Bidirectional synaptic plasticity rapidly modifies hippocampal representations
Learning requires neural adaptations thought to be mediated by activity-dependent synaptic plasticity. A relatively non-standard form of synaptic plasticity driven by dendritic calcium spikes, or plateau potentials, has been reported to underlie place field formation in rodent hippocampal CA1 neuron...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2021-12-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/73046 |
| _version_ | 1811199894751281152 |
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| author | Aaron D Milstein Yiding Li Katie C Bittner Christine Grienberger Ivan Soltesz Jeffrey C Magee Sandro Romani |
| author_facet | Aaron D Milstein Yiding Li Katie C Bittner Christine Grienberger Ivan Soltesz Jeffrey C Magee Sandro Romani |
| author_sort | Aaron D Milstein |
| collection | DOAJ |
| description | Learning requires neural adaptations thought to be mediated by activity-dependent synaptic plasticity. A relatively non-standard form of synaptic plasticity driven by dendritic calcium spikes, or plateau potentials, has been reported to underlie place field formation in rodent hippocampal CA1 neurons. Here, we found that this behavioral timescale synaptic plasticity (BTSP) can also reshape existing place fields via bidirectional synaptic weight changes that depend on the temporal proximity of plateau potentials to pre-existing place fields. When evoked near an existing place field, plateau potentials induced less synaptic potentiation and more depression, suggesting BTSP might depend inversely on postsynaptic activation. However, manipulations of place cell membrane potential and computational modeling indicated that this anti-correlation actually results from a dependence on current synaptic weight such that weak inputs potentiate and strong inputs depress. A network model implementing this bidirectional synaptic learning rule suggested that BTSP enables population activity, rather than pairwise neuronal correlations, to drive neural adaptations to experience. |
| first_indexed | 2024-04-12T01:55:39Z |
| format | Article |
| id | doaj.art-240b8b65f5a5412999917e8bd9fde04a |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T01:55:39Z |
| publishDate | 2021-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-240b8b65f5a5412999917e8bd9fde04a2022-12-22T03:52:49ZengeLife Sciences Publications LtdeLife2050-084X2021-12-011010.7554/eLife.73046Bidirectional synaptic plasticity rapidly modifies hippocampal representationsAaron D Milstein0https://orcid.org/0000-0002-7186-5779Yiding Li1Katie C Bittner2Christine Grienberger3Ivan Soltesz4Jeffrey C Magee5Sandro Romani6https://orcid.org/0000-0002-4727-4207Department of Neurosurgery and Stanford Neurosciences Institute, Stanford University School of Medicine, Stanford, United States; Department of Neuroscience and Cell Biology, Robert Wood Johnson Medical School and Center for Advanced Biotechnology and Medicine, Rutgers University, Piscataway, United StatesHoward Hughes Medical Institute, Baylor College of Medicine, Houston, United StatesHoward Hughes Medical Institute, Janelia Research Campus, Ashburn, United StatesHoward Hughes Medical Institute, Baylor College of Medicine, Houston, United StatesDepartment of Neurosurgery and Stanford Neurosciences Institute, Stanford University School of Medicine, Stanford, United StatesHoward Hughes Medical Institute, Baylor College of Medicine, Houston, United StatesHoward Hughes Medical Institute, Janelia Research Campus, Ashburn, United StatesLearning requires neural adaptations thought to be mediated by activity-dependent synaptic plasticity. A relatively non-standard form of synaptic plasticity driven by dendritic calcium spikes, or plateau potentials, has been reported to underlie place field formation in rodent hippocampal CA1 neurons. Here, we found that this behavioral timescale synaptic plasticity (BTSP) can also reshape existing place fields via bidirectional synaptic weight changes that depend on the temporal proximity of plateau potentials to pre-existing place fields. When evoked near an existing place field, plateau potentials induced less synaptic potentiation and more depression, suggesting BTSP might depend inversely on postsynaptic activation. However, manipulations of place cell membrane potential and computational modeling indicated that this anti-correlation actually results from a dependence on current synaptic weight such that weak inputs potentiate and strong inputs depress. A network model implementing this bidirectional synaptic learning rule suggested that BTSP enables population activity, rather than pairwise neuronal correlations, to drive neural adaptations to experience.https://elifesciences.org/articles/73046plasticitylearningplace celldendriteshippocampuscomputational model |
| spellingShingle | Aaron D Milstein Yiding Li Katie C Bittner Christine Grienberger Ivan Soltesz Jeffrey C Magee Sandro Romani Bidirectional synaptic plasticity rapidly modifies hippocampal representations eLife plasticity learning place cell dendrites hippocampus computational model |
| title | Bidirectional synaptic plasticity rapidly modifies hippocampal representations |
| title_full | Bidirectional synaptic plasticity rapidly modifies hippocampal representations |
| title_fullStr | Bidirectional synaptic plasticity rapidly modifies hippocampal representations |
| title_full_unstemmed | Bidirectional synaptic plasticity rapidly modifies hippocampal representations |
| title_short | Bidirectional synaptic plasticity rapidly modifies hippocampal representations |
| title_sort | bidirectional synaptic plasticity rapidly modifies hippocampal representations |
| topic | plasticity learning place cell dendrites hippocampus computational model |
| url | https://elifesciences.org/articles/73046 |
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