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


Journal

Nature neuroscience
ISSN: 1546-1726
Titre abrégé: Nat Neurosci
Pays: United States
ID NLM: 9809671

Informations de publication

Date de publication:
09 2023
Historique:
received: 07 06 2020
accepted: 13 07 2023
medline: 4 9 2023
pubmed: 1 9 2023
entrez: 31 8 2023
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 37653166
doi: 10.1038/s41593-023-01405-5
pii: 10.1038/s41593-023-01405-5
doi:

Substances chimiques

Calcium SY7Q814VUP

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1555-1565

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature America, Inc.

Références

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).
pubmed: 34293296 pmcid: 7611560
Cossart, R. & Garel, S. Step by step: cells with multiple functions in cortical circuit assembly. Nat. Rev. Neurosci. 23, 395–410 (2022).
pubmed: 35422526
Reh, R. K. et al. Critical period regulation across multiple timescales. Proc. Natl Acad. Sci. USA 117, 23242–23251 (2020).
pubmed: 32503914 pmcid: 7519216
Luhmann, H. J. & Khazipov, R. Neuronal activity patterns in the developing barrel cortex. Neuroscience 368, 256–267 (2017).
pubmed: 28528963
Bonifazi, P. et al. GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science 326, 1419–1424 (2009).
pubmed: 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).
pubmed: 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).
pubmed: 21867885 pmcid: 3163067
Khazipov, R. et al. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432, 758–761 (2004).
pubmed: 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).
pubmed: 32413304 pmcid: 7314650
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).
pubmed: 22442068 pmcid: 3333790
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).
pubmed: 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).
pubmed: 30618626 pmcid: 6304748
Papagiakoumou, E., Sars, V., de, Oron, D. & Emiliani, V. Patterned two-photon illumination by spatiotemporal shaping of ultrashort pulses. Opt. Express 16, 22039 (2008).
pubmed: 19104638
Lutz, C. et al. Holographic photolysis of caged neurotransmitters. Nat. Methods 5, 821–827 (2008).
pubmed: 19160517 pmcid: 2711023
Landers, M. & Zeigler, H. P. Development of rodent whisking: trigeminal input and central pattern generation. Somatosens. Mot. Res. 23, 1–10 (2006).
pubmed: 16846954
Pnevmatikakis, E. A. et al. Simultaneous denoising, deconvolution, and demixing of calcium imaging data. Neuron 89, 285–299 (2016).
pubmed: 26774160 pmcid: 4881387
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).
pubmed: 34341584 pmcid: 7611618
Melzer, S. et al. Long-range-projecting GABAergic neurons modulate inhibition in hippocampus and entorhinal cortex. Science 335, 1506–1510 (2012).
pubmed: 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).
pubmed: 20023653 pmcid: 2840225
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).
pubmed: 17548818 pmcid: 1891224
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).
pubmed: 23986241 pmcid: 3756753
Yu, S., Huang, D., Singer, W. & Nikolić, D. A small world of neuronal synchrony. Cereb. Cortex 18, 2891–2901 (2008).
pubmed: 18400792 pmcid: 2583154
Broido, A. D. & Clauset, A. Scale-free networks are rare. Nat. Commun. 10, 1017 (2019).
pubmed: 30833554 pmcid: 6399239
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).
pubmed: 19726647 pmcid: 2771734
Sridharan, S. et al. High-performance microbial opsins for spatially and temporally precise perturbations of large neuronal networks. Neuron 110, 1139–1155 (2022).
pubmed: 35120626 pmcid: 8989680
Tuncdemir, S. N. et al. Early somatostatin interneuron connectivity mediates the maturation of deep layer cortical circuits. Neuron 89, 521–535 (2016).
pubmed: 26844832 pmcid: 4861073
Marques-Smith, A. et al. A transient translaminar GABAergic interneuron circuit connects thalamocortical recipient layers in neonatal somatosensory cortex. Neuron 89, 536–549 (2016).
pubmed: 26844833 pmcid: 4742537
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).
pubmed: 17928435 pmcid: 6672847
Chettih, S. N. & Harvey, C. D. Single-neuron perturbations reveal feature-specific competition in V1. Nature 567, 334–340 (2019).
pubmed: 30842660 pmcid: 6682407
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).
pubmed: 32320944 pmcid: 8006069
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).
pubmed: 31257030 pmcid: 6747687
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).
pubmed: 25402854 pmcid: 4459599
Robinson, N. T. M. et al. Targeted activation of hippocampal place cells drives memory-guided spatial behavior. Cell 183, 2041–2042 (2020).
pubmed: 33357402 pmcid: 7773032
Okada, T. et al. Pain induces stable, active microcircuits in the somatosensory cortex that provide a therapeutic target. Sci. Adv. 7, eabd8261 (2021).
pubmed: 33741588 pmcid: 7978434
Wrosch, J. K. et al. Rewiring of neuronal networks during synaptic silencing. Sci. Rep. 7, 11724 (2017).
pubmed: 28916806 pmcid: 5601899
Bocchio, M. et al. Hippocampal hub neurons maintain distinct connectivity throughout their lifetime. Nat. Commun. 11, 4559 (2020).
pubmed: 32917906 pmcid: 7486410
Kaiser, M. Mechanisms of connectome development. Trends Cogn. Sci. 21, 703–717 (2017).
pubmed: 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).
pubmed: 29089360 pmcid: 5702067
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).
pubmed: 30388120 pmcid: 6235603
Kirmse, K. et al. GABA depolarizes immature neurons and inhibits network activity in the neonatal neocortex in vivo. Nat. Commun. 6, 7750 (2015).
pubmed: 26177896
Murata, Y. & Colonnese, M. T. GABAergic interneurons excite neonatal hippocampus in vivo. Sci. Adv. 6, eaba1430 (2020).
pubmed: 32582852 pmcid: 7292633
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).
pubmed: 27803649 pmcid: 5067533
Ronzitti, E. et al. Submillisecond optogenetic control of neuronal firing with two-photon holographic photoactivation of Chronos. J. Neurosci. 37, 10679–10689 (2017).
pubmed: 28972125 pmcid: 5666587
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).
pubmed: 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).
pubmed: 28782629
Guizar-Sicairos, M., Thurman, S. T. & Fienup, J. R. Efficient subpixel image registration algorithms. Opt. Lett. 33, 156–158 (2008).
pubmed: 18197224
Rubinov, M. & Sporns, O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52, 1059–1069 (2010).
pubmed: 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).

