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Serotonin sensing by microglia conditions the proper development of neuronal circuits and of social and adaptive skills

Molecular Psychiatry (2023)Cite this article

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Abstract

The proper maturation of emotional and sensory circuits requires fine-tuning of serotonin (5-HT) level during early postnatal development. Consistently, dysfunctions of the serotonergic system have been associated with neurodevelopmental psychiatric diseases, including autism spectrum disorders (ASD). However, the mechanisms underlying the developmental effects of 5-HT remain partially unknown, one obstacle being the action of 5-HT on different cell types. Here, we focused on microglia, which play a role in brain wiring refinement, and we investigated whether the control of these cells by 5-HT is relevant for neurodevelopment and spontaneous behaviors in mice. Since the main 5-HT sensor in microglia is the 5-HT2B receptor subtype, we prevented 5-HT signaling specifically in microglia by conditional invalidation of the Htr2b gene in these cells. We observed that abrogating the serotonergic control of microglia during early postnatal development affects the phagolysosomal compartment of these cells and their proximity to dendritic spines and perturbs neuronal circuits maturation. Furthermore, this early ablation of microglial 5-HT2B receptors leads to adult hyperactivity in a novel environment and behavioral defects in sociability and flexibility. Importantly, we show that these behavioral alterations result from a developmental effect, since they are not observed when microglial Htr2b invalidation is induced later, at P30 onward. Thus, a primary alteration of 5-HT sensing in microglia, during a critical time window between birth and P30, is sufficient to impair social and flexibility skills. This link between 5-HT and microglia may explain the association between serotonergic dysfunctions and behavioral traits like impaired sociability and inadaptability to novelty, which are prominent in psychiatric disorders such as ASD.

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Fig. 1: Absence of 5-HT2B receptors in neonatal microglia decreases their lysosome content, alters their morphology, and impacts the synapse-microglia proximity in the developing hippocampus (CA1).
Fig. 2: Absence of 5-HT2B receptors in microglia since birth impairs neuronal circuits refinement in the developing hippocampus and thalamus.
Fig. 3: Absence of 5-HT2B receptors in microglia since birth impacts activity in a novel environment, sociability and flexibility in male mice.
Fig. 4: Absence of 5-HT2B receptors in microglia since birth impacts activity in a novel environment, sociability and flexibility in female mice.
Fig. 5: Ablation of 5-HT2B receptors in microglia at P30 does not alter spontaneous behaviors in adult male mice.

References

  1. Thion MS, Ginhoux F, Garel S. Microglia and early brain development: An intimate journey. Science. 2018;362:185–9.

    Article  CAS  PubMed  Google Scholar 

  2. Conio B, Martino M, Magioncalda P, Escelsior A, Inglese M, Amore M, et al. Opposite effects of dopamine and serotonin on resting-state networks: review and implications for psychiatric disorders. Mol Psychiatry. 2020;25:82–93.

    Article  PubMed  Google Scholar 

  3. Lin S-H, Lee L-T, Yang YK. Serotonin and mental disorders: A concise review on molecular neuroimaging evidence. Clin Psychopharmacol Neurosci. 2014;12:196–202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Marazziti D. Understanding the role of serotonin in psychiatric diseases. F1000Res. 2017;6:180.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Anderson GM, Horne WC, Chatterjee D, Cohen DJ. The Hyperserotonemia of Autism. Ann NY Acad Sci. 1990;600:331–40.

    Article  CAS  PubMed  Google Scholar 

  6. Gabriele S, Sacco R, Persico AM. Blood serotonin levels in autism spectrum disorder: a systematic review and meta-analysis. Eur Neuropsychopharmacol. 2014;24:919–29.

    Article  CAS  PubMed  Google Scholar 

  7. Migliarini S, Pacini G, Pelosi B, Lunardi G, Pasqualetti M. Lack of brain serotonin affects postnatal development and serotonergic neuronal circuitry formation. Mol Psychiatry. 2013;18:1106–18.

    Article  CAS  PubMed  Google Scholar 

  8. Witteveen JS, Middelman A, van Hulten JA, Martens GJM, Homberg JR, Kolk SM. Lack of serotonin reuptake during brain development alters rostral raphe-prefrontal network formation. Front Cell Neurosci. 2013;7:143.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Teissier A, Soiza-Reilly M, Gaspar P. Refining the Role of 5-HT in postnatal development of brain circuits. Front Cell Neurosci. 2017;11:139.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Kolodziejczak M, Béchade C, Gervasi N, Irinopoulou T, Banas SM, Cordier C, et al. Serotonin modulates developmental Microglia via 5-HT 2B Receptors: Potential implication during synaptic refinement of retinogeniculate projections. ACS Chem Neurosci. 2015;6:1219–30.

