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Development/Plasticity/Repair

Brain-Derived Neurotrophic Factor Mediates Activity-Dependent Dendritic Growth in Nonpyramidal Neocortical Interneurons in Developing Organotypic Cultures

Xiaoming Jin, Hang Hu, Peter H. Mathers and Ariel Agmon
Journal of Neuroscience 2 July 2003, 23 (13) 5662-5673; DOI: https://doi.org/10.1523/JNEUROSCI.23-13-05662.2003
Xiaoming Jin
Departments of 1Neurobiology and Anatomy, 2Otolaryngology, 3Biochemistry and Molecular Pharmacology, and 4Ophthalmology, and 5The Sensory Neuroscience Research Center, West Virginia University, Morgantown, West Virginia 26506-9128
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Hang Hu
Departments of 1Neurobiology and Anatomy, 2Otolaryngology, 3Biochemistry and Molecular Pharmacology, and 4Ophthalmology, and 5The Sensory Neuroscience Research Center, West Virginia University, Morgantown, West Virginia 26506-9128
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Peter H. Mathers
Departments of 1Neurobiology and Anatomy, 2Otolaryngology, 3Biochemistry and Molecular Pharmacology, and 4Ophthalmology, and 5The Sensory Neuroscience Research Center, West Virginia University, Morgantown, West Virginia 26506-9128
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Ariel Agmon
Departments of 1Neurobiology and Anatomy, 2Otolaryngology, 3Biochemistry and Molecular Pharmacology, and 4Ophthalmology, and 5The Sensory Neuroscience Research Center, West Virginia University, Morgantown, West Virginia 26506-9128
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Abstract

Brain-derived neurotrophic factor (BDNF) promotes postnatal maturation of GABAergic inhibition in the cerebral and cerebellar cortices, and its expression and release are enhanced by neuronal activity, suggesting that it acts in a feedback manner to maintain a balance between excitation and inhibition during development. BDNF promotes differentiation of cerebellar, hippocampal, and neostriatal inhibitory neurons, but its effects on the dendritic development of neocortical inhibitory interneurons remain unknown. Here, we show that BDNF mediates depolarization-induced dendritic growth and branching in neocortical interneurons. To visualize inhibitory interneurons, we biolistically transfected organotypic cortical slice cultures from neonatal mice with green fluorescent protein (GFP) driven by the glutamic acid decarboxylase (GAD)67 promoter. Nearly all GAD67–GFP-expressing neurons were nonpyramidal, many contained GABA, and some expressed markers of neurochemically defined GABAergic subtypes, indicating that GAD67–GFP-expressing neurons were GABAergic. We traced dendritic trees from confocal images of the same GAD67–GFP-expressing neurons before and after a 5 d growth period, and quantified the change in total dendritic length (TDL) and total dendritic branch points (TDBPs) for each neuron. GAD67–GFP-expressing neurons growing in control medium exhibited a 20% increase in TDL, but in 200 ng/ml BDNF or 10 mm KCl, this increase nearly doubled and was accompanied by a significant increase in TDBPs. Blocking action potentials with TTX did not prevent the BDNF-induced growth, but antibodies against BDNF blocked the growth-promoting effect of KCl. We conclude that BDNF, released by neocortical pyramidal neurons in response to depolarization, enhances dendritic growth and branching in nearby inhibitory interneurons.

  • biolistic
  • BDNF
  • GABA
  • GAD67
  • gene gun
  • inhibitory interneuron
  • neocortical development
  • neurotrophins
  • organotypic slice
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The Journal of Neuroscience: 23 (13)
Journal of Neuroscience
Vol. 23, Issue 13
2 Jul 2003
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Brain-Derived Neurotrophic Factor Mediates Activity-Dependent Dendritic Growth in Nonpyramidal Neocortical Interneurons in Developing Organotypic Cultures
Xiaoming Jin, Hang Hu, Peter H. Mathers, Ariel Agmon
Journal of Neuroscience 2 July 2003, 23 (13) 5662-5673; DOI: 10.1523/JNEUROSCI.23-13-05662.2003

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Brain-Derived Neurotrophic Factor Mediates Activity-Dependent Dendritic Growth in Nonpyramidal Neocortical Interneurons in Developing Organotypic Cultures
Xiaoming Jin, Hang Hu, Peter H. Mathers, Ariel Agmon
Journal of Neuroscience 2 July 2003, 23 (13) 5662-5673; DOI: 10.1523/JNEUROSCI.23-13-05662.2003
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Keywords

  • biolistic
  • BDNF
  • GABA
  • GAD67
  • gene gun
  • inhibitory interneuron
  • neocortical development
  • neurotrophins
  • organotypic slice

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