Self-organization of in vitro neuronal assemblies drives to complex network topology
Activity-dependent self-organization plays an important role in the formation of specific and stereotyped connectivity patterns in neural circuits. By combining neuronal cultures, and tools with approaches from network neuroscience and information theory, we can study how complex network topology em...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-06-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/74921 |
| _version_ | 1797998265797443584 |
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| author | Priscila C Antonello Thomas F Varley John Beggs Marimélia Porcionatto Olaf Sporns Jean Faber |
| author_facet | Priscila C Antonello Thomas F Varley John Beggs Marimélia Porcionatto Olaf Sporns Jean Faber |
| author_sort | Priscila C Antonello |
| collection | DOAJ |
| description | Activity-dependent self-organization plays an important role in the formation of specific and stereotyped connectivity patterns in neural circuits. By combining neuronal cultures, and tools with approaches from network neuroscience and information theory, we can study how complex network topology emerges from local neuronal interactions. We constructed effective connectivity networks using a transfer entropy analysis of spike trains recorded from rat embryo dissociated hippocampal neuron cultures between 6 and 35 days in vitro to investigate how the topology evolves during maturation. The methodology for constructing the networks considered the synapse delay and addressed the influence of firing rate and population bursts as well as spurious effects on the inference of connections. We found that the number of links in the networks grew over the course of development, shifting from a segregated to a more integrated architecture. As part of this progression, three significant aspects of complex network topology emerged. In agreement with previous in silico and in vitro studies, a small-world architecture was detected, largely due to strong clustering among neurons. Additionally, the networks developed in a modular topology, with most modules comprising nearby neurons. Finally, highly active neurons acquired topological characteristics that made them important nodes to the network and integrators of modules. These findings leverage new insights into how neuronal effective network topology relates to neuronal assembly self-organization mechanisms. |
| first_indexed | 2024-04-11T10:45:55Z |
| format | Article |
| id | doaj.art-c0f77a66d966431290833be23e615bdb |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T10:45:55Z |
| publishDate | 2022-06-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-c0f77a66d966431290833be23e615bdb2022-12-22T04:29:03ZengeLife Sciences Publications LtdeLife2050-084X2022-06-011110.7554/eLife.74921Self-organization of in vitro neuronal assemblies drives to complex network topologyPriscila C Antonello0https://orcid.org/0000-0002-0624-1169Thomas F Varley1https://orcid.org/0000-0002-3317-9882John Beggs2Marimélia Porcionatto3Olaf Sporns4Jean Faber5https://orcid.org/0000-0002-2129-8251Department of Biochemistry – Escola Paulista de Medicina – Universidade Federal de São Paulo (UNIFESP), São Paulo, BrazilDepartment of Psychological and Brain Sciences, Indiana University, Bloomington, United States; Department of Informatics, Computing, and Engineering, Indiana University, Bloomington, United StatesDepartment of Physics, Indiana University, Bloomington, United StatesDepartment of Biochemistry – Escola Paulista de Medicina – Universidade Federal de São Paulo (UNIFESP), São Paulo, BrazilDepartment of Psychological and Brain Sciences, Indiana University, Bloomington, United StatesDepartment of Neurology and Neurosurgery – Escola Paulista de Medicina – Universidade Federal de São Paulo (UNIFESP), São Paulo, BrazilActivity-dependent self-organization plays an important role in the formation of specific and stereotyped connectivity patterns in neural circuits. By combining neuronal cultures, and tools with approaches from network neuroscience and information theory, we can study how complex network topology emerges from local neuronal interactions. We constructed effective connectivity networks using a transfer entropy analysis of spike trains recorded from rat embryo dissociated hippocampal neuron cultures between 6 and 35 days in vitro to investigate how the topology evolves during maturation. The methodology for constructing the networks considered the synapse delay and addressed the influence of firing rate and population bursts as well as spurious effects on the inference of connections. We found that the number of links in the networks grew over the course of development, shifting from a segregated to a more integrated architecture. As part of this progression, three significant aspects of complex network topology emerged. In agreement with previous in silico and in vitro studies, a small-world architecture was detected, largely due to strong clustering among neurons. Additionally, the networks developed in a modular topology, with most modules comprising nearby neurons. Finally, highly active neurons acquired topological characteristics that made them important nodes to the network and integrators of modules. These findings leverage new insights into how neuronal effective network topology relates to neuronal assembly self-organization mechanisms.https://elifesciences.org/articles/74921effective connectivitynetwork neuroscienceneuronal networks |
| spellingShingle | Priscila C Antonello Thomas F Varley John Beggs Marimélia Porcionatto Olaf Sporns Jean Faber Self-organization of in vitro neuronal assemblies drives to complex network topology eLife effective connectivity network neuroscience neuronal networks |
| title | Self-organization of in vitro neuronal assemblies drives to complex network topology |
| title_full | Self-organization of in vitro neuronal assemblies drives to complex network topology |
| title_fullStr | Self-organization of in vitro neuronal assemblies drives to complex network topology |
| title_full_unstemmed | Self-organization of in vitro neuronal assemblies drives to complex network topology |
| title_short | Self-organization of in vitro neuronal assemblies drives to complex network topology |
| title_sort | self organization of in vitro neuronal assemblies drives to complex network topology |
| topic | effective connectivity network neuroscience neuronal networks |
| url | https://elifesciences.org/articles/74921 |
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