synchronized circuits. Finally, we find that highly synchronized circuits are largely protected against the effects of neuronal deletion but may display changes in frequency properties across circuits with targeted neuronal loss. Together, our results suggest that strongly and weakly connected regions differ in their inherent resilience to damage and may serve different roles in a larger network.https://www.frontiersin.org/article/10.3389/fncom.2020.00018/fullneurodegenerationmicrocircuitnetworksynchronizationrhythms |
| spellingShingle | Samantha N. Schumm David Gabrieli David F. Meaney David F. Meaney Neuronal Degeneration Impairs Rhythms Between Connected Microcircuits Frontiers in Computational Neuroscience neurodegeneration microcircuit network synchronization rhythms |
| title | Neuronal Degeneration Impairs Rhythms Between Connected Microcircuits |
| title_full | Neuronal Degeneration Impairs Rhythms Between Connected Microcircuits |
| title_fullStr | Neuronal Degeneration Impairs Rhythms Between Connected Microcircuits |
| title_full_unstemmed | Neuronal Degeneration Impairs Rhythms Between Connected Microcircuits |
| title_short | Neuronal Degeneration Impairs Rhythms Between Connected Microcircuits |
| title_sort | neuronal degeneration impairs rhythms between connected microcircuits |
| topic | neurodegeneration microcircuit network synchronization rhythms |
| url | https://www.frontiersin.org/article/10.3389/fncom.2020.00018/full |
| work_keys_str_mv | AT samanthanschumm neuronaldegenerationimpairsrhythmsbetweenconnectedmicrocircuits AT davidgabrieli neuronaldegenerationimpairsrhythmsbetweenconnectedmicrocircuits AT davidfmeaney neuronaldegenerationimpairsrhythmsbetweenconnectedmicrocircuits AT davidfmeaney neuronaldegenerationimpairsrhythmsbetweenconnectedmicrocircuits |