A computational model to uncover the biophysical underpinnings of neural firing heterogeneity in dissociated hippocampal cultures.
calcium imaging
dissociated hippocampal cultures
mathematical modeling
non-synaptic signaling
parameter estimation
Journal
Hippocampus
ISSN: 1098-1063
Titre abrégé: Hippocampus
Pays: United States
ID NLM: 9108167
Informations de publication
Date de publication:
11 2023
11 2023
Historique:
revised:
12
07
2023
received:
01
09
2022
accepted:
21
08
2023
medline:
23
10
2023
pubmed:
14
9
2023
entrez:
14
9
2023
Statut:
ppublish
Résumé
Calcium (Ca
Substances chimiques
Calcium
SY7Q814VUP
Glutamic Acid
3KX376GY7L
Inositol 1,4,5-Trisphosphate Receptors
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1208-1227Informations de copyright
© 2023 Wiley Periodicals LLC.
Références
Altemus, K. L., Lavenex, P., Ishizuka, N., & Amaral, D. G. (2005). Morphological characteristics and electrophysiological properties of CA1 pyramidal neurons in macaque monkeys. Neuroscience, 136(3), 741-756.
Bechtholt-Gompf, A. J., Walther, H. V., Adams, M. A., Carlezon, W. A., Jr., Ongür, D., & Cohen, B. M. (2010). Blockade of astrocytic glutamate uptake in rats induces signs of anhedonia and impaired spatial memory. Neuropsychopharmacology, 35(10), 2049-2059.
Biffi, E., Regalia, G., Menegon, A., Ferrigno, G., & Pedrocchi, A. (2013). The influence of neuronal density and maturation on network activity of hippocampal cell cultures: A methodological study. PLoS One, 8(12), e83899.
Bright, D. P., & Smart, T. G. (2013). Methods for recording and measuring tonic GABAA receptor-mediated inhibition. Frontiers in Neural Circuits, 7, 193.
Britzolaki, A., Cronin, C. C., Flaherty, P. R., Rufo, R. L., & Pitychoutis, P. M. (2021). Chronic but not acute pharmacological activation of SERCA induces behavioral and neurochemical effects in male and female mice. Behavioural Brain Research, 399, 112984.
Cairano, D., Eliana, S., Moretti, S., Marciani, P., Sacchi, V. F., Castagna, M., Davalli, A., Folli, F., & Perego, C. (2016). Neurotransmitters and neuropeptides: New players in the control of islet of Langerhans' cell mass and function. Journal of Cellular Physiology, 231(4), 756-767.
Carmignoto, G., & Fellin, T. (2006). Glutamate release from astrocytes as a non-synaptic mechanism for neuronal synchronization in the hippocampus. Journal of Physiology, 99(2-3), 98-102.
Carvalho, G., & Damasio, A. (2019). Non-synaptic transmission and the foundations of affect. https://doi.org/10.20944/preprints201901.0252.v1
Cembrowski, M. S., & Spruston, N. (2019). Heterogeneity within classical cell types is the rule: Lessons from hippocampal pyramidal neurons. Nature Reviews. Neuroscience, 20(4), 193-204.
Chiu, D. N., & Jahr, C. E. (2017). Extracellular glutamate in the nucleus accumbens is nanomolar in both synaptic and non-synaptic compartments. Cell Reports, 18(11), 2576-2583.
de Pittà, M., Ben-Jacob, E., & Berry, H. (2019). G protein-coupled receptor-mediated calcium signaling in astrocytes Springer series in computational neuroscience (pp. 115-150). Springer International Publishing.
de Pitta, M., & Berry, H. (Eds.). (2019). Computational glioscience Springer series in computational neuroscience (1st ed.). Springer Nature.
de Pittà, M., Goldberg, M., Volman, V., Berry, H., & Ben-Jacob, E. (2009). Glutamate regulation of calcium and IP3 oscillating and pulsating dynamics in astrocytes. Journal of Biological Physics, 35(4), 383-411.
