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Prominent in vivo influence of single interneurons in the developing barrel cortex.

التفاصيل البيبلوغرافية
العنوان: Prominent in vivo influence of single interneurons in the developing barrel cortex.
المؤلفون: Bollmann Y; Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France., Modol L; Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France., Tressard T; Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France., Vorobyev A; Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France., Dard R; Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France., Brustlein S; Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France., Sims R; Wavefront-Engineering Microscopy Group, Photonics Department, Vision Institute, Sorbonne University, INSERM, CNRS, Paris, France., Bendifallah I; Wavefront-Engineering Microscopy Group, Photonics Department, Vision Institute, Sorbonne University, INSERM, CNRS, Paris, France., Leprince E; Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France., de Sars V; Wavefront-Engineering Microscopy Group, Photonics Department, Vision Institute, Sorbonne University, INSERM, CNRS, Paris, France., Ronzitti E; Wavefront-Engineering Microscopy Group, Photonics Department, Vision Institute, Sorbonne University, INSERM, CNRS, Paris, France., Baude A; Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France., Adesnik H; Department of Molecular & Cell Biology, University of California, Berkeley, Berkeley, CA, USA.; Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA, USA., Picardo MA; Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France., Platel JC; Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France., Emiliani V; Wavefront-Engineering Microscopy Group, Photonics Department, Vision Institute, Sorbonne University, INSERM, CNRS, Paris, France., Angulo-Garcia D; Departamento de Matemáticas y Estadística, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Colombia, Manizales, Colombia., Cossart R; Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France. rosa.cossart@inserm.fr.
المصدر: Nature neuroscience [Nat Neurosci] 2023 Sep; Vol. 26 (9), pp. 1555-1565. Date of Electronic Publication: 2023 Aug 31.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: United States NLM ID: 9809671 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1546-1726 (Electronic) Linking ISSN: 10976256 NLM ISO Abbreviation: Nat Neurosci Subsets: MEDLINE
أسماء مطبوعة: Publication: <2002->: New York, NY : Nature Publishing Group
Original Publication: New York, NY : Nature America Inc., c1998-
مواضيع طبية MeSH: Endocrine Glands* , Holography*, Animals ; Mice ; Interneurons ; Calcium ; GABAergic Neurons
مستخلص: Spontaneous synchronous activity is a hallmark of developing brain circuits and promotes their formation. Ex vivo, synchronous activity was shown to be orchestrated by a sparse population of highly connected GABAergic 'hub' neurons. The recent development of all-optical methods to record and manipulate neuronal activity in vivo now offers the unprecedented opportunity to probe the existence and function of hub cells in vivo. Using calcium imaging, connectivity analysis and holographic optical stimulation, we show that single GABAergic, but not glutamatergic, neurons influence population dynamics in the barrel cortex of non-anaesthetized mouse pups. Single GABAergic cells mainly exert an inhibitory influence on both spontaneous and sensory-evoked population bursts. Their network influence scales with their functional connectivity, with highly connected hub neurons displaying the strongest impact. We propose that hub neurons function in tailoring intrinsic cortical dynamics to external sensory inputs.
(© 2023. The Author(s), under exclusive licence to Springer Nature America, Inc.)
References: Martini, F. J., Guillamón-Vivancos, T., Moreno-Juan, V., Valdeolmillos, M. & López-Bendito, G. Spontaneous activity in developing thalamic and cortical sensory networks. Neuron 109, 2519–2534 (2021). (PMID: 342932967611560)
Cossart, R. & Garel, S. Step by step: cells with multiple functions in cortical circuit assembly. Nat. Rev. Neurosci. 23, 395–410 (2022). (PMID: 35422526)
Reh, R. K. et al. Critical period regulation across multiple timescales. Proc. Natl Acad. Sci. USA 117, 23242–23251 (2020). (PMID: 325039147519216)
Luhmann, H. J. & Khazipov, R. Neuronal activity patterns in the developing barrel cortex. Neuroscience 368, 256–267 (2017). (PMID: 28528963)
Bonifazi, P. et al. GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science 326, 1419–1424 (2009). (PMID: 19965761)
Mòdol, L. et al. Spatial embryonic origin delineates GABAergic hub neurons driving network dynamics in the developing entorhinal cortex. Cereb. Cortex 27, 4649–4661 (2017). (PMID: 28922859)
Feldt, S., Bonifazi, P. & Cossart, R. Dissecting functional connectivity of neuronal microcircuits: experimental and theoretical insights. Trends Neurosci. 34, 225–236 (2011).
