Dendritic branch structure compartmentalizes voltage-dependent calcium influx in cortical layer 2/3 pyramidal cells
Back-propagating action potentials (bAPs) regulate synaptic plasticity by evoking voltage-dependent calcium influx throughout dendrites. Attenuation of bAP amplitude in distal dendritic compartments alters plasticity in a location-specific manner by reducing bAP-dependent calcium influx. However, it...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2022-03-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/76993 |
| _version_ | 1828108691719585792 |
|---|---|
| author | Andrew T Landau Pojeong Park J David Wong-Campos He Tian Adam E Cohen Bernardo L Sabatini |
| author_facet | Andrew T Landau Pojeong Park J David Wong-Campos He Tian Adam E Cohen Bernardo L Sabatini |
| author_sort | Andrew T Landau |
| collection | DOAJ |
| description | Back-propagating action potentials (bAPs) regulate synaptic plasticity by evoking voltage-dependent calcium influx throughout dendrites. Attenuation of bAP amplitude in distal dendritic compartments alters plasticity in a location-specific manner by reducing bAP-dependent calcium influx. However, it is not known if neurons exhibit branch-specific variability in bAP-dependent calcium signals, independent of distance-dependent attenuation. Here, we reveal that bAPs fail to evoke calcium influx through voltage-gated calcium channels (VGCCs) in a specific population of dendritic branches in mouse cortical layer 2/3 pyramidal cells, despite evoking substantial VGCC-mediated calcium influx in sister branches. These branches contain VGCCs and successfully propagate bAPs in the absence of synaptic input; nevertheless, they fail to exhibit bAP-evoked calcium influx due to a branch-specific reduction in bAP amplitude. We demonstrate that these branches have more elaborate branch structure compared to sister branches, which causes a local reduction in electrotonic impedance and bAP amplitude. Finally, we show that bAPs still amplify synaptically-mediated calcium influx in these branches because of differences in the voltage-dependence and kinetics of VGCCs and NMDA-type glutamate receptors. Branch-specific compartmentalization of bAP-dependent calcium signals may provide a mechanism for neurons to diversify synaptic tuning across the dendritic tree. |
| first_indexed | 2024-04-11T10:50:48Z |
| format | Article |
| id | doaj.art-35d554ddd3e747feac0df7f795bbe7b9 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T10:50:48Z |
| publishDate | 2022-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-35d554ddd3e747feac0df7f795bbe7b92022-12-22T04:28:55ZengeLife Sciences Publications LtdeLife2050-084X2022-03-011110.7554/eLife.76993Dendritic branch structure compartmentalizes voltage-dependent calcium influx in cortical layer 2/3 pyramidal cellsAndrew T Landau0https://orcid.org/0000-0001-9105-1636Pojeong Park1J David Wong-Campos2He Tian3https://orcid.org/0000-0003-3282-7275Adam E Cohen4https://orcid.org/0000-0002-8699-2404Bernardo L Sabatini5https://orcid.org/0000-0003-0095-9177Howard Hughes Medical Institute, Department of Neurobiology, Harvard Medical School, Boston, United StatesDepartment of Chemistry and Chemical Biology, Harvard University, Cambridge, United StatesDepartment of Chemistry and Chemical Biology, Harvard University, Cambridge, United StatesDepartment of Chemistry and Chemical Biology, Harvard University, Cambridge, United StatesDepartment of Chemistry and Chemical Biology, Harvard University, Cambridge, United States; Department of Physics, Harvard University, Cambridge, United StatesHoward Hughes Medical Institute, Department of Neurobiology, Harvard Medical School, Boston, United StatesBack-propagating action potentials (bAPs) regulate synaptic plasticity by evoking voltage-dependent calcium influx throughout dendrites. Attenuation of bAP amplitude in distal dendritic compartments alters plasticity in a location-specific manner by reducing bAP-dependent calcium influx. However, it is not known if neurons exhibit branch-specific variability in bAP-dependent calcium signals, independent of distance-dependent attenuation. Here, we reveal that bAPs fail to evoke calcium influx through voltage-gated calcium channels (VGCCs) in a specific population of dendritic branches in mouse cortical layer 2/3 pyramidal cells, despite evoking substantial VGCC-mediated calcium influx in sister branches. These branches contain VGCCs and successfully propagate bAPs in the absence of synaptic input; nevertheless, they fail to exhibit bAP-evoked calcium influx due to a branch-specific reduction in bAP amplitude. We demonstrate that these branches have more elaborate branch structure compared to sister branches, which causes a local reduction in electrotonic impedance and bAP amplitude. Finally, we show that bAPs still amplify synaptically-mediated calcium influx in these branches because of differences in the voltage-dependence and kinetics of VGCCs and NMDA-type glutamate receptors. Branch-specific compartmentalization of bAP-dependent calcium signals may provide a mechanism for neurons to diversify synaptic tuning across the dendritic tree.https://elifesciences.org/articles/76993dendritescalciumimpedancebiophysicsaction potentials |
| spellingShingle | Andrew T Landau Pojeong Park J David Wong-Campos He Tian Adam E Cohen Bernardo L Sabatini Dendritic branch structure compartmentalizes voltage-dependent calcium influx in cortical layer 2/3 pyramidal cells eLife dendrites calcium impedance biophysics action potentials |
| title | Dendritic branch structure compartmentalizes voltage-dependent calcium influx in cortical layer 2/3 pyramidal cells |
| title_full | Dendritic branch structure compartmentalizes voltage-dependent calcium influx in cortical layer 2/3 pyramidal cells |
| title_fullStr | Dendritic branch structure compartmentalizes voltage-dependent calcium influx in cortical layer 2/3 pyramidal cells |
| title_full_unstemmed | Dendritic branch structure compartmentalizes voltage-dependent calcium influx in cortical layer 2/3 pyramidal cells |
| title_short | Dendritic branch structure compartmentalizes voltage-dependent calcium influx in cortical layer 2/3 pyramidal cells |
| title_sort | dendritic branch structure compartmentalizes voltage dependent calcium influx in cortical layer 2 3 pyramidal cells |
| topic | dendrites calcium impedance biophysics action potentials |
| url | https://elifesciences.org/articles/76993 |
| work_keys_str_mv | AT andrewtlandau dendriticbranchstructurecompartmentalizesvoltagedependentcalciuminfluxincorticallayer23pyramidalcells AT pojeongpark dendriticbranchstructurecompartmentalizesvoltagedependentcalciuminfluxincorticallayer23pyramidalcells AT jdavidwongcampos dendriticbranchstructurecompartmentalizesvoltagedependentcalciuminfluxincorticallayer23pyramidalcells AT hetian dendriticbranchstructurecompartmentalizesvoltagedependentcalciuminfluxincorticallayer23pyramidalcells AT adamecohen dendriticbranchstructurecompartmentalizesvoltagedependentcalciuminfluxincorticallayer23pyramidalcells AT bernardolsabatini dendriticbranchstructurecompartmentalizesvoltagedependentcalciuminfluxincorticallayer23pyramidalcells |