Dhyani, V., Jana, S., & Giri, L. (2021). Gaussian mixture modeling of single-neuron responses obtained from confocal-calcium-imaging of dissociated rat hippocampal neurons. In 2021 10th international IEEE/EMBS conference on neural engineering (NER). IEEE. https://doi.org/10.1109/ner49283.2021.9441102
Dhyani, V., Kumar, S., Manne, S. R., Kaur, I., Jana, S., Russell, S., Sarkar, R., & Giri, L. (2023). Three-dimensional tracking of intracellular calcium and redox state during real-time control in a hypoxic gradient in microglia culture: Comparison of the channel blocker and Reoxygenation under ischemic shock. ACS Chemical Neuroscience, 14(10), 1810-1825.
Dhyani, V., Swain, S., Gupta, R. K., Saxena, A., Singh, R., & Giri, L. (2021). Role of metabotropic glutamate receptors (MGluRs) in the regulation of cellular calcium signaling: Theory, protocols, and data analysis. In Neuromethods (pp. 81-115). Springer US.
Dwivedi, Y. (2002). Antidepressants reduce phosphoinositide-specific phospholipase C (PI-PLC) activity and the MRNA and protein expression of selective PLC Β1 isozyme in rat brain. Neuropharmacology, 43(8), 1269-1279.
Eisenman, L. N., Kress, G., Zorumski, C. F., & Mennerick, S. (2006). A spontaneous tonic chloride conductance in solitary glutamatergic hippocampal neurons. Brain Research, 1118(1), 66-74.
Fleming, W., Jewell, S., Engelhard, B., Witten, D. M., & Witten, I. B. (2021). Inferring spikes from calcium imaging in dopamine neurons. PLoS One, 16(6), e0252345.
Frade, J. G., Barbosa, R. M., & Laranjinha, J. (2009). Stimulation of NMDA and AMPA glutamate receptors elicits distinct concentration dynamics of nitric oxide in rat hippocampal slices. Hippocampus, 19(7), 603-611.
Friedhoff, V. N., Antunes, G., Falcke, M., Fabio, M., & de Souza, S. (2021). Stochastic reaction-diffusion modeling of calcium dynamics in 3D dendritic spines of Purkinje cells. Biophysical Journal, 120(11), 2112-2123.
Gardner, A., Jukkola, P., & Chen, G. (2012). Myelination of rodent hippocampal neurons in culture. Nature Protocols, 7(10), 1774-1782.
Griego, E., Hernández-Frausto, M., Márquez, L. A., Lara-Valderrabano, L., Rubalcava, C. L., & Galván, E. J. (2022). Activation of D1/D5 receptors ameliorates decreased intrinsic excitability of hippocampal neurons induced by neonatal blockade of N-methyl-d-aspartate receptors. British Journal of Pharmacology, 179(8), 1695-1715.
Hirtz, J. J., Boesen, M., Braun, N., Deitmer, J. W., Kramer, F., Lohr, C., Müller, B., Nothwang, H. G., Striessnig, J., Löhrke, S., & Friauf, E. (2011). Cav1.3 calcium channels are required for Normal development of the auditory brainstem. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 31(22), 8280-8294.
Holbro, N., Grunditz, A., & Oertner, T. G. (2009). Differential distribution of endoplasmic reticulum controls metabotropic signaling and plasticity at hippocampal synapses. Proceedings of the National Academy of Sciences of the United States of America, 106(35), 15055-15060.
Ionescu, L., White, C., Cheung, K.-H., Shuai, J., Parker, I., Pearson, J. E., Kevin Foskett, J., & Mak, D.-O. D. (2007). Mode switching is the major mechanism of ligand regulation of InsP3 receptor calcium release channels. The Journal of General Physiology, 130(6), 631-645.
