Motor Skill Training Induces Coordinated Strengthening and Weakening between Neighboring Synapses

Lee, Kea Joo; Park, In Sung; Kim, H.; Greenough, William T.; Pak, Daniel T.S.; Rhyu, Im Joo

doi:10.1523/jneurosci.0848-12.2013

Cited by 45 publications

(53 citation statements)

References 39 publications

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“…There is an alternative scenario where local differences in post-synaptic b-catenin level between spines of different neurons could bias their competition for a common pre-synaptic axonal terminus (Holtmaat and Svoboda, 2009;Knott et al, 2006;Lee et al, 2013). Deducing from our inter-spine competition model, we would expect that between such neighboring neurons, the one with higher total b-catenin level would be advantaged and thus have a higher spine density.…”

Section: Inter-spine Competition For B-catenin Biases Spine Fatementioning

confidence: 96%

Coordinated Spine Pruning and Maturation Mediated by Inter-Spine Competition for Cadherin/Catenin Complexes

Bian

Miao

et al. 2015

Cell

145

128

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Dendritic spines are postsynaptic compartments of excitatory synapses that undergo dynamic changes during development, including rapid spinogenesis in early postnatal life and significant pruning during adolescence. Spine pruning defects have been implicated in developmental neurological disorders such as autism, yet much remains to be uncovered regarding its molecular mechanism. Here, we show that spine pruning and maturation in the mouse somatosensory cortex are coordinated via the cadherin/catenin cell adhesion complex and bidrectionally regulated by sensory experience. We further demonstrate that locally enhancing cadherin/catenin-dependent adhesion or photo-stimulating a contacting channelrhodopsin-expressing axon stabilized the manipulated spine and eliminated its neighbors, an effect requiring cadherin/catenin-dependