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Competition from newborn granule cells does not drive axonal retraction of silenced old granule cells in the adult hippocampus
In the developing nervous system synaptic refinement, typified by the neuromuscular junction where supernumerary connections are eliminated by axon retraction leaving the postsynaptic target innervated by a single dominant input, critically regulates neuronal circuit formation. Whether such competit...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2012
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3499763/ https://www.ncbi.nlm.nih.gov/pubmed/23162435 http://dx.doi.org/10.3389/fncir.2012.00085 |
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author | Lopez, Carla M. Pelkey, Kenneth A. Chittajallu, Ramesh Nakashiba, Toshiaki Tóth, Katalin Tonegawa, Susumu McBain, Chris J. |
author_facet | Lopez, Carla M. Pelkey, Kenneth A. Chittajallu, Ramesh Nakashiba, Toshiaki Tóth, Katalin Tonegawa, Susumu McBain, Chris J. |
author_sort | Lopez, Carla M. |
collection | PubMed |
description | In the developing nervous system synaptic refinement, typified by the neuromuscular junction where supernumerary connections are eliminated by axon retraction leaving the postsynaptic target innervated by a single dominant input, critically regulates neuronal circuit formation. Whether such competition-based pruning continues in established circuits of mature animals remains unknown. This question is particularly relevant in the context of adult neurogenesis where newborn cells must integrate into preexisting circuits, and thus, potentially compete with functionally mature synapses to gain access to their postsynaptic targets. The hippocampus plays an important role in memory formation/retrieval and the dentate gyrus (DG) subfield exhibits continued neurogenesis into adulthood. Therefore, this region contains both mature granule cells (old GCs) and immature recently born GCs that are generated throughout adult life (young GCs), providing a neurogenic niche model to examine the role of competition in synaptic refinement. Recent work from an independent group in developing animals indicated that embryonically/early postnatal generated GCs placed at a competitive disadvantage by selective expression of tetanus toxin (TeTX) to prevent synaptic release rapidly retracted their axons, and that this retraction was driven by competition from newborn GCs lacking TeTX. In contrast, following 3–6 months of selective TeTX expression in old GCs of adult mice we did not observe any evidence of axon retraction. Indeed ultrastructural analyses indicated that the terminals of silenced GCs even maintained synaptic contact with their postsynaptic targets. Furthermore, we did not detect any significant differences in the electrophysiological properties between old GCs in control and TeTX conditions. Thus, our data demonstrate a remarkable stability in the face of a relatively prolonged period of altered synaptic competition between two populations of neurons within the adult brain. |
format | Online Article Text |
id | pubmed-3499763 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2012 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-34997632012-11-16 Competition from newborn granule cells does not drive axonal retraction of silenced old granule cells in the adult hippocampus Lopez, Carla M. Pelkey, Kenneth A. Chittajallu, Ramesh Nakashiba, Toshiaki Tóth, Katalin Tonegawa, Susumu McBain, Chris J. Front Neural Circuits Neuroscience In the developing nervous system synaptic refinement, typified by the neuromuscular junction where supernumerary connections are eliminated by axon retraction leaving the postsynaptic target innervated by a single dominant input, critically regulates neuronal circuit formation. Whether such competition-based pruning continues in established circuits of mature animals remains unknown. This question is particularly relevant in the context of adult neurogenesis where newborn cells must integrate into preexisting circuits, and thus, potentially compete with functionally mature synapses to gain access to their postsynaptic targets. The hippocampus plays an important role in memory formation/retrieval and the dentate gyrus (DG) subfield exhibits continued neurogenesis into adulthood. Therefore, this region contains both mature granule cells (old GCs) and immature recently born GCs that are generated throughout adult life (young GCs), providing a neurogenic niche model to examine the role of competition in synaptic refinement. Recent work from an independent group in developing animals indicated that embryonically/early postnatal generated GCs placed at a competitive disadvantage by selective expression of tetanus toxin (TeTX) to prevent synaptic release rapidly retracted their axons, and that this retraction was driven by competition from newborn GCs lacking TeTX. In contrast, following 3–6 months of selective TeTX expression in old GCs of adult mice we did not observe any evidence of axon retraction. Indeed ultrastructural analyses indicated that the terminals of silenced GCs even maintained synaptic contact with their postsynaptic targets. Furthermore, we did not detect any significant differences in the electrophysiological properties between old GCs in control and TeTX conditions. Thus, our data demonstrate a remarkable stability in the face of a relatively prolonged period of altered synaptic competition between two populations of neurons within the adult brain. Frontiers Media S.A. 2012-11-16 /pmc/articles/PMC3499763/ /pubmed/23162435 http://dx.doi.org/10.3389/fncir.2012.00085 Text en Copyright © 2012 Lopez, Pelkey, Chittajallu, Nakashiba, Tóth, Tonegawa and McBain. http://www.frontiersin.org/licenseagreement This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc. |
spellingShingle | Neuroscience Lopez, Carla M. Pelkey, Kenneth A. Chittajallu, Ramesh Nakashiba, Toshiaki Tóth, Katalin Tonegawa, Susumu McBain, Chris J. Competition from newborn granule cells does not drive axonal retraction of silenced old granule cells in the adult hippocampus |
title | Competition from newborn granule cells does not drive axonal retraction of silenced old granule cells in the adult hippocampus |
title_full | Competition from newborn granule cells does not drive axonal retraction of silenced old granule cells in the adult hippocampus |
title_fullStr | Competition from newborn granule cells does not drive axonal retraction of silenced old granule cells in the adult hippocampus |
title_full_unstemmed | Competition from newborn granule cells does not drive axonal retraction of silenced old granule cells in the adult hippocampus |
title_short | Competition from newborn granule cells does not drive axonal retraction of silenced old granule cells in the adult hippocampus |
title_sort | competition from newborn granule cells does not drive axonal retraction of silenced old granule cells in the adult hippocampus |
topic | Neuroscience |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3499763/ https://www.ncbi.nlm.nih.gov/pubmed/23162435 http://dx.doi.org/10.3389/fncir.2012.00085 |
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