Reproducing asymmetrical spine shape fluctuations in a model of actin dynamics predicts self-organized criticality

Bonilla-Quintana, Mayte; Wörgötter, Florentin; D’Este, Elisa; Tetzlaff, Christian; Fauth, Michael

doi:10.1038/s41598-021-83331-9

Cited by 6 publications

(7 citation statements)

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“…The motor walking in the system may not be sufficiently slow to yield SOC behavior, which requires a sharp separation of time scales between slow driving and fast dissipation, and the nonconservative transfer of mechanical energy between network components may also play a role ( 13 , 24 , 46 , 67 , 68 ). We note, however, that recent studies have indicated that branched cytoskeletal networks polymerizing against a flexible membrane can produce shape fluctuations of the membrane that exhibit true SOC, leaving open the question of whether criticality is an inherent feature of cytoskeletal dynamics ( 69 , 70 ).…”

Section: Discussionmentioning

confidence: 92%

Understanding cytoskeletal avalanches using mechanical stability analysis

Floyd

Levine

Jarzynski

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Eukaryotic cells are mechanically supported by a polymer network called the cytoskeleton, which consumes chemical energy to dynamically remodel its structure. Recent experiments in vivo have revealed that this remodeling occasionally happens through anomalously large displacements, reminiscent of earthquakes or avalanches. These cytoskeletal avalanches might indicate that the cytoskeleton’s structural response to a changing cellular environment is highly sensitive, and they are therefore of significant biological interest. However, the physics underlying “cytoquakes” is poorly understood. Here, we use agent-based simulations of cytoskeletal self-organization to study fluctuations in the network’s mechanical energy. We robustly observe non-Gaussian statistics and asymmetrically large rates of energy release compared to accumulation in a minimal cytoskeletal model. The large events of energy release are found to correlate with large, collective displacements of the cytoskeletal filaments. We also find that the changes in the localization of tension and the projections of the network motion onto the vibrational normal modes are asymmetrically distributed for energy release and accumulation. These results imply an avalanche-like process of slow energy storage punctuated by fast, large events of energy release involving a collective network rearrangement. We further show that mechanical instability precedes cytoquake occurrence through a machine-learning model that dynamically forecasts cytoquakes using the vibrational spectrum as input. Our results provide a connection between the cytoquake phenomenon and the network’s mechanical energy and can help guide future investigations of the cytoskeleton’s structural susceptibility.

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Section: Discussionmentioning

confidence: 92%

Understanding cytoskeletal avalanches using mechanical stability analysis

Floyd

Levine

Jarzynski

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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“…New models were proposed to investigate these spontaneous spine shape fluctuations [106,107] and their implications in LTP [14, 107] by continuously changing the membrane according to the actin dynamics. These models couple the biochemical and mechanical properties of dendritic spines, and thus, their function and structure.…”

Section: Models Incorporating Spine Shapementioning

confidence: 99%

“…AMPARs dynamics also span from seconds, in studies of AMPARs lateral diffusion [85], to minutes, when investigating different sources of AMPARs [15,98]. Moreover, models investigating spontaneous fluctuations of spine shape [106,107] or AMPARs [89] can span from seconds to minutes, respectively (figure 2).…”

Section: Design Considerations For Model Buildingmentioning

confidence: 99%

“…Most of the models look at the reactions induced by Ca 2+ influx through NMDARs, but also other sources of calcium such as organelles [17,18]. Moreover, the spatial representation of the dendritic spine also expands from a volume [74] or number of AMPARs readout [75] to the embodiment in static idealized [16-18, 28, 85] and real geometries [99] or motile shapes [14, 106,107].…”

Section: Design Considerations For Model Buildingmentioning

confidence: 99%

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Can biophysical models of dendritic spines be used to explore synaptic changes associated with addiction?

Bonilla-Quintana¹,

Rangamani²

2022

Phys. Biol.

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Effective treatments that prevent or reduce drug relapse vulnerability should be developed to relieve the high burden of drug addiction on society. This will only be possible by enhancing the understanding of the molecular mechanisms underlying the neurobiology of addiction. Recent experimental data have shown that dendritic spines, small protrusions from the dendrites that receive excitatory input, of spiny neurons in the nucleus accumbens exhibit morphological changes during drug exposure and withdrawal. Moreover, these changes relate to the characteristic drug-seeking behavior of addiction. However, due to the complexity of the dendritic spines, we do not yet fully understand the processes underlying their structural changes in response to different inputs. We propose that biophysical models can enhance the current understanding of these processes by incorporating different, and sometimes, discrepant experimental data to identify the shared underlying mechanisms and generate experimentally testable hypotheses. This review aims to give an up-to-date report on biophysical models of dendritic spines, focusing on those models that describe their shape changes, which are well-known to relate to learning and memory. Moreover, it examines how these models can enhance our understanding of the effect of the drugs and the synaptic changes during withdrawal, as well as during neurodegenerative disease progression such as Alzheimer’s disease.

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“…Models linking these findings to single spine dynamics using various approaches already exist 12 , 15 , 22 , 30 , 31 . In this study, we introduce a model that can reproduce both long-term potentiation (LTP)-triggered spine changes and activity-independent spine fluctuations within a common framework.…”

Section: Introductionmentioning

confidence: 99%

Linking spontaneous and stimulated spine dynamics

Eggl,

Chater,

Petkovic

et al. 2023

Commun Biol

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Our brains continuously acquire and store memories through synaptic plasticity. However, spontaneous synaptic changes can also occur and pose a challenge for maintaining stable memories. Despite fluctuations in synapse size, recent studies have shown that key population-level synaptic properties remain stable over time. This raises the question of how local synaptic plasticity affects the global population-level synaptic size distribution and whether individual synapses undergoing plasticity escape the stable distribution to encode specific memories. To address this question, we (i) studied spontaneously evolving spines and (ii) induced synaptic potentiation at selected sites while observing the spine distribution pre- and post-stimulation. We designed a stochastic model to describe how the current size of a synapse affects its future size under baseline and stimulation conditions and how these local effects give rise to population-level synaptic shifts. Our study offers insights into how seemingly spontaneous synaptic fluctuations and local plasticity both contribute to population-level synaptic dynamics.

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Reproducing asymmetrical spine shape fluctuations in a model of actin dynamics predicts self-organized criticality

Cited by 6 publications

References 50 publications

Understanding cytoskeletal avalanches using mechanical stability analysis

Understanding cytoskeletal avalanches using mechanical stability analysis

Can biophysical models of dendritic spines be used to explore synaptic changes associated with addiction?

Linking spontaneous and stimulated spine dynamics

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