    Article  CAS  PubMed  Google Scholar 

  11. Krabbe G, Matyash V, Pannasch U, Mamer L, Boddeke HWGM, Kettenmann H. Activation of serotonin receptors promotes microglial injury-induced motility but attenuates phagocytic activity. Brain, Behav Immunity. 2012;26:419–28.

    Article  CAS  Google Scholar 

  12. Béchade C, D’Andrea I, Etienne F, Verdonk F, Moutkine I, Banas SM, et al. The serotonin 2B receptor is required in neonatal microglia to limit neuroinflammation and sickness behavior in adulthood. Glia. 2021;69:638–54.

    Article  PubMed  Google Scholar 

  13. Etienne F, Mastrolia V, Maroteaux L, Girault J-A, Gervasi N, Roumier A. Two-photon imaging of microglial processes’ attraction toward ATP or serotonin in acute brain slices. JoVE. 2019;143:e58788.

    Google Scholar 

  14. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, et al. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron. 2012;74:691–705.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Upton AL, Salichon N, Lebrand C, Ravary A, Blakely R, Seif I, et al. Excess of Serotonin (5-HT) Alters the Segregation of Ispilateral and Contralateral Retinal Projections in Monoamine Oxidase A Knock-Out Mice: Possible Role of 5-HT Uptake in Retinal Ganglion Cells During Development. J Neurosci. 1999;19:7007–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Gaspar P, Cases O, Maroteaux L. The developmental role of serotonin: news from mouse molecular genetics. Nat Rev Neurosci. 2003;4:1002–12.

    Article  CAS  PubMed  Google Scholar 

  17. Pitychoutis PM, Belmer A, Moutkine I, Adrien J, Maroteaux L. Mice Lacking the Serotonin Htr2B Receptor Gene Present an Antipsychotic-Sensitive Schizophrenic-Like Phenotype. Neuropsychopharmacol. 2015;40:2764–73.

    Article  CAS  Google Scholar 

  18. Diaz SL, Doly S, Narboux-Nême N, Fernández S, Mazot P, Banas SM, et al. 5-HT2B receptors are required for serotonin-selective antidepressant actions. Mol Psychiatry. 2012;17:154–63.

    Article  CAS  PubMed  Google Scholar 

  19. Doly S, Quentin E, Eddine R, Tolu S, Fernandez SP, Bertran-Gonzalez J, et al. Serotonin 2B Receptors in Mesoaccumbens Dopamine Pathway Regulate Cocaine Responses. J Neurosci. 2017;37:10372–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Nikodemova M, Kimyon RS, De I, Small AL, Collier LS, Watters JJ. Microglial numbers attain adult levels after undergoing a rapid decrease in cell number in the third postnatal week. J Neuroimmunol. 2015;278:280–8.

    Article  CAS  PubMed  Google Scholar 

  21. Dalmau I, Vela JM, González B, Finsen B, Castellano B. Dynamics of microglia in the developing rat brain: Proliferation and death of microglia in immature brain. J Comp Neurol. 2003;458:144–57.

    Article  PubMed  Google Scholar 

  22. Weinhard L, di Bartolomei G, Bolasco G, Machado P, Schieber NL, Neniskyte U, et al. Microglia remodel synapses by presynaptic trogocytosis and spine head filopodia induction. Nat Commun. 2018;9:1228.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Vainchtein ID, Chin G, Cho FS, Kelley KW, Miller JG, Chien EC, et al. Astrocyte-derived interleukin-33 promotes microglial synapse engulfment and neural circuit development. Science. 2018;359:1269–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, et al. The classical complement cascade mediates CNS synapse elimination. Cell. 2007;131:1164–78.

    Article  CAS  PubMed  Google Scholar 

  25. Basilico B, Pagani F, Grimaldi A, Cortese B, Di Angelantonio S, Weinhard L, et al. Microglia shape presynaptic properties at developing glutamatergic synapses. Glia. 2019;67:53–67.

    Article  PubMed  Google Scholar 

  26. Filipello F, Morini R, Corradini I, Zerbi V, Canzi A, Michalski B, et al. The microglial innate immune receptor TREM2 is required for synapse elimination and normal brain connectivity. Immunity. 2018;48:979–991.e8

    Article  CAS  PubMed  Google Scholar 

  27. Paolicelli RC, Bolasco G, Pagani F, Maggi L, Scianni M, Panzanelli P, et al. Synaptic pruning by microglia is necessary for normal brain development. Science. 2011;333:1456–8.

