Abstract
Dendritic spines change their size and shape spontaneously, but the function of this remains unclear. Here, we address this in a biophysical model of spine fluctuations, which reproduces experimentally measured spine fluctuations. For this, we characterize size- and shape fluctuations from confocal microscopy image sequences using autoregressive models and a new set of shape descriptors derived from circular statistics. Using the biophysical model, we extrapolate into longer temporal intervals and find the presence of 1/f noise. When investigating its origins, the model predicts that the actin dynamics underlying shape fluctuations self-organizes into a critical state, which creates a fine balance between static actin filaments and free monomers. In a comparison against a non-critical model, we show that this state facilitates spine enlargement, which happens after LTP induction. Thus, ongoing spine shape fluctuations might be necessary to react quickly to plasticity events.
Highlights
Dendritic spines change their size and shape spontaneously, but the function of this remains unclear
The model allows us to predict spine characteristics for periods of time that exceed those currently accessible experimentally. Analyzing such long time intervals, we find that the spine fluctuations exhibit 1/f noise, which can be explained by the actin polymerization dynamics that occurs in bursts (“avalanches”) from specific polymerization foci
To investigate the influence of actin dynamics on the spine shape fluctuations, we adapted and extended our previously published m odel[14], in which asymmetric shape fluctuations emerge from an imbalance between an expanding force generated by actin polymerization and a force generated by the lipid membrane, that counteracts shape deformations (Fig. 1b)
Summary
Dendritic spines change their size and shape spontaneously, but the function of this remains unclear. Bonilla-Quintana et al.[14] proposed an actin based model that mimics rapid spine motility of around 100 ms To date it remains unclear whether these rapid shape fluctuations have a possible function and, if they have, which function they fulfill[15]. We use a biologically realistic theoretical model to study rapid, spontaneous shape fluctuations of dendritic spines generated by the dynamics of actin, observed by Fisher et al.[2] and o thers[3,4,5]. The model allows us to predict spine characteristics for periods of time that exceed those currently accessible experimentally Analyzing such long time intervals, we find that the spine fluctuations exhibit 1/f noise, which can be explained by the actin polymerization dynamics that occurs in bursts (“avalanches”) from specific polymerization foci. The model further predicts that these polymerization dynamics self-organizes into
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