Picardo, M. A., Guigue, P., Allene, C. & Fishell, G. Pioneer GABA cells comprise a subpopulation of hub neurons in the developing hippocampus. Neuron 71, 695–709 (2011). (PMID: 218678853163067)
Khazipov, R. et al. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432, 758–761 (2004). (PMID: 15592414)
Dooley, J. C., Glanz, R. M., Sokoloff, G. & Blumberg, M. S. Self-generated whisker movements drive state-dependent sensory input to developing barrel cortex. Curr. Biol. 30, 2404–2410 (2020). (PMID: 324133047314650)
Dzhala, V., Valeeva, G., Glykys, J., Khazipov, R. & Staley, K. Traumatic alterations in GABA signaling disrupt hippocampal network activity in the developing brain. J. Neurosci. 32, 4017–4031 (2012). (PMID: 224420683333790)
Carrillo-Reid, L., Yang, W., Miller, J.-E. K., Peterka, D. S. & Yuste, R. Imaging and optically manipulating neuronal ensembles. Annu. Rev. Biophys. 46, 271–293 (2017). (PMID: 28301770)
Packer, A. M., Russell, L. E., Dalgleish, H. W. P. & Häusser, M. Simultaneous all-optical manipulation and recording of neural circuit activity with cellular resolution in vivo. Nat. Methods 12, 140–146 (2014).
Mardinly, A. R. et al. Precise multimodal optical control of neural ensemble activity. Nat. Neurosci. 21, 881–893 (2018).
Ronzitti, E., Emiliani, V. & Papagiakoumou, E. Methods for three-dimensional all-optical manipulation of neural circuits. Front. Cell. Neurosci. 12, 469 (2018). (PMID: 306186266304748)
Papagiakoumou, E., Sars, V., de, Oron, D. & Emiliani, V. Patterned two-photon illumination by spatiotemporal shaping of ultrashort pulses. Opt. Express 16, 22039 (2008). (PMID: 19104638)
Lutz, C. et al. Holographic photolysis of caged neurotransmitters. Nat. Methods 5, 821–827 (2008). (PMID: 191605172711023)
Landers, M. & Zeigler, H. P. Development of rodent whisking: trigeminal input and central pattern generation. Somatosens. Mot. Res. 23, 1–10 (2006). (PMID: 16846954)
Pnevmatikakis, E. A. et al. Simultaneous denoising, deconvolution, and demixing of calcium imaging data. Neuron 89, 285–299 (2016). (PMID: 267741604881387)
Rupprecht, P. et al. A database and deep learning toolbox for noise-optimized, generalized spike inference from calcium imaging. Nat. Neurosci. 24, 1324–1337 (2021). (PMID: 343415847611618)
Melzer, S. et al. Long-range-projecting GABAergic neurons modulate inhibition in hippocampus and entorhinal cortex. Science 335, 1506–1510 (2012). (PMID: 22442486)
Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133–140 (2009). (PMID: 200236532840225)
Clauset, A., Shalizi, C. R. & Newman, M. E. J. Power-law distributions in empirical data. SIAM Rev. 51, 661–703 (2009).
Honey, C. J., Kötter, R., Breakspear, M. & Sporns, O. Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc. Natl Acad. Sci. USA 104, 10240–10245 (2007). (PMID: 175488181891224)
Sadovsky, A. J. & MacLean, J. N. Scaling of topologically similar functional modules defines mouse primary auditory and somatosensory microcircuitry. J. Neurosci. 33, 14048–14060 (2013). (PMID: 239862413756753)
Yu, S., Huang, D., Singer, W. & Nikolić, D. A small world of neuronal synchrony. Cereb. Cortex 18, 2891–2901 (2008). (PMID: 184007922583154)
Broido, A. D. & Clauset, A. Scale-free networks are rare. Nat. Commun. 10, 1017 (2019). (PMID: 308335546399239)
Das, A. & Fiete, I. R. Systematic errors in connectivity inferred from activity in strongly recurrent networks. Nat. Neurosci. 500, 1–34 (2020).
Mòdol, L. et al. Assemblies of perisomatic GABAergic neurons in the developing barrel cortex. Neuron 105, 93–105 (2019).
Golshani, P. et al. Internally mediated developmental desynchronization of neocortical network activity. J. Neurosci. 29, 10890–10899 (2009). (PMID: 197266472771734)
Sridharan, S. et al. High-performance microbial opsins for spatially and temporally precise perturbations of large neuronal networks. Neuron 110, 1139–1155 (2022). (PMID: 351206268989680)
Tuncdemir, S. N. et al. Early somatostatin interneuron connectivity mediates the maturation of deep layer cortical circuits. Neuron 89, 521–535 (2016). (PMID: 268448324861073)
Marques-Smith, A. et al. A transient translaminar GABAergic interneuron circuit connects thalamocortical recipient layers in neonatal somatosensory cortex. Neuron 89, 536–549 (2016). (PMID: 268448334742537)
Fogarty, M. et al. Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J. Neurosci. 27, 10935–10946 (2007). (PMID: 179284356672847)
Chettih, S. N. & Harvey, C. D. Single-neuron perturbations reveal feature-specific competition in V1. Nature 567, 334–340 (2019). (PMID: 308426606682407)
Carrillo-Reid, L. & Yuste, R. Playing the piano with the cortex: role of neuronal ensembles and pattern completion in perception and behavior. Curr. Opin. Neurobiol. 64, 89–95 (2020). (PMID: 323209448006069)
Carrillo-Reid, L., Han, S., Yang, W., Akrouh, A. & Yuste, R. Controlling visually guided behavior by holographic recalling of cortical ensembles. Cell 178, 447–457 (2019). (PMID: 312570306747687)
Marshel, J. H. et al. Cortical layer-specific critical dynamics triggering perception. Science 365, eaaw5202 (2019).
