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  3. Astrocytes mediate long-lasting synaptic regulation of ventral tegmental area dopamine neurons

Astrocytes mediate long-lasting synaptic regulation of ventral tegmental area dopamine neurons

  • Nat Neurosci. 2022 Dec;25(12):1639-1650. doi: 10.1038/s41593-022-01193-4.
Linda Maria Requie # 1,  Marta Gómez-Gonzalo # 2,  Michele Speggiorin # 1,  Francesca Managò 3,  Marcello Melone 4,  Mauro Congiu 5 6,  Angela Chiavegato 1,  Annamaria Lia 1,  Micaela Zonta 1,  Gabriele Losi 1 7,  Vanessa Jorge Henriques 1,  Arianna Pugliese 4,  Giada Pacinelli 3 8,  Giovanni Marsicano 9,  Francesco Papaleo 3,  Anna Lisa Muntoni 6,  Fiorenzo Conti 4,  Giorgio Carmignoto 10
Affiliations

Affiliations

  • 1 Neuroscience Institute, Section of Padova, National Research Council (CNR) and Department of Biomedical Sciences, Università degli Studi di Padova, Padova, Italy.
  • 2 Neuroscience Institute, Section of Padova, National Research Council (CNR) and Department of Biomedical Sciences, Università degli Studi di Padova, Padova, Italy. marta.gomezgonzalo@cnr.it.
  • 3 Genetics of Cognition Laboratory, Neuroscience Area, Istituto Italiano di Tecnologia (IIT), Genova, Italy.
  • 4 Department of Experimental and Clinical Medicine, Section of Neuroscience & Cell Biology, Università Politecnica delle Marche, and Center for Neurobiology of Aging, IRCCS INRCA, Ancona, Italy.
  • 5 Department of Biomedical Sciences, Division of Neuroscience and Clinical Pharmacology, Università degli Studi di Cagliari, Cagliari, Italy.
  • 6 Neuroscience Institute, Section of Cagliari, National Research Council (CNR), Cagliari, Italy.
  • 7 Nanoscience Institute, National Research Council (CNR), Modena, Italy.
  • 8 Padova Neuroscience Center (PNC), University of Padova, Padova, Italy.
  • 9 University of Bordeaux and Interdisciplinary Institute for Neuroscience (CNRS), Bordeaux, France.
  • 10 Neuroscience Institute, Section of Padova, National Research Council (CNR) and Department of Biomedical Sciences, Università degli Studi di Padova, Padova, Italy. giorgio.carmignoto@bio.unipd.it.
  • # Contributed equally.
PMID: 36396976 DOI: 10.1038/s41593-022-01193-4
Abstract

The plasticity of glutamatergic transmission in the ventral tegmental area (VTA) represents a fundamental mechanism in the modulation of dopamine neuron burst firing and phasic dopamine release at target regions. These processes encode basic behavioral responses, including locomotor activity, learning and motivated behaviors. Here we describe a hitherto unidentified mechanism of long-term synaptic plasticity in mouse VTA. We found that the burst firing in individual dopamine neurons induces a long-lasting potentiation of excitatory synapses on adjacent dopamine neurons that crucially depends on CA2+ elevations in astrocytes, mediated by endocannabinoid CB1 and dopamine D2 receptors co-localized at the same astrocytic process, and activation of pre-synaptic Metabotropic Glutamate Receptors. Consistent with these findings, selective in vivo activation of astrocytes increases the burst firing of dopamine neurons in the VTA and induces locomotor hyperactivity. Astrocytes play, therefore, a key role in the modulation of VTA dopamine neuron functional activity.

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