    Article  CAS  PubMed  Google Scholar 

  28. Weinhard L, Neniskyte U, Vadisiute A, di Bartolomei G, Aygün N, Riviere L, et al. Sexual dimorphism of microglia and synapses during mouse postnatal development: Sexual dimorphism in microglia and synapses. Devel Neurobio. 2018;78:618–26.

    Article  Google Scholar 

  29. Cheadle L, Rivera SA, Phelps JS, Ennis KA, Stevens B, Burkly LC, et al. Sensory experience engages microglia to shape neural connectivity through a non-phagocytic mechanism. Neuron. 2020;108:451–468.e9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Miyamoto A, Wake H, Ishikawa AW, Eto K, Shibata K, Murakoshi H, et al. Microglia contact induces synapse formation in developing somatosensory cortex. Nat Commun. 2016;7:12540.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Risher WC, Ustunkaya T, Singh Alvarado J, Eroglu C. Rapid golgi analysis method for efficient and unbiased classification of dendritic spines. PLoS ONE. 2014;9:e107591.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Assali A, Gaspar P, Rebsam A. Activity dependent mechanisms of visual map formation–from retinal waves to molecular regulators. Semin Cell Dev Biol. 2014;35:136–46.

    Article  CAS  PubMed  Google Scholar 

  33. Brioschi S, d’Errico P, Amann LS, Janova H, Wojcik SM, Meyer-Luehmann M, et al. Detection of synaptic proteins in microglia by flow cytometry. Front Mol Neurosci. 2020;13:149.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. D’Andrea I, Alleva E, Branchi I. Communal nesting, an early social enrichment, affects social competences but not learning and memory abilities at adulthood. Behavioural Brain Res. 2007;183:60–66.

    Article  Google Scholar 

  35. May T, Adesina I, McGillivray J, Rinehart NJ. Sex differences in neurodevelopmental disorders. Curr Opin Neurol. 2019;32:622–6.

    Article  PubMed  Google Scholar 

  36. van den Berg WE, Lamballais S, Kushner SA. Sex-specific mechanism of social hierarchy in mice. Neuropsychopharmacol. 2015;40:1364–72.

    Article  Google Scholar 

  37. Zhan Y, Paolicelli RC, Sforazzini F, Weinhard L, Bolasco G, Pagani F, et al. Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat Neurosci. 2014;17:400–6.

    Article  CAS  PubMed  Google Scholar 

  38. Parkhurst CN, Yang G, Ninan I, Savas JN, Yates JR, Lafaille JJ, et al. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell. 2013;155:1596–609.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Badimon A, Strasburger HJ, Ayata P, Chen X, Nair A, Ikegami A, et al. Negative feedback control of neuronal activity by microglia. Nature. 2020;586:417–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Cserép C, Pósfai B, Lénárt N, Fekete R, László ZI, Lele Z, et al. Microglia monitor and protect neuronal function through specialized somatic purinergic junctions. Science. 2020;367:528–37.

    Article  PubMed  Google Scholar 

  41. Akiyoshi R, Wake H, Kato D, Horiuchi H, Ono R, Ikegami A, et al. Microglia enhance synapse activity to promote local network synchronization. ENeuro. 2018;5:ENEURO.0088–18.2018.

    Article  PubMed  Google Scholar 

  42. Assali A, Le Magueresse C, Bennis M, Nicol X, Gaspar P, Rebsam A. RIM1/2 in retinal ganglion cells are required for the refinement of ipsilateral axons and eye-specific segregation. Sci Rep. 2017;7:3236.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Thion MS, Low D, Silvin A, Chen J, Grisel P, Schulte-Schrepping J, et al. Microbiome influences prenatal and adult microglia in a sex-specific manner. Cell. 2018;172:500–516.e16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Villa A. Sexual differentiation of microglia. Front Neuroendocrinol. 2019;52:156–64.

    Article  PubMed  Google Scholar 

  45. Hanamsagar R, Alter MD, Block CS, Sullivan H, Bolton JL, Bilbo SD. Generation of a microglial developmental index in mice and in humans reveals a sex difference in maturation and immune reactivity: HANAMSAGAR et al. Glia. 2017;65:1504–20.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Jovanovic H, Lundberg J, Karlsson P, Cerin Å, Saijo T, Varrone A, et al. Sex differences in the serotonin 1A receptor and serotonin transporter binding in the human brain measured by PET. NeuroImage. 2008;39:1408–19.

