Running reorganizes the circuitry of one-week-old adult-born hippocampal neurons

Adult hippocampal neurogenesis is an important form of structural and functional plasticity in the mature mammalian brain. The existing consensus is that GABA regulates the initial integration of adult-born neurons, similar to neuronal development during embryogenesis. Surprisingly, virus-based anat...

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Published inScientific reports Vol. 7; no. 1; pp. 10903 - 15
Main Authors Sah, Nirnath, Peterson, Benjamin D, Lubejko, Susan T, Vivar, Carmen, van Praag, Henriette
Format Journal Article
LanguageEnglish
Published England Nature Publishing Group 07.09.2017
Nature Publishing Group UK
Subjects
Action Potentials
Adult
Animals
Cell number
Cytology
Embryogenesis
Functional plasticity
Glutamatergic transmission
Granule cells
Hippocampal plasticity
Hippocampus
Hippocampus - physiology
Humans
Innervation
Interneurons
Mice, Inbred C57BL
N-Methyl-D-aspartic acid
Nerve Net - physiology
Neurogenesis
Neurons - physiology
Patch-Clamp Techniques
Pyramidal cells
Rodents
Running
Structure-function relationships
Wheel running
γ-Aminobutyric acid
Online AccessGet full text

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Abstract Adult hippocampal neurogenesis is an important form of structural and functional plasticity in the mature mammalian brain. The existing consensus is that GABA regulates the initial integration of adult-born neurons, similar to neuronal development during embryogenesis. Surprisingly, virus-based anatomical tracing revealed that very young, one-week-old, new granule cells in male C57Bl/6 mice receive input not only from GABAergic interneurons, but also from multiple glutamatergic cell types, including mature dentate granule cells, area CA1-3 pyramidal cells and mossy cells. Consistently, patch-clamp recordings from retrovirally labeled new granule cells at 7-8 days post retroviral injection (dpi) show that these cells respond to NMDA application with tonic currents, and that both electrical and optogenetic stimulation can evoke NMDA-mediated synaptic responses. Furthermore, new dentate granule cell number, morphology and excitatory synaptic inputs at 7 dpi are modified by voluntary wheel running. Overall, glutamatergic and GABAergic innervation of newly born neurons in the adult hippocampus develops concurrently, and excitatory input is reorganized by exercise.
AbstractList Abstract Adult hippocampal neurogenesis is an important form of structural and functional plasticity in the mature mammalian brain. The existing consensus is that GABA regulates the initial integration of adult-born neurons, similar to neuronal development during embryogenesis. Surprisingly, virus-based anatomical tracing revealed that very young, one-week-old, new granule cells in male C57Bl/6 mice receive input not only from GABAergic interneurons, but also from multiple glutamatergic cell types, including mature dentate granule cells, area CA1-3 pyramidal cells and mossy cells. Consistently, patch-clamp recordings from retrovirally labeled new granule cells at 7–8 days post retroviral injection (dpi) show that these cells respond to NMDA application with tonic currents, and that both electrical and optogenetic stimulation can evoke NMDA-mediated synaptic responses. Furthermore, new dentate granule cell number, morphology and excitatory synaptic inputs at 7 dpi are modified by voluntary wheel running. Overall, glutamatergic and GABAergic innervation of newly born neurons in the adult hippocampus develops concurrently, and excitatory input is reorganized by exercise.
Adult hippocampal neurogenesis is an important form of structural and functional plasticity in the mature mammalian brain. The existing consensus is that GABA regulates the initial integration of adult-born neurons, similar to neuronal development during embryogenesis. Surprisingly, virus-based anatomical tracing revealed that very young, one-week-old, new granule cells in male C57Bl/6 mice receive input not only from GABAergic interneurons, but also from multiple glutamatergic cell types, including mature dentate granule cells, area CA1-3 pyramidal cells and mossy cells. Consistently, patch-clamp recordings from retrovirally labeled new granule cells at 7–8 days post retroviral injection (dpi) show that these cells respond to NMDA application with tonic currents, and that both electrical and optogenetic stimulation can evoke NMDA-mediated synaptic responses. Furthermore, new dentate granule cell number, morphology and excitatory synaptic inputs at 7 dpi are modified by voluntary wheel running. Overall, glutamatergic and GABAergic innervation of newly born neurons in the adult hippocampus develops concurrently, and excitatory input is reorganized by exercise.
ArticleNumber 10903
Author van Praag, Henriette
Sah, Nirnath
Peterson, Benjamin D
Lubejko, Susan T
Vivar, Carmen
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  surname: Lubejko
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  organization: Neuroplasticity and Behavior Unit, Laboratory of Neurosciences, Intramural Research Program, National Institute on Aging, National Institutes of Health, Baltimore, MD, 21224, USA
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  fullname: Vivar, Carmen
  email: cvivar@fisio.cinvestav.mx
  organization: Laboratory of Neurogenesis and Neuroplasticity, Department of Physiology, Biophysics, and Neuroscience, Center for Research and Advanced Studies of the National Polytechnic Institute, Mexico City, 07360, Mexico. cvivar@fisio.cinvestav.mx
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  email: h.van.praag1@gmail.com
  organization: Neuroplasticity and Behavior Unit, Laboratory of Neurosciences, Intramural Research Program, National Institute on Aging, National Institutes of Health, Baltimore, MD, 21224, USA. h.van.praag1@gmail.com
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Snippet Adult hippocampal neurogenesis is an important form of structural and functional plasticity in the mature mammalian brain. The existing consensus is that GABA...
Abstract Adult hippocampal neurogenesis is an important form of structural and functional plasticity in the mature mammalian brain. The existing consensus is...
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SubjectTerms Action Potentials
Adult
Animals
Cell number
Cytology
Embryogenesis
Functional plasticity
Glutamatergic transmission
Granule cells
Hippocampal plasticity
Hippocampus
Hippocampus - physiology
Humans
Innervation
Interneurons
Mice, Inbred C57BL
N-Methyl-D-aspartic acid
Nerve Net - physiology
Neurogenesis
Neurons - physiology
Patch-Clamp Techniques
Pyramidal cells
Rodents
Running
Structure-function relationships
Wheel running
γ-Aminobutyric acid
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Title Running reorganizes the circuitry of one-week-old adult-born hippocampal neurons
URI https://www.ncbi.nlm.nih.gov/pubmed/28883658
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