The flow of axonal information among hippocampal sub-regions 2: patterned stimulation sharpens routing of information transmission
The sub-regions of the hippocampal formation are essential for episodic learning and memory formation, yet the spike dynamics of each region contributing to this function are poorly understood, in part because of a lack of access to the inter-regional communicating axons. Here, we reconstructed hipp...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-12-01
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| Series: | Frontiers in Neural Circuits |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fncir.2023.1272925/full |
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| author | Samuel Brandon Lassers Yash S. Vakilna Yash S. Vakilna William C. Tang William C. Tang Gregory J. Brewer Gregory J. Brewer |
| author_facet | Samuel Brandon Lassers Yash S. Vakilna Yash S. Vakilna William C. Tang William C. Tang Gregory J. Brewer Gregory J. Brewer |
| author_sort | Samuel Brandon Lassers |
| collection | DOAJ |
| description | The sub-regions of the hippocampal formation are essential for episodic learning and memory formation, yet the spike dynamics of each region contributing to this function are poorly understood, in part because of a lack of access to the inter-regional communicating axons. Here, we reconstructed hippocampal networks confined to four subcompartments in 2D cultures on a multi-electrode array that monitors individual communicating axons. In our novel device, somal, and axonal activity was measured simultaneously with the ability to ascertain the direction and speed of information transmission. Each sub-region and inter-regional axons had unique power-law spiking dynamics, indicating differences in computational functions, with abundant axonal feedback. After stimulation, spiking, and burst rates decreased in all sub-regions, spikes per burst generally decreased, intraburst spike rates increased, and burst duration decreased, which were specific for each sub-region. These changes in spiking dynamics post-stimulation were found to occupy a narrow range, consistent with the maintenance of the network at a critical state. Functional connections between the sub-region neurons and communicating axons in our device revealed homeostatic network routing strategies post-stimulation in which spontaneous feedback activity was selectively decreased and balanced by decreased feed-forward activity. Post-stimulation, the number of functional connections per array decreased, but the reliability of those connections increased. The networks maintained a balance in spiking and bursting dynamics in response to stimulation and sharpened network routing. These plastic characteristics of the network revealed the dynamic architecture of hippocampal computations in response to stimulation by selective routing on a spatiotemporal scale in single axons. |
| first_indexed | 2024-03-09T01:59:10Z |
| format | Article |
| id | doaj.art-e9dc4b74607e46dca3ddc12cad6c5d8a |
| institution | Directory Open Access Journal |
| issn | 1662-5110 |
| language | English |
| last_indexed | 2024-03-09T01:59:10Z |
| publishDate | 2023-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neural Circuits |
| spelling | doaj.art-e9dc4b74607e46dca3ddc12cad6c5d8a2023-12-08T11:17:24ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102023-12-011710.3389/fncir.2023.12729251272925The flow of axonal information among hippocampal sub-regions 2: patterned stimulation sharpens routing of information transmissionSamuel Brandon Lassers0Yash S. Vakilna1Yash S. Vakilna2William C. Tang3William C. Tang4Gregory J. Brewer5Gregory J. Brewer6Department of Biomedical Engineering, University of California, Irvine, Irvine, CA, United StatesDepartment of Biomedical Engineering, University of California, Irvine, Irvine, CA, United StatesTexas Institute of Restorative Neurotechnologies (TIRN), The University of Texas Health Science Center (UTHealth), Houston, TX, United StatesDepartment of Biomedical Engineering, University of California, Irvine, Irvine, CA, United StatesDepartment of Biomedical Engineering, National Taiwan University, Taipei, TaiwanDepartment of Biomedical Engineering, University of California, Irvine, Irvine, CA, United StatesMemory Impairments and Neurological Disorders (MIND) Institute, Center for Neuroscience of Learning and Memory, University of California, Irvine, Irvine, CA, United StatesThe sub-regions of the hippocampal formation are essential for episodic learning and memory formation, yet the spike dynamics of each region contributing to this function are poorly understood, in part because of a lack of access to the inter-regional communicating axons. Here, we reconstructed hippocampal networks confined to four subcompartments in 2D cultures on a multi-electrode array that monitors individual communicating axons. In our novel device, somal, and axonal activity was measured simultaneously with the ability to ascertain the direction and speed of information transmission. Each sub-region and inter-regional axons had unique power-law spiking dynamics, indicating differences in computational functions, with abundant axonal feedback. After stimulation, spiking, and burst rates decreased in all sub-regions, spikes per burst generally decreased, intraburst spike rates increased, and burst duration decreased, which were specific for each sub-region. These changes in spiking dynamics post-stimulation were found to occupy a narrow range, consistent with the maintenance of the network at a critical state. Functional connections between the sub-region neurons and communicating axons in our device revealed homeostatic network routing strategies post-stimulation in which spontaneous feedback activity was selectively decreased and balanced by decreased feed-forward activity. Post-stimulation, the number of functional connections per array decreased, but the reliability of those connections increased. The networks maintained a balance in spiking and bursting dynamics in response to stimulation and sharpened network routing. These plastic characteristics of the network revealed the dynamic architecture of hippocampal computations in response to stimulation by selective routing on a spatiotemporal scale in single axons.https://www.frontiersin.org/articles/10.3389/fncir.2023.1272925/fullnetworkshippocampuselectrode arrayentorhinaldentateCA3 |
| spellingShingle | Samuel Brandon Lassers Yash S. Vakilna Yash S. Vakilna William C. Tang William C. Tang Gregory J. Brewer Gregory J. Brewer The flow of axonal information among hippocampal sub-regions 2: patterned stimulation sharpens routing of information transmission Frontiers in Neural Circuits networks hippocampus electrode array entorhinal dentate CA3 |
| title | The flow of axonal information among hippocampal sub-regions 2: patterned stimulation sharpens routing of information transmission |
| title_full | The flow of axonal information among hippocampal sub-regions 2: patterned stimulation sharpens routing of information transmission |
| title_fullStr | The flow of axonal information among hippocampal sub-regions 2: patterned stimulation sharpens routing of information transmission |
| title_full_unstemmed | The flow of axonal information among hippocampal sub-regions 2: patterned stimulation sharpens routing of information transmission |
| title_short | The flow of axonal information among hippocampal sub-regions 2: patterned stimulation sharpens routing of information transmission |
| title_sort | flow of axonal information among hippocampal sub regions 2 patterned stimulation sharpens routing of information transmission |
| topic | networks hippocampus electrode array entorhinal dentate CA3 |
| url | https://www.frontiersin.org/articles/10.3389/fncir.2023.1272925/full |
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