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Research ArticleNew Research, Neuronal Excitability

Long-Term Treatment with Low Doses of Methamphetamine Promotes Neuronal Differentiation and Strengthens Long-Term Potentiation of Glutamatergic Synapses onto Dentate Granule Neurons

Sofia Baptista, Joana Lourenço, Nuno Milhazes, Fernanda Borges, Ana Paula Silva and Alberto Bacci
eNeuro 22 June 2016, 3 (3) ENEURO.0141-16.2016; DOI: https://doi.org/10.1523/ENEURO.0141-16.2016
Sofia Baptista
1Institute of Pharmacology and Experimental Therapeutics, Faculty of Medicine, University of Coimbra, 3000-548 Coimbra, Portugal
2Institute for Biomedical Imaging and Life Sciences, Faculty of Medicine, University of Coimbra, 3000-548 Coimbra, Portugal
3Sorbonne Universités, Université Pierre et Marie Curie, Unité Mixte de Recherche (UMR) S 1127, Institut National de la Santé et de la Recherche Médicale U 1127, Centre National de la Recherche Scientifique UMR 7225, and Institut du Cerveau et de la Moelle épinière, 75013 Paris, France
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Joana Lourenço
3Sorbonne Universités, Université Pierre et Marie Curie, Unité Mixte de Recherche (UMR) S 1127, Institut National de la Santé et de la Recherche Médicale U 1127, Centre National de la Recherche Scientifique UMR 7225, and Institut du Cerveau et de la Moelle épinière, 75013 Paris, France
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Nuno Milhazes
4Institute of Health Sciences-North, 4585-116 Gandra, Portugal
5Department of Chemistry and Biochemistry, Faculty of Sciences, Centro de Investigação em Química da Universidade do Porto, 4169-007 Porto, Portugal
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Fernanda Borges
5Department of Chemistry and Biochemistry, Faculty of Sciences, Centro de Investigação em Química da Universidade do Porto, 4169-007 Porto, Portugal
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Ana Paula Silva
1Institute of Pharmacology and Experimental Therapeutics, Faculty of Medicine, University of Coimbra, 3000-548 Coimbra, Portugal
2Institute for Biomedical Imaging and Life Sciences, Faculty of Medicine, University of Coimbra, 3000-548 Coimbra, Portugal
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Alberto Bacci
3Sorbonne Universités, Université Pierre et Marie Curie, Unité Mixte de Recherche (UMR) S 1127, Institut National de la Santé et de la Recherche Médicale U 1127, Centre National de la Recherche Scientifique UMR 7225, and Institut du Cerveau et de la Moelle épinière, 75013 Paris, France
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Abstract

Methamphetamine (METH) is a psychostimulant, affecting hippocampal function with disparate cognitive effects, which depends on the dose and time of administration, ranging from improvement to impairment of memory. Importantly, in the United States, METH is approved for the treatment of attention deficit hyperactivity disorder. Modifications of long-term plasticity of synapses originating from the entorhinal cortex onto dentate granule cells (DGCs) have been proposed to underlie cognitive alterations similar to those seen in METH users. However, the effects of METH on synaptic plasticity of the dentate gyrus are unknown. Here, we investigated the impact of long-term administration of METH (2 mg/kg/d) on neurogenesis and synaptic plasticity of immature and mature DGCs of juvenile mice. We used a mouse model of neurogenesis (the G42 line of GAD67-GFP), in which GFP is expressed by differentiating young DGCs. METH treatment enhanced the differentiation of GFP+ cells, as it increased the fraction of GFP+ cells expressing the neuronal marker NeuN, and decreased the amount of immature DGCs coexpressing doublecortin. Interestingly, METH did not change the magnitude of long-term potentiation (LTP) in more immature neurons, but facilitated LTP induction in more differentiated GFP+ and strengthened plasticity in mature GFP− DGCs. The METH-induced facilitation of LTP in GFP+ neurons was accompanied with spine enlargement. Our results reveal a specific action of long-term use of METH in the long-term plasticity of excitatory synapses onto differentiating DGCs and might have important implications toward the understanding of the synaptic basis of METH-induced cognitive alterations.

  • ADHD
  • dentate gyrus
  • methamphetamine
  • neurogenesis
  • synaptic plasticity

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by fellowship SFRH/BD/63773/2009 from the Foundation for Science and Technology, Portugal; was cofinanced by Quadro de Referência Estratégica Nacional (S.B.), strategic project UID/NEU/04539/2013 (A.P.S.), and the European Research Council (ERC) under the 7th Framework Programme for the European Community (FP7/2007-2013)/ERC Grant agreement No. 200808); “Investissements d’avenir” ANR-10-IAIHU-06; Agence Nationale de la Recherche (ANR-13-BSV4-0015-01), Fondation Recherche Médicale (Equipe FRM DEQ20150331684), and a grant from the Institut du Cerveau et de la Moelle épinière (Paris) (A.B.). A.B. is supported by a 2014 NARSAD Independent Investigator Grant from the Brain and Behavior Research Foundation.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Long-Term Treatment with Low Doses of Methamphetamine Promotes Neuronal Differentiation and Strengthens Long-Term Potentiation of Glutamatergic Synapses onto Dentate Granule Neurons
Sofia Baptista, Joana Lourenço, Nuno Milhazes, Fernanda Borges, Ana Paula Silva, Alberto Bacci
eNeuro 22 June 2016, 3 (3) ENEURO.0141-16.2016; DOI: 10.1523/ENEURO.0141-16.2016

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Long-Term Treatment with Low Doses of Methamphetamine Promotes Neuronal Differentiation and Strengthens Long-Term Potentiation of Glutamatergic Synapses onto Dentate Granule Neurons
Sofia Baptista, Joana Lourenço, Nuno Milhazes, Fernanda Borges, Ana Paula Silva, Alberto Bacci
eNeuro 22 June 2016, 3 (3) ENEURO.0141-16.2016; DOI: 10.1523/ENEURO.0141-16.2016
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Keywords

  • ADHD
  • dentate gyrus
  • methamphetamine
  • neurogenesis
  • synaptic plasticity

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