Abstract
Modeling studies suggest that clustered structural plasticity of dendritic spines is an efficient mechanism of information storage in cortical circuits. However, why new clustered spines occur in specific locations and how their formation relates to learning and memory (L&M) remain unclear. Using in vivo two-photon microscopy, we track spine dynamics in retrosplenial cortex before, during, and after two forms of episodic-like learning and find that spine turnover before learning predicts future L&M performance, as well as the localization and rates of spine clustering. Consistent with the idea that these measures are causally related, a genetic manipulation that enhances spine turnover also enhances both L&M and spine clustering. Biophysically inspired modeling suggests turnover increases clustering, network sparsity, and memory capacity. These results support a hotspot model where spine turnover is the driver for localization of clustered spine formation, which serves to modulate network function, thus influencing storage capacity and L&M.
Highlights
Modeling studies suggest that clustered structural plasticity of dendritic spines is an efficient mechanism of information storage in cortical circuits
We used in vivo two-photon microscopy to image spines in retrosplenial cortex (RSC) in Thy1-YFP-H mice and coupled this with a contextual fear conditioning (CFC) protocol (Fig. 1a, b) that produced a gradual increase in contextual freezing over 5 days of training (Fig. 1c)
There was individual variability in the pre-learning spine turnover ratio as measured in two imaging sessions before commencement of training. We found that this pre-learning turnover ratio correlated with levels of future contextual learning and memory (Fig. 1d) as well as learning rate (Supplementary Fig. 1a, c), though no association was found between spine turnover and animal age within the range tested (Supplementary Fig. 2; see Supplementary Fig. 3a, b for correlation of pre-learning turnover and freezing through training)
Summary
Modeling studies suggest that clustered structural plasticity of dendritic spines is an efficient mechanism of information storage in cortical circuits. These findings support the hypothesis that clustering of plasticity events within dendrites is a means to efficiently store information[2,7,19,20] Both spine turnover and spine clustering are shown to impact learning and memory, it remains unclear how spine turnover and clustered spine addition relate to one and other and how these subcellular processes influence neural network function. We used transcranial two-photon microscopy to track spine dynamics, and examined the relation between basal spine turnover, contextual or spatial learning and memory, and subsequent spine clustering in the mouse retrosplenial cortex (RSC). RSC is an ideal cortical structure in which to examine the effects of contextual and spatial learning on spine dynamics
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