Auteurs

Yannick Bollmann (Y)

Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France.

Laura Modol (L)

Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France.

Thomas Tressard (T)

Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France.

Artem Vorobyev (A)

Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France.

Robin Dard (R)

Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France.

Sophie Brustlein (S)

Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France.

Ruth Sims (R)

Wavefront-Engineering Microscopy Group, Photonics Department, Vision Institute, Sorbonne University, INSERM, CNRS, Paris, France.

Imane Bendifallah (I)

Wavefront-Engineering Microscopy Group, Photonics Department, Vision Institute, Sorbonne University, INSERM, CNRS, Paris, France.

Erwan Leprince (E)

Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France.

Vincent de Sars (V)

Wavefront-Engineering Microscopy Group, Photonics Department, Vision Institute, Sorbonne University, INSERM, CNRS, Paris, France.

Emiliano Ronzitti (E)

Wavefront-Engineering Microscopy Group, Photonics Department, Vision Institute, Sorbonne University, INSERM, CNRS, Paris, France.

Agnès Baude (A)

Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France.

Hillel 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.

Michel Aimé Picardo (MA)

Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France.

Jean-Claude Platel (JC)

Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France.

Valentina Emiliani (V)

Wavefront-Engineering Microscopy Group, Photonics Department, Vision Institute, Sorbonne University, INSERM, CNRS, Paris, France.

David Angulo-Garcia (D)

Departamento de Matemáticas y Estadística, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Colombia, Manizales, Colombia.

Rosa Cossart (R)

Aix Marseille Univ, Inserm, INMED, Turing Center for Living Systems, Marseille, France. rosa.cossart@inserm.fr.

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