Hippocampal recording with a soft microelectrode array in a cranial window imaging scheme: a validation study.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
19 Oct 2024
19 Oct 2024
Historique:
received:
26
03
2024
accepted:
03
10
2024
medline:
20
10
2024
pubmed:
20
10
2024
entrez:
19
10
2024
Statut:
epublish
Résumé
The hippocampus has a crucial role in the formation, consolidation and recall of memories as well as in navigation related processes. These functions are in the focus of neuroscience and different disciplines have contributed to this research field for decades. Two-photon imaging in awake animals is a valuable new aspect for these observations, especially when it is supported by electrophysiology. In this study, we applied high speed two-photon hippocampal imaging through a chronically implanted, soft, transparent microelectrode (STM) device incorporated into a cranial window chamber in awake mice. We monitored the impedance of the recording sites over the course of the experiments to observe long-term changes in recording quality. The large-scale ipsilateral local field potential (LFP) recordings from the dorsal hippocampus provided reliable sharp wave-ripples (SPW-Rs), multi-unit activity (MUA) and single-unit activity (SUA) for up to two months. Calcium imaging of GCaMP6f. labeled cells from the CA1 pyramidal layer under the transparent device was possible even after six months in thy1-GCaMP6f. transgenic mice. We investigated the immune response with GFAP staining after the end of the long-term experiments. Based on our results, this dedicated transparent electrode device proved to be suitable for simultaneous two-photon imaging and large-scale electrophysiological measurements in chronic experiments in mice.
Identifiants
pubmed: 39427030
doi: 10.1038/s41598-024-75170-1
pii: 10.1038/s41598-024-75170-1
doi:
Types de publication
Journal Article
Validation Study
Langues
eng
Sous-ensembles de citation
IM
Pagination
24585Subventions
Organisme : National Research, Development and Innovation Office
ID : VKE-2018-00032
Organisme : Innovációs és Technológiai Minisztérium
ID : 2020-2.1.1-ED-2022-00208
Organisme : Nemzeti Kutatási Fejlesztési és Innovációs Hivatal
ID : TKP2021-EGA-42
Organisme : Hungarian Brain Research Program
ID : NAP2022I-8/2022
Informations de copyright
© 2024. The Author(s).
Références
Buzsáki, G. Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning. Hippocampus 25(10), 1073–1188 (2015).
doi: 10.1002/hipo.22488
pubmed: 26135716
pmcid: 4648295
Liu, X. et al. E-Cannula reveals anatomical diversity in sharp-wave ripples as a driver for the recruitment of distinct hippocampal assemblies. Cell Rep. 41(1), 111453 (2022).
doi: 10.1016/j.celrep.2022.111453
pubmed: 36198271
pmcid: 9640218
Dombeck, D. A., Harvey, C. D., Tian, L., Looger, L. L. & Tank, D. W. Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat. Neurosci. 13(11), 1433–1440 (2010).
doi: 10.1038/nn.2648
pubmed: 20890294
pmcid: 2967725
Geiller, T. et al. Large-scale 3D two-photon imaging of molecularly identified CA1 interneuron dynamics in behaving mice. Neuron 108(5), 968–983 (2020).
doi: 10.1016/j.neuron.2020.09.013
pubmed: 33022227
pmcid: 7736348
Malvache, A., Reichinnek, S., Villette, V., Haimerl, C. & Cossart, R. Awake hippocampal reactivations project onto orthogonal neuronal assemblies. Science 353(6305), 1280–1283 (2016).
doi: 10.1126/science.aaf3319
pubmed: 27634534
Judák, L. et al. Sharp-wave ripple doublets induce complex dendritic spikes in parvalbumin interneurons in vivo. Nat. Commun. 13(1), 6715 (2022).
doi: 10.1038/s41467-022-34520-1
pubmed: 36344570
pmcid: 9640570
Ware, T. et al. Three-dimensional flexible electronics enabled by shape memory polymer substrates for responsive neural interfaces. Macromol. Mater. Eng. 297(12), 1193–1202 (2012).
doi: 10.1002/mame.201200241
pubmed: 25530708
pmcid: 4268152
Stiller, A. M. et al. Chronic intracortical recording and electrochemical stability of thiol-ene/acrylate shape memory polymer electrode arrays. Micromachines 9(10), 500 (2018).