    Article  PubMed  Google Scholar 

  47. Ohsawa K, Irino Y, Sanagi T, Nakamura Y, Suzuki E, Inoue K, et al. P2Y 12 receptor-mediated integrin-β1 activation regulates microglial process extension induced by ATP. Glia. 2010. 2010. https://doi.org/10.1002/glia.20963.

  48. Sipe GO, Lowery RL, Tremblay M-È, Kelly EA, Lamantia CE, Majewska AK. Microglial P2Y12 is necessary for synaptic plasticity in mouse visual cortex. Nat Commun. 2016;7:10905.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Maroteaux L, Béchade C, Roumier A. Dimers of serotonin receptors: Impact on ligand affinity and signaling. Biochimie. 2019;161:23–33.

    Article  CAS  PubMed  Google Scholar 

  50. von Kügelgen I, Hoffmann K. Pharmacology and structure of P2Y receptors. Neuropharmacology. 2016;104:50–61.

    Article  Google Scholar 

  51. Oliver KH, Duvernay MT, Hamm HE, Carneiro AMD. Loss of serotonin transporter function alters ADP-mediated Glycoprotein αIIbβ3 activation through dysregulation of the 5-HT2A Receptor. J Biol Chem. 2016;291:20210–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Baqi Y, Müller CE. Antithrombotic P2Y12 receptor antagonists: recent developments in drug discovery. Drug Discov Today. 2019;24:325–33.

    Article  PubMed  Google Scholar 

  53. Saini HK, Takeda N, Goyal RK, Kumamoto H, Arneja AS, Dhalla NS. Therapeutic potentials of sarpogrelate in cardiovascular disease*. Cardiovasc Drug Rev. 2006;22:27–54.

    Article  Google Scholar 

  54. Percie du Sert N, Hurst V, Ahluwalia A, Alam S, Avey MT, Baker M, et al. The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol. 2020;18:e3000410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Belmer A, Quentin E, Diaz SL, Guiard BP, Fernandez SP, Doly S, et al. Positive regulation of raphe serotonin neurons by serotonin 2B receptors. Neuropsychopharmacol. 2018;43:1623–32.

    Article  CAS  Google Scholar 

  56. Pitulescu ME, Schmidt I, Benedito R, Adams RH. Inducible gene targeting in the neonatal vasculature and analysis of retinal angiogenesis in mice. Nat Protoc. 2010;5:1518–34.

    Article  CAS  PubMed  Google Scholar 

  57. Goldmann T, Wieghofer P, Müller PF, Wolf Y, Varol D, Yona S, et al. A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat Neurosci. 2013;16:1618–26.

    Article  CAS  PubMed  Google Scholar 

  58. Peng J, Gu N, Zhou L, B Eyo U, Murugan M, Gan W-B, et al. Microglia and monocytes synergistically promote the transition from acute to chronic pain after nerve injury. Nat Commun. 2016;7:12029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Wolf Y, Yona S, Kim K-W, Jung S. Microglia, seen from the CX3CR1 angle. Front Cell Neurosci. 2013;7:26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Yona S, Kim K-W, Wolf Y, Mildner A, Varol D, Breker M, et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity. 2013;38:79–91.

    Article  CAS  PubMed  Google Scholar 

  61. Franklin KBJ, Paxinos G. Paxino’s and Franklin’s the Mouse Brain in Stereotaxic Coordinates: Compact. 5th Edition. San Diego: Elsevier Science & Technology; 2019.

    Google Scholar 

  62. Schafer DP, Lehrman EK, Heller CT, Stevens B. An Engulfment Assay: A Protocol to Assess Interactions Between CNS Phagocytes and Neurons. JoVE. 2014; 88:e51482.

    Google Scholar 

  63. Young K, Morrison H. Quantifying Microglia Morphology from Photomicrographs of Immunohistochemistry Prepared Tissue Using ImageJ. JoVE. 2018;136:e57648.

    Google Scholar 

  64. Heck N, Betuing S, Vanhoutte P, Caboche J. A deconvolution method to improve automated 3D-analysis of dendritic spines: application to a mouse model of Huntington’s disease. Brain Struct Funct. 2012;217:421–34.

