Enhanced Non-Associative Long-Term Potentiation in Immature Granule Cells in the Dentate Gyrus of Adult Rats
The dentate gyrus is one of the few sites of neurogenesis in the adult brain. Integration of new-generated granule cells into the hippocampal circuitry provides a substrate for structural plasticity, fundamental for normal function of adult hippocampus. However, mechanisms of synaptic plasticity tha...
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Frontiers Media S.A.
2022-05-01
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| Series: | Frontiers in Synaptic Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnsyn.2022.889947/full |
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| author | Natalia A. Simonova Maxim A. Volgushev Maxim A. Volgushev Alexey Y. Malyshev |
| author_facet | Natalia A. Simonova Maxim A. Volgushev Maxim A. Volgushev Alexey Y. Malyshev |
| author_sort | Natalia A. Simonova |
| collection | DOAJ |
| description | The dentate gyrus is one of the few sites of neurogenesis in the adult brain. Integration of new-generated granule cells into the hippocampal circuitry provides a substrate for structural plasticity, fundamental for normal function of adult hippocampus. However, mechanisms of synaptic plasticity that mediate integration of new-generated granule cells into the existing circuitry remain poorly understood. Especially mechanisms of plasticity at GABA-ergic synapses remain elusive. Here, we show that postsynaptic spiking without presynaptic activation can induce heterosynaptic, non-associative plasticity at GABA-ergic inputs to both immature and mature granule cells. In both immature and mature neurons, plastic changes were bidirectional and individual inputs could express long-term potentiation (LTP) or long-term depression (LTD), or do not change. However, properties of non-associative plasticity dramatically change with maturation of newly generated granule cells: while in immature cells there was a clear predominance of non-associative LTP and net potentiation across the inputs, in mature neurons, potentiation and depression were balanced with no net change on average. We conclude that GABA-ergic inputs to granule cells are plastic, and that the rules for induction of non-associative plasticity change with maturation. We propose that potentiation-biased non-associative plasticity of GABA-ergic transmission might help to counter-balance an increase of excitatory drive that is facilitated by enhanced LTP at glutamatergic synapses in maturating granule cells. Such mechanism might help to build a strong GABA-ergic input to surviving active new cells, necessary for normal function of mature granule cells, which operate under a tight inhibitory control and generate sparse spiking activity. |
| first_indexed | 2024-12-12T04:33:31Z |
| format | Article |
| id | doaj.art-39e5b4ec82c0439d83a0eba3aaae7b75 |
| institution | Directory Open Access Journal |
| issn | 1663-3563 |
| language | English |
| last_indexed | 2024-12-12T04:33:31Z |
| publishDate | 2022-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Synaptic Neuroscience |
| spelling | doaj.art-39e5b4ec82c0439d83a0eba3aaae7b752022-12-22T00:38:01ZengFrontiers Media S.A.Frontiers in Synaptic Neuroscience1663-35632022-05-011410.3389/fnsyn.2022.889947889947Enhanced Non-Associative Long-Term Potentiation in Immature Granule Cells in the Dentate Gyrus of Adult RatsNatalia A. Simonova0Maxim A. Volgushev1Maxim A. Volgushev2Alexey Y. Malyshev3Institute of Higher Nervous Activity and Neurophysiology of Russian Academy of Sciences, Moscow, RussiaInstitute of Higher Nervous Activity and Neurophysiology of Russian Academy of Sciences, Moscow, RussiaDepartment of Psychological Sciences, University of Connecticut, Storrs, CT, United StatesInstitute of Higher Nervous Activity and Neurophysiology of Russian Academy of Sciences, Moscow, RussiaThe dentate gyrus is one of the few sites of neurogenesis in the adult brain. Integration of new-generated granule cells into the hippocampal circuitry provides a substrate for structural plasticity, fundamental for normal function of adult hippocampus. However, mechanisms of synaptic plasticity that mediate integration of new-generated granule cells into the existing circuitry remain poorly understood. Especially mechanisms of plasticity at GABA-ergic synapses remain elusive. Here, we show that postsynaptic spiking without presynaptic activation can induce heterosynaptic, non-associative plasticity at GABA-ergic inputs to both immature and mature granule cells. In both immature and mature neurons, plastic changes were bidirectional and individual inputs could express long-term potentiation (LTP) or long-term depression (LTD), or do not change. However, properties of non-associative plasticity dramatically change with maturation of newly generated granule cells: while in immature cells there was a clear predominance of non-associative LTP and net potentiation across the inputs, in mature neurons, potentiation and depression were balanced with no net change on average. We conclude that GABA-ergic inputs to granule cells are plastic, and that the rules for induction of non-associative plasticity change with maturation. We propose that potentiation-biased non-associative plasticity of GABA-ergic transmission might help to counter-balance an increase of excitatory drive that is facilitated by enhanced LTP at glutamatergic synapses in maturating granule cells. Such mechanism might help to build a strong GABA-ergic input to surviving active new cells, necessary for normal function of mature granule cells, which operate under a tight inhibitory control and generate sparse spiking activity.https://www.frontiersin.org/articles/10.3389/fnsyn.2022.889947/fulladult neurogenesisdentate gyrusgranule cellsGABAnon-associative potentiationheterosynaptic plasticity |
| spellingShingle | Natalia A. Simonova Maxim A. Volgushev Maxim A. Volgushev Alexey Y. Malyshev Enhanced Non-Associative Long-Term Potentiation in Immature Granule Cells in the Dentate Gyrus of Adult Rats Frontiers in Synaptic Neuroscience adult neurogenesis dentate gyrus granule cells GABA non-associative potentiation heterosynaptic plasticity |
| title | Enhanced Non-Associative Long-Term Potentiation in Immature Granule Cells in the Dentate Gyrus of Adult Rats |
| title_full | Enhanced Non-Associative Long-Term Potentiation in Immature Granule Cells in the Dentate Gyrus of Adult Rats |
| title_fullStr | Enhanced Non-Associative Long-Term Potentiation in Immature Granule Cells in the Dentate Gyrus of Adult Rats |
| title_full_unstemmed | Enhanced Non-Associative Long-Term Potentiation in Immature Granule Cells in the Dentate Gyrus of Adult Rats |
| title_short | Enhanced Non-Associative Long-Term Potentiation in Immature Granule Cells in the Dentate Gyrus of Adult Rats |
| title_sort | enhanced non associative long term potentiation in immature granule cells in the dentate gyrus of adult rats |
| topic | adult neurogenesis dentate gyrus granule cells GABA non-associative potentiation heterosynaptic plasticity |
| url | https://www.frontiersin.org/articles/10.3389/fnsyn.2022.889947/full |
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