Plasticity of Spine Structure: Local Signaling, Translation and Cytoskeletal Reorganization

Abstract

Dendritic spines are small protrusive structures on dendritic surfaces, and function as postsynaptic compartments for excitatory synapses. Plasticity of spine structure is associated with many forms of long-term neuronal plasticity, learning and memory. Inside these small dendritic compartments, biochemical states and protein-protein interactions are dynamically modulated by synaptic activity, leading to the regulation of protein synthesis and reorganization of cytoskeletal architecture. This in turn causes plasticity of structure and function of the spine. Technical advances in monitoring molecular behaviors in single dendritic spines have revealed that each signaling pathway is differently regulated across multiple spatiotemporal domains. The spatial pattern of signaling activity expands from a single spine to the nearby dendritic area, dendritic branch and the nucleus, regulating different cellular events at each spatial scale. Temporally, biochemical events are typically triggered by short Ca2+ pulses (~10–100 ms). However, these signals can then trigger activation of downstream protein cascades that can last from milliseconds to hours. Recent imaging studies provide many insights into the biochemical processes governing signaling events of molecular assemblies at different spatial localizations. Here, we highlight recent findings of signaling dynamics during synaptic plasticity and discuss their roles in long-term structural plasticity of dendritic spines.

Co‐administration of ethanol and nicotine heightens sensitivity to ethanol reward within the nucleus accumbens (NAc) shell and increasing NAc shell BDNF is sufficient to enhance ethanol reward in naïve Wistar rats

“…BDNF is part of the neurotrophin family and via binding with tropomyosin receptor kinase B (TrkB) promotes neuronal development, modulates synaptic function, and regulates synaptic plasticity (Park and Poo ; Nakahata and Yasuda ). A number of studies have examined BDNF in response to acute exposure, seeking, dependence, and relapse to EtOH or NIC (Logrip et al ; Machaalani and Chen ).…”

Alcohol causes lasting differential transcription inDrosophilamushroom body neurons

“…Second, nuclear RNA from neurons contributes to the integrity of the active transcriptome snapshot by minimizing contamination from mRNA stored in the cytoplasm, along dendrites, and within axons, while allowing for the detection of experience-dependent differential expression (LACAR et al 2016). Finally, given evidence that mRNA handling in subcellular compartments has been implicated in the formation and storage of memory (BRAMHAM AND WELLS 2007;RICHTER 2010;SHIGEOKA et al 2016;NAKAHATA AND YASUDA 2018;BIEVER et al 2019), this approach provides a robust profile of the stable post-exposure transcriptome unencumbered by the diversity of whole cell RNA.…”

Myosin 18Aα targets guanine nucleotide exchange factor β-Pix to dendritic spines of cerebellar Purkinje neurons to promote spine maturation

“…Actin filaments comprise the major structural element of spines, and changes in spine size and shape that occur upon synapse usage are thought to result largely from changes in spine actin content, organization and dynamics (Yuste and Bonhoeffer, 2001;Lamprecht and LeDoux, 2004;Matsuzaki et al, 2004;Okamoto et al, 2004;Bourne and Harris, 2008;Holtmaat and Svoboda, 2009;Newpher and Ehlers, 2009). Moreover, these actin-dependent changes in spine morphology (structural plasticity) are thought to promote the long-lasting changes in synaptic strength (functional plasticity) that underlie learning and memory (Kasai et al, 2010;Roberts et al, 2010;Fortin, Srivastava and Soderling, 2012;Hlushchenko, Koskinen and Hotulainen, 2016;Basu and Lamprecht, 2018;Nakahata and Yasuda, 2018). Consistently, many learning and memory disorders (e.g.…”

“…Dendritic spines are small protrusions on the surface of neuronal dendrites that form the postsynaptic component of most excitatory synapses in the brain, function as signaling microcompartments, and serve as the primary site of memory formation (Yuste and Bonhoeffer, 2001;Okamoto et al, 2004;Lamprecht and LeDoux, 2004;Matsuzaki et al, 2004;Bourne and Harris, 2008;Holtmaat and Svoboda, 2009;Newpher and Ehlers, 2009;Roberts et al, 2010;Kasai et al, 2010;Fortin, Srivastava and Soderling, 2012;Hlushchenko, Koskinen and Hotulainen, 2016;Basu and Lamprecht, 2018;Nakahata and Yasuda, 2018). Actin filaments comprise the major structural element of spines, and changes in spine size and shape that occur upon synapse usage are thought to result largely from changes in spine actin content, organization and dynamics (Yuste and Bonhoeffer, 2001;Lamprecht and LeDoux, 2004;Matsuzaki et al, 2004;Okamoto et al, 2004;Bourne and Harris, 2008;Holtmaat and Svoboda, 2009;Newpher and Ehlers, 2009).…”