Koyanagi, Y., Torturo, C. L., Cook, D. C., Zhou, Z., & Hemmings Jr, H. C. (2019). Role of specific presynaptic calcium channel subtypes in isoflurane inhibition of synaptic vesicle exocytosis in rat hippocampal neurones. British Journal of Anaesthesia, 123(2), 219-227.
Landau, A. T., Pojeong, P., David Wong-Campos, J., He, T., Cohen, A. E., & Sabatini, B. L. (2022). Dendritic branch structure compartmentalizes voltage-dependent calcium influx in cortical layer 2/3 pyramidal cells. eLife, 11, e76993. https://doi.org/10.7554/eLife.76993
Larter, R., & Craig, M. G. (2005). Glutamate-induced glutamate release: A proposed mechanism for calcium bursting in astrocytes. Chaos, 15(4), 047511.
Li, Y. X., & Rinzel, J. (1994). Equations for InsP3 receptor-mediated [Ca2+]i oscillations derived from a detailed kinetic model: A Hodgkin-Huxley like formalism. Journal of Theoretical Biology, 166(4), 461-473.
Linaro, D., Levy, M. J., & Hunt, D. L. (2022). Cell type-specific mechanisms of information transfer in data-driven biophysical models of hippocampal CA3 principal neurons. PLoS Computational Biology, 18(4), e1010071.
Lopez, J. R., Kolster, J., Uryash, A., Estève, E., Altamirano, F., & Adams, J. A. (2018). Dysregulation of intracellular Ca2+ in dystrophic cortical and hippocampal neurons. Molecular Neurobiology, 55(1), 603-618.
Ludewig, S., Herrmann, U., Michaelsen-Preusse, K., Metzdorf, K., Just, J., Bold, C., Müller, U. C., & Korte, M. (2021). APPsα rescues impaired Ca2+ homeostasis in APP- and APLP2-deficient hippocampal neurons. Proceedings of the National Academy of Sciences of the United States of America, 118(26), e2011506118.
Ma, J., Mengmeng, D., Wang, R., & Ying, W. (2016). Dynamic transition of neuronal firing induced by abnormal astrocytic glutamate oscillation. Scientific Reports, 6(1), 32343. https://doi.org/10.1038/srep32343
Magee, J. C., & Carruth, M. (1999). Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. Journal of Neurophysiology, 82(4), 1895-1901.
Malci, A., Lin, X., Sandoval, R., Gundelfinger, E. D., Naumann, M., Seidenbecher, C. I., & Herrera-Molina, R. (2022). Ca2+ signaling in postsynaptic neurons: Neuroplastin-65 regulates the interplay between plasma membrane Ca2+ ATPases and ionotropic glutamate receptors. Cell Calcium, 106, 102623.
Matrosov, V., Gordleeva, S., Boldyreva, N., Ben-Jacob, E., Kazantsev, V., & de Pittà, M. (2019). Emergence of regular and complex calcium oscillations by inositol 1,4,5-trisphosphate signaling in astrocytes Springer series in computational neuroscience (pp. 151-176). Springer International Publishing.
Mirzakhalili, E., Epureanu, B. I., & Gourgou, E. (2018). A mathematical and computational model of the calcium dynamics in Caenorhabditis Elegans ASH sensory neuron. PLoS One, 13(7), e0201302.
Mölter, J., Avitan, L., & Goodhill, G. J. (2018). Detecting neural assemblies in calcium imaging data. BMC Biology, 16(1), 143.
Muldoon, F., Sarah, I. S., & Cossart, R. (2013). Spatially clustered neuronal assemblies comprise the microstructure of synchrony in chronically epileptic networks. Proceedings of the National Academy of Sciences of the United States of America, 110(9), 3567-3572.
Kondo, M., Kobayashi, K., Ohkura, M., Nakai, J., & Matsuzaki, M. (2017). Two-photon calcium imaging of the medial prefrontal cortex and hippocampus without cortical invasion. eLife, 6, e26839. https://doi.org/10.7554/eLife.26839
Nadkarni, S., & Jung, P. (2007). Modeling synaptic transmission of the tripartite synapse. Physical Biology, 4(1), 1-9.