doi: 10.3390/mi9100500
pubmed: 30424433
pmcid: 6215160
Zátonyi, A. et al. A softening laminar electrode for recording single unit activity from the rat hippocampus. Sci. Rep. 9(1), 2321 (2019).
doi: 10.1038/s41598-019-39835-6
pubmed: 30787389
pmcid: 6382803
Black, B. J. et al. In vitro compatibility testing of thiol-ene/acrylate-based shape memory polymers for use in implantable neural interfaces. J. Biomed. Mater. Res. Part A 106(11), 2891–2898 (2018).
doi: 10.1002/jbm.a.36478
Shoffstall, A. J. et al. Characterization of the neuroinflammatory response to thiol-ene shape memory polymer coated intracortical microelectrodes. Micromachines 9(10), 486 (2018).
doi: 10.3390/mi9100486
pubmed: 30424419
pmcid: 6215215
Fedor, F. Z. et al. Soft, thiol-ene/acrylate-based electrode array for long-term recording of intracranial EEG signals with improved biocompatibility in mice. Adv. Mater. Technol. 7(5), 2100942 (2022).
doi: 10.1002/admt.202100942
Szabó, Á. et al. Transparent thiol-ene/acrylate-based microECoG devices used for concurrent recording of fluorescent calcium signals and electrophysiology in awake animals. Adv. Mater. Interfaces 9(25), 2200729 (2022).
doi: 10.1002/admi.202200729
Fekete, Z., Zátonyi, A., Kaszás, A., Madarász, M. & Slézia, A. Transparent neural interfaces: challenges and solutions of microengineered multimodal implants designed to measure intact neuronal populations using high-resolution electrophysiology and microscopy simultaneously. Microsyst. Nanoeng. 9(1), 66 (2023).
doi: 10.1038/s41378-023-00519-x
pubmed: 37213820
pmcid: 10195795
Chiovini, B. et al. Theoretical design, synthesis, and in vitro neurobiological applications of a highly efficient two-photon caged GABA validated on an epileptic case. ACS Omega 6(23), 15029–15045 (2021).
doi: 10.1021/acsomega.1c01164
pubmed: 34151084
pmcid: 8210458
Szalay, G. et al. Fast 3D imaging of spine, dendritic, and neuronal assemblies in behaving animals. Neuron 92(4), 723–738 (2016).
doi: 10.1016/j.neuron.2016.10.002
pubmed: 27773582
pmcid: 5167293
Senzai, Y. & Buzsáki, G. Physiological properties and behavioral correlates of hippocampal granule cells and mossy cells. Neuron 93(3), 691–704 (2017).
doi: 10.1016/j.neuron.2016.12.011
pubmed: 28132824
pmcid: 5293146
Paxinos, G., and Franklin, K. B. J., The Mouse Brain in Stereotaxic Coordinates, Academic Press, 2019, eBook ISBN:9780128161586 (2001).
Patel, J., Schomburg, E. W., Berényi, A., Fujisawa, S., & Buzsáki, G. Local generation and propagation ofripples along the septotemporal axis of the hippocampus. J. Neuroscience, 33(43), 17029–17041 (2013).
Tóth, R. et al. Do not waste your electrodes—Principles of optimal electrode geometry for spike sorting. J. Neural Eng. 18(4), 0460a8 (2021).
doi: 10.1088/1741-2552/ac0f49
Zátonyi, A. et al. Transparent, low-autofluorescence microECoG device for simultaneous Ca2+ imaging and cortical electrophysiology in vivo. J. Neural Eng. 17(1), 016062 (2020).
doi: 10.1088/1741-2552/ab603f
pubmed: 31822640
Dijk, G., Kaszas, A., Pas, J. & O’Connor, R. P. Fabrication and in vivo 2-photon microscopy validation of transparent PEDOT: PSS microelectrode arrays. Microsyst. Nanoeng. 8(1), 90 (2022).
doi: 10.1038/s41378-022-00434-7
pubmed: 36051746
pmcid: 9424218
Madarász, M., Fedor, F. Z., Fekete, Z. & Rózsa, B. Immunohistological responses in mice implanted with Parylene HT–ITO ECoG devices. Front. Neurosci. 17, 1209913 (2023).
doi: 10.3389/fnins.2023.1209913
pubmed: 37746144
pmcid: 10513038