Modeling the Shape of Synaptic Spines by Their Actin Dynamics
Dendritic spines are the morphological basis of excitatory synapses in the cortex and their size and shape correlates with functional synaptic properties. Recent experiments show that spines exhibit large shape fluctuations that are not related to activity-dependent plasticity but nonetheless might...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-03-01
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| Series: | Frontiers in Synaptic Neuroscience |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fnsyn.2020.00009/full |
| _version_ | 1818942878044389376 |
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| author | Mayte Bonilla-Quintana Florentin Wörgötter Florentin Wörgötter Christian Tetzlaff Christian Tetzlaff Michael Fauth |
| author_facet | Mayte Bonilla-Quintana Florentin Wörgötter Florentin Wörgötter Christian Tetzlaff Christian Tetzlaff Michael Fauth |
| author_sort | Mayte Bonilla-Quintana |
| collection | DOAJ |
| description | Dendritic spines are the morphological basis of excitatory synapses in the cortex and their size and shape correlates with functional synaptic properties. Recent experiments show that spines exhibit large shape fluctuations that are not related to activity-dependent plasticity but nonetheless might influence memory storage at their synapses. To investigate the determinants of such spontaneous fluctuations, we propose a mathematical model for the dynamics of the spine shape and analyze it in 2D—related to experimental microscopic imagery—and in 3D. We show that the spine shape is governed by a local imbalance between membrane tension and the expansive force from actin bundles that originates from discrete actin polymerization foci. Experiments have shown that only few such polymerization foci co-exist at any time in a spine, each having limited life time. The model shows that the momentarily existing set of such foci pushes the membrane along certain directions until foci are replaced and other directions may now be affected. We explore these relations in depth and use our model to predict shape and temporal characteristics of spines from the different biophysical parameters involved in actin polymerization. Approximating the model by a single recursive equation we finally demonstrate that the temporal evolution of the number of active foci is sufficient to predict the size of the model-spines. Thus, our model provides the first platform to study the relation between molecular and morphological properties of the spine with a high degree of biophysical detail. |
| first_indexed | 2024-12-20T07:18:25Z |
| format | Article |
| id | doaj.art-946e0c04dced44b381662c70b3868cb3 |
| institution | Directory Open Access Journal |
| issn | 1663-3563 |
| language | English |
| last_indexed | 2024-12-20T07:18:25Z |
| publishDate | 2020-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Synaptic Neuroscience |
| spelling | doaj.art-946e0c04dced44b381662c70b3868cb32022-12-21T19:48:44ZengFrontiers Media S.A.Frontiers in Synaptic Neuroscience1663-35632020-03-011210.3389/fnsyn.2020.00009520540Modeling the Shape of Synaptic Spines by Their Actin DynamicsMayte Bonilla-Quintana0Florentin Wörgötter1Florentin Wörgötter2Christian Tetzlaff3Christian Tetzlaff4Michael Fauth5Department for Computational Neuroscience, Third Institute of Physics-Biophysics, Georg-August-University, Göttingen, GermanyDepartment for Computational Neuroscience, Third Institute of Physics-Biophysics, Georg-August-University, Göttingen, GermanyBernstein Center for Computational Neuroscience, Georg-August-University, Göttingen, GermanyDepartment for Computational Neuroscience, Third Institute of Physics-Biophysics, Georg-August-University, Göttingen, GermanyBernstein Center for Computational Neuroscience, Georg-August-University, Göttingen, GermanyDepartment for Computational Neuroscience, Third Institute of Physics-Biophysics, Georg-August-University, Göttingen, GermanyDendritic spines are the morphological basis of excitatory synapses in the cortex and their size and shape correlates with functional synaptic properties. Recent experiments show that spines exhibit large shape fluctuations that are not related to activity-dependent plasticity but nonetheless might influence memory storage at their synapses. To investigate the determinants of such spontaneous fluctuations, we propose a mathematical model for the dynamics of the spine shape and analyze it in 2D—related to experimental microscopic imagery—and in 3D. We show that the spine shape is governed by a local imbalance between membrane tension and the expansive force from actin bundles that originates from discrete actin polymerization foci. Experiments have shown that only few such polymerization foci co-exist at any time in a spine, each having limited life time. The model shows that the momentarily existing set of such foci pushes the membrane along certain directions until foci are replaced and other directions may now be affected. We explore these relations in depth and use our model to predict shape and temporal characteristics of spines from the different biophysical parameters involved in actin polymerization. Approximating the model by a single recursive equation we finally demonstrate that the temporal evolution of the number of active foci is sufficient to predict the size of the model-spines. Thus, our model provides the first platform to study the relation between molecular and morphological properties of the spine with a high degree of biophysical detail.https://www.frontiersin.org/article/10.3389/fnsyn.2020.00009/fulldendritic spinesactinsimulationsmodelspontaneous shape change |
| spellingShingle | Mayte Bonilla-Quintana Florentin Wörgötter Florentin Wörgötter Christian Tetzlaff Christian Tetzlaff Michael Fauth Modeling the Shape of Synaptic Spines by Their Actin Dynamics Frontiers in Synaptic Neuroscience dendritic spines actin simulations model spontaneous shape change |
| title | Modeling the Shape of Synaptic Spines by Their Actin Dynamics |
| title_full | Modeling the Shape of Synaptic Spines by Their Actin Dynamics |
| title_fullStr | Modeling the Shape of Synaptic Spines by Their Actin Dynamics |
| title_full_unstemmed | Modeling the Shape of Synaptic Spines by Their Actin Dynamics |
| title_short | Modeling the Shape of Synaptic Spines by Their Actin Dynamics |
| title_sort | modeling the shape of synaptic spines by their actin dynamics |
| topic | dendritic spines actin simulations model spontaneous shape change |
| url | https://www.frontiersin.org/article/10.3389/fnsyn.2020.00009/full |
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