Nakade, S., Rhee, S. K., Hamanaka, H., & Mikoshiba, K. (1994). Cyclic AMP-dependent phosphorylation of an Immunoaffinity-purified Homotetrameric inositol 1,4,5-trisphosphate receptor (type I) increases Ca2+ flux in reconstituted lipid vesicles. The Journal of Biological Chemistry, 269(9), 6735-6742.
Nault, F., & de Koninck, P. (2009). Dissociated hippocampal cultures Springer protocols handbooks (pp. 137-159). Humana Press.
Okujeni, S., Kandler, S., & Egert, U. (2017). Mesoscale architecture shapes initiation and richness of spontaneous network activity. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 37(14), 3972-3987.
O'Leary, T., Williams, A. H., Caplan, J. S., & Marder, E. (2013). Correlations in Ion Channel expression emerge from homeostatic tuning rules. Proceedings of the National Academy of Sciences of the United States of America, 110(28), E2645-E2654.
Pandey, G. N., Dwivedi, Y., SridharaRao, J., Ren, X., Janicak, P. G., & Sharma, R. (2002). Protein kinase C and phospholipase C activity and expression of their specific isozymes is decreased and expression of MARCKS is increased in platelets of bipolar but not in unipolar patients. Neuropsychopharmacology, 26(2), 216-228.
Patoary, M. N., Ishlam, C. T., McDougal, R. A., Lin, Z., & Lytton, W. W. (2019). Parallel stochastic discrete event simulation of calcium dynamics in neuron. IEEE/ACM Transactions on Computational Biology and Bioinformatics, 16(3), 1007-1019.
Pinheiro, P. S., & Mulle, C. (2008). Presynaptic glutamate receptors: Physiological functions and mechanisms of action. Nature Reviews. Neuroscience, 9(6), 423-436.
Pinsky, P. F., & Rinzel, J. (1994). Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons. Journal of Computational Neuroscience, 1(1-2), 39-60.
Podestá, M. F., Yam, P., Codagnone, M. G., Uccelli, N. A., Colman, D., & Reinés, A. (2014). Distinctive PSA-NCAM and NCAM hallmarks in glutamate-induced dendritic atrophy and synaptic disassembly. PLoS One, 9(10), e108921.
Ramírez, O. A., & Couve, A. (2011). The endoplasmic reticulum and protein trafficking in dendrites and axons. Trends in Cell Biology, 21(4), 219-227.
Rüdiger, S., & Shuai, J. (2019). Modeling of stochastic $$\mathrmca^2+$$ signals Springer series in computational neuroscience (pp. 91-114). Springer International Publishing.
Samtleben, S., Wachter, B., & Blum, R. (2015). Store-operated calcium entry compensates fast ER calcium loss in resting hippocampal neurons. Cell Calcium, 58(2), 147-159.
Saxena, A., Ravutla, S., Upadhyay, V., Jana, S., Murhammer, D., & Giri, L. (2020). Statistical modeling of cell-to-cell variability in viral infection during passaging in suspension cell culture: Application in Monte-Carlo simulation. Biotechnology and Bioengineering, 117(5), 1483-1501.
Schlick, B., Flucher, B. E., & Obermair, G. J. (2010). Voltage-activated Calcium Channel expression profiles in mouse brain and cultured hippocampal neurons. Neuroscience, 167(3), 786-798.
Shuai, J.-W., & Jung, P. (2002). Stochastic properties of Ca(2+) release of inositol 1,4,5-trisphosphate receptor clusters. Biophysical Journal, 83(1), 87-97.
Sugawara, Y., Echigo, R., Kashima, K., Minami, H., Watanabe, M., Nishikawa, Y., Muranishi, M., Yoneda, M., & Ohno-Shosaku, T. (2013). Intracellular calcium level is an important factor influencing ion channel modulations by PLC-coupled metabotropic receptors in hippocampal neurons. Brain Research, 1512, 9-21.
