Rapid 3D Enhanced Resolution Microscopy Reveals Diversity in Dendritic Spinule Dynamics, Regulation, and Function

Zaccard, Colleen R.; Shapiro, Lauren P.; Martín-de-Saavedra, María Dolores; Pratt, Christopher P.; Myczek, Kristoffer; Song, Amy; Forrest, Marc P.; Penzes, Peter

doi:10.1016/j.neuron.2020.04.025

Cited by 30 publications

(32 citation statements)

References 56 publications

(99 reference statements)

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“…Coated pits often are seen at the ends of spinules ( Westrum and Blackstad, 1962 ; Spacek and Harris, 2004 ; Yao et al, 2005 ; Tao-Cheng et al, 2009 ), mediating removal and absorption of spinule ends into the terminal. And recent studies with enhanced resolution 3D light microscopy have confirmed that neuronal activity induces spine-derived spinule elongation ( Zaccard et al, 2020 ).…”

Section: Resultsmentioning

confidence: 96%

“…This is especially true for the smaller spinule types of invaginating structures because they are difficult to identify without TEM, and even with standard 2D TEM, the origins of the invaginating structures are often obscure. Today, super-resolution and other specialized light microscopy techniques allow better visualization of these invaginating structures in synapses ( Ueda and Hayashi, 2013 ; Zaccard et al, 2020 ). Moreover, the new wave of 3D EM methods such as focused ion beam-scanning electron microscopy (FIB-SEM) makes tracing of these invaginating structures possible.…”

Section: Introductionmentioning

confidence: 99%

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Invaginating Structures in Synapses – Perspective

Petralia

Yao

Kapogiannis

et al. 2021

Front. Synaptic Neurosci.

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Invaginating structures are common in the synapses of most animals. However, the details of these invaginating structures remain understudied in part because they are not well resolved in light microscopy and were often misidentified in early electron microscope (EM) studies. Utilizing experimental techniques along with the latest advances in microscopy, such as focused ion beam-scanning EM (FIB-SEM), evidence is gradually building to suggest that the synaptic invaginating structures contribute to synapse development, maintenance, and plasticity. These invaginating structures are most elaborate in synapses mediating rapid integration of signals, such as muscle contraction, mechanoreception, and vision. Here we argue that the synaptic invaginations should be considered in future studies seeking to understand their role in sensory integration and coordination, learning, and memory. We review the various types of invaginating structures in the synapses and discuss their potential functions. We also present several new examples of invaginating structures from a variety of animals including Drosophila and mice, mainly using FIB-SEM, with which we trace the form and arrangement of these structures.

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Section: Resultsmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

Invaginating Structures in Synapses – Perspective

Petralia

Yao

Kapogiannis

et al. 2021

Front. Synaptic Neurosci.

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“…To understand the mechanism of this activity-stability correlation, intracellular Ca 2+ is important for spine formation and stability in cortical pyramidal neurons as shown in ex-vivo preparations 29, 30 where spine lifetime was positively correlated with Ca 2+ peak frequency and duration. Chelating Ca 2+ resulted in lower spine formation, spinule number and cumulative lifespan per spine 29 . When we presented short duration odor, the activity-stability correlation was not induced, although this stimulus did shift the cumulative distributions of stable and new spines, but this did not correlate with individual dendritic activity.…”

Section: Discussionmentioning

confidence: 99%

“…When we presented short duration odor, the activity-stability correlation was not induced, although this stimulus did shift the cumulative distributions of stable and new spines, but this did not correlate with individual dendritic activity. As to the cellular machinery of spine maintenance and formation, spine stability and lifetime are also associated with the gain of PSD-95 31 and its expression complexity 29 , respectively, whereas spine removal is often preceded by PSD-95 loss 31, 32 . Although it has been shown that GC PSD-95 puncta stabilize with odor enrichment 17 , suggesting an overall activity-dependence, our current results support a direct relationship between activity and stability.…”

Section: Discussionmentioning

confidence: 99%

Interneuron activity-structural plasticity association is driven by context-dependent sensory experience

Saha

Meng

Riecke

et al. 2021

Preprint

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Neuronal dendritic spine dynamics provide a plasticity mechanism for altering brain circuit connectivity to integrate new information for learning and memory. Previous in vivo studies in the olfactory bulb (OB) showed that regional increases in activity caused localized spine stability, at a population level, yet how activity affects spine dynamics at an individual neuron level remains unknown. In this study, we tracked in vivo the correlation between an individual neuron’s activity and its dendritic spine dynamics of OB granule cell (GC) interneurons. Odor experience caused a consistent correlation between individual GC activity and spine stability. Dissecting the components of the OB circuit showed that increased principal cell (MC) activity was sufficient to drive this correlation, whereas cell-autonomously driven GC activity had no effect. A mathematical model was able to replicate the GC activity-spine stability correlation and showed MC output having improved odor discriminability while retaining odor memory. These results reveal that GC spine plasticity provides a sufficient network mechanism to decorrelate odors and maintain a memory trace.

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“…Neuronal activity induces long lasting structural modifications in synapses to promote changes in synaptic strength. For example, LTP induction results in the enlargement of dendritic spines and the formation of multi-contact synapses (Hruska et al, 2018;Zaccard et al, 2020), including MIS, a unique form of structural synaptic plasticity. Indeed, formation of MIS is associated with NMDAR-dependent LTP (Nikonenko et al, 2003;Hruska et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Wnt Signaling Through Nitric Oxide Synthase Promotes the Formation of Multi-Innervated Spines

McLeod

Boyle

Marzo

et al. 2020

Front. Synaptic Neurosci.

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Structural plasticity of synapses correlates with changes in synaptic strength. Dynamic modifications in dendritic spine number and size are crucial for long-term potentiation (LTP), the cellular correlate of learning and memory. Recent studies have suggested the generation of multi-innervated spines (MIS), in the form of several excitatory presynaptic inputs onto one spine, are crucial for hippocampal memory storage. However, little is known about the molecular mechanisms underlying MIS formation and their contribution to LTP. Using 3D enhanced resolution confocal images, we examined the contribution of Wnt synaptic modulators in MIS formation in the context of LTP. We show that blockage of endogenous Wnts with specific Wnt antagonists supresses the formation of MIS upon chemical LTP induction in cultured hippocampal neurons. Gain-and lossof-function studies demonstrate that Wnt7a signaling promotes MIS formation through the postsynaptic Wnt scaffold protein Disheveled 1 (Dvl1) by stimulating neuronal nitric oxide (NO) synthase (nNOS). Subsequently, NO activates soluble guanylyl cyclase (sGC) to increase MIS formation. Consistently, we observed an enhanced frequency and amplitude of excitatory postsynaptic currents. Collectively, our findings identify a unique role for Wnt secreted proteins through nNOS/NO/sGC signaling to modulate MIS formation during LTP.

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Rapid 3D Enhanced Resolution Microscopy Reveals Diversity in Dendritic Spinule Dynamics, Regulation, and Function

Cited by 30 publications

References 56 publications

Invaginating Structures in Synapses – Perspective

Invaginating Structures in Synapses – Perspective

Interneuron activity-structural plasticity association is driven by context-dependent sensory experience

Wnt Signaling Through Nitric Oxide Synthase Promotes the Formation of Multi-Innervated Spines

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