Rickgauer, J. P., Deisseroth, K. & Tank, D. W. Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields. Nat. Neurosci. 17, 1816–1824 (2014). (PMID: 254028544459599)
Robinson, N. T. M. et al. Targeted activation of hippocampal place cells drives memory-guided spatial behavior. Cell 183, 2041–2042 (2020). (PMID: 333574027773032)
Okada, T. et al. Pain induces stable, active microcircuits in the somatosensory cortex that provide a therapeutic target. Sci. Adv. 7, eabd8261 (2021). (PMID: 337415887978434)
Wrosch, J. K. et al. Rewiring of neuronal networks during synaptic silencing. Sci. Rep. 7, 11724 (2017). (PMID: 289168065601899)
Bocchio, M. et al. Hippocampal hub neurons maintain distinct connectivity throughout their lifetime. Nat. Commun. 11, 4559 (2020). (PMID: 329179067486410)
Kaiser, M. Mechanisms of connectome development. Trends Cogn. Sci. 21, 703–717 (2017). (PMID: 28610804)
Hu, J. S., Vogt, D., Sandberg, M. & Rubenstein, J. L. Cortical interneuron development: a tale of time and space. Development 144, 3867–3878 (2017). (PMID: 290893605702067)
Wang, C.-Z. et al. Early-generated interneurons regulate neuronal circuit formation during early postnatal development. eLife 8, 333 (2019).
García, N. V. D. M., Karayannis, T. & Fishell, G. Neuronal activity is required for the development of specific cortical interneuron subtypes. Nature 472, 351–355 (2011).
Luccioli, S. et al. Modeling driver cells in developing neuronal networks. PLoS Comput. Biol. 14, e1006551 (2018). (PMID: 303881206235603)
Kirmse, K. et al. GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo. Nat. Commun. 6, 7750 (2015). (PMID: 26177896)
Murata, Y. & Colonnese, M. T. GABAergic interneurons excite neonatal hippocampus in vivo. Sci. Adv. 6, eaba1430 (2020). (PMID: 325828527292633)
Steinmetz, N. A. et al. Aberrant cortical activity in multiple GCaMP6-expressing transgenic mouse lines. eNeuro 4, ENEURO.0207–17.2017 (2017).
Golshani, P. & Portera-Cailliau, C. In vivo 2-photon calcium imaging in layer 2/3 of mice. J. Vis. Exp. 681 (2008).
Chaigneau, E. et al. Two-photon holographic stimulation of ReaChR. Front. Cell. Neurosci. 10, 234 (2016). (PMID: 278036495067533)
Ronzitti, E. et al. Submillisecond optogenetic control of neuronal firing with two-photon holographic photoactivation of Chronos. J. Neurosci. 37, 10679–10689 (2017). (PMID: 289721255666587)
Chen, I.-W. et al. In vivo sub-millisecond two-photon optogenetics with temporally focused patterned light. J. Neurosci. 39, 3484–3497 (2019).
Hernandez, O., Guillon, M., Papagiakoumou, E. & Emiliani, V. Zero-order suppression for two-photon holographic excitation. Opt. Lett. 39, 5953–5956 (2014). (PMID: 25361128)
Pnevmatikakis, E. A. & Giovannucci, A. NoRMCorre: an online algorithm for piecewise rigid motion correction of calcium imaging data. J. Neurosci. Methods 291, 83–94 (2017). (PMID: 28782629)
Guizar-Sicairos, M., Thurman, S. T. & Fienup, J. R. Efficient subpixel image registration algorithms. Opt. Lett. 33, 156–158 (2008). (PMID: 18197224)
Rubinov, M. & Sporns, O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52, 1059–1069 (2010). (PMID: 19819337)
Gillespie, C. S. Fitting heavy tailed distributions: the poweRlaw package. J. Stat. Softw. 64, 1–16 (2015).
Rodrigues, F. A., Peron, T. K. D., Ji, P. & Kurths, J. The Kuramoto model in complex networks. Phys. Rep. 610, 1–98 (2016).
المشرفين على المادة: SY7Q814VUP (Calcium)
تواريخ الأحداث: Date Created: 20230831 Date Completed: 20230904 Latest Revision: 20230926
رمز التحديث: 20231215
DOI: 10.1038/s41593-023-01405-5
PMID: 37653166
قاعدة البيانات: MEDLINE
الوصف
تدمد:1546-1726
DOI:10.1038/s41593-023-01405-5