Swain, S., Gupta, R. K., Ratnayake, K., Priyanka, P. D., Singh, R., Jana, S., Mitra, K., Karunarathne, A., & Giri, L. (2018). Confocal imaging and K-means clustering of GABAB and MGluR mediated modulation of Ca2+ spiking in hippocampal neurons. ACS Chemical Neuroscience, 9(12), 3094-3107.
Taheri, M., Handy, G., Borisyuk, A., & White, J. A. (2017). Diversity of evoked astrocyte Ca2+ dynamics quantified through experimental measurements and mathematical modeling. Frontiers in Systems Neuroscience, 11, 79.
Tedoldi, A., Ludwig, P., Fulgenzi, G., Takeshima, H., Pedarzani, P., & Stocker, M. (2020). Calcium-induced calcium release and type 3 ryanodine receptors modulate the slow Afterhyperpolarising current, SIAHP, and its potentiation in hippocampal pyramidal neurons. PLoS One, 15(6), e0230465.
Toivari, E., Manninen, T., Nahata, A. K., Jalonen, T. O., & Linne, M.-L. (2011). Effects of transmitters and amyloid-Beta peptide on calcium signals in rat cortical astrocytes: Fura-2AM measurements and stochastic model simulations. PLoS One, 6(3), e17914.
Venkataramani, V., Tanev, D. I., Strahle, C., Studier-Fischer, A., Fankhauser, L., Kessler, T., Körber, C., Kardorff, M., Ratliff, M., Xie, R., Horstmann, H., Messer, M., Paik, S. P., Knabbe, J., Sahm, F., Kurz, F. T., Acikgöz, A. A., Herrmannsdörfer, F., Agarwal, A., … Kuner, T. (2019). Glutamatergic synaptic input to glioma cells drives brain tumour progression. Nature, 573(7775), 532-538.
Venkateswarlu, K., Suman, G., Dhyani, V., Swain, S., Giri, L., & Samavedi, S. (2020). Three-dimensional imaging and quantification of real-time cytosolic calcium oscillations in microglial cells cultured on electrospun matrices using laser scanning confocal microscopy. Biotechnology and Bioengineering, 117(10), 3108-3123.
Verisokin, A. Y., Verveyko, D. V., Postnov, D. E., & Brazhe, A. R. (2021). Modeling of astrocyte networks: Toward realistic topology and dynamics. Frontiers in Cellular Neuroscience, 15, 645068.
Vizi, E. S., Fekete, A., Karoly, R., & Mike, A. (2010). Non-synaptic receptors and transporters involved in brain functions and targets of drug treatment. British Journal of Pharmacology, 160(4), 785-809.
Williams, C. L., & Smith, S. M. (2018). Calcium dependence of spontaneous neurotransmitter release. Journal of Neuroscience Research, 96(3), 335-347.
Yao, J., Pilko, A., & Wollman, R. (2016). Distinct cellular states determine calcium signaling response. Molecular Systems Biology, 12(12), 894.
Yoshizumi, M., Eisenach, J. C., & Hayashida, K.-I. (2012). Riluzole and Gabapentinoids activate glutamate transporters to facilitate glutamate-induced glutamate release from cultured astrocytes. European Journal of Pharmacology, 677(1-3), 87-92.
Zeng, S., Li, B., Zeng, S., & Chen, S. (2009). Simulation of spontaneous Ca2+ oscillations in astrocytes mediated by voltage-gated calcium channels. Biophysical Journal, 97(9), 2429-2437.
Zhou, Q., Godwin, D. W., O'Malley, D. M., & Adams, P. R. (1997). Visualization of calcium influx through channels that shape the burst and tonic firing modes of thalamic relay cells. Journal of Neurophysiology, 77(5), 2816-2825.