    Article  PubMed  Google Scholar 

  65. Rodriguez A, Ehlenberger DB, Dickstein DL, Hof PR, Wearne SL. Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images. PLoS ONE. 2008;3:e1997.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Giralt A, Brito V, Chevy Q, Simonnet C, Otsu Y, Cifuentes-Díaz C, et al. Pyk2 modulates hippocampal excitatory synapses and contributes to cognitive deficits in a Huntington’s disease model. Nat Commun. 2017;8:15592.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Zaqout S, Kaindl AM. Golgi-Cox Staining Step by Step. Front Neuroanat. 2016;10:38.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Rebsam A, Petros TJ, Mason CA. Switching retinogeniculate axon laterality leads to normal targeting but abnormal eye-specific segregation that is activity dependent. J Neurosci. 2009;29:14855–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Hayakawa I, Kawasaki H. Rearrangement of retinogeniculate projection patterns after eye-specific segregation in mice. PLoS ONE. 2010;5:e11001.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Silverman JL, Tolu SS, Barkan CL, Crawley JN. Repetitive self-grooming behavior in the BTBR mouse model of autism is blocked by the mGluR5 Antagonist MPEP. Neuropsychopharmacol. 2010;35:976–89.

    Article  CAS  Google Scholar 

  71. Scattoni ML, Gandhy SU, Ricceri L, Crawley JN. Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PLoS ONE. 2008;3:e3067.

    Article  PubMed  PubMed Central  Google Scholar 

  72. D’Andrea I, Fardella V, Fardella S, Pallante F, Ghigo A, Iacobucci R, et al. Lack of kinase‐independent activity of PI3Kγ in locus coeruleus induces ADHD symptoms through increased CREB signaling. EMBO Mol Med. 2015;7:904–17.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Yang M, Crawley JN. Simple Behavioral Assessment of Mouse Olfaction. Current Protocols in Neuroscience. 2009;48:8.24.1–12.

    Google Scholar 

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Acknowledgements

We thank Chris N. Parkhurst and Wenbiao B. Gan for providing the Cx3cr1creERT2 knock-in mice, the Cell and Tissue Imaging Facility of the Institut du Fer à Moulin (namely Theano Eirinopoulou, Mythili Savariradjane, and Xavier Marquès), where all image acquisitions and analyses have been performed, and the staff of the IFM animal facility (namely Baptiste Lecomte, Gaël Grannec, François Baudon, Anna-Sophia Mourenco, Emma Courteau and Eloise Marsan). We warmly thank Patricia Gaspar, Ludmilla Lokmane, Sonia Garel, Véronique Fabre and Jean Christophe Poncer for the discussion and revision. This work has been supported by grants from the Agence Nationale de la Recherche (ANR-17-CE16-0008, ANR-11-IDEX-0004-02), the Fondation pour la Recherche Médicale (Equipe FRM DEQ2014039529) and the Fédération pour la Recherche sur le Cerveau (FRC-2019-19F10).

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Author notes

  1. These authors contributed equally: Giulia Albertini, Ivana D’Andrea.

  2. These authors jointly supervised this work: Luc Maroteaux, Anne Roumier.

Authors and Affiliations

  1. Sorbonne Université, INSERM, Institut du Fer à Moulin, F-75005, Paris, France

    Giulia Albertini, Ivana D’Andrea, Mélanie Druart, Catherine Béchade, Nayadoleni Nieves-Rivera, Fanny Etienne, Corentin Le Magueresse, Alexandra Rebsam, Luc Maroteaux & Anne Roumier

  2. Sorbonne Université, INSERM, CNRS, Institut de la Vision, F-75012, Paris, France

    Alexandra Rebsam

  3. Sorbonne Université, CNRS, INSERM, Neurosciences Paris Seine, Institut de Biologie Paris Seine, F-75005, Paris, France

    Nicolas Heck

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Contributions

GA, ID, LM, and ARo designed the studies. GA, ID, ARo, and LM wrote the manuscript, all authors revised it. GA, ID, FE, and CB performed tamoxifen administration. GA performed immunofluorescence, image acquisition and analysis, Golgi-Cox staining and spine analyses. N.H. contributed to the design of DiOlistic labeling of dendritic spines, provided reagents and created the ImageJ Macro to analyze microglia/spines proximity. GA delivered DiI, performed image acquisition and analysis. CLM contributed to the design and analysis of the electrophysiology experiments and provided reagents. GA, MD, and NRN performed the electrophysiology experiments. ARe contributed to the design and analysis of the anterograde labeling of retinogeniculate projections and GA performed the intravitreal injections and image acquisition and analysis. ID performed behavioral experiments. GA, ID, and MD performed data analysis.

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Correspondence to Anne Roumier.

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Albertini, G., D’Andrea, I., Druart, M. et al. Serotonin sensing by microglia conditions the proper development of neuronal circuits and of social and adaptive skills. Mol Psychiatry (2023). https://doi.org/10.1038/s41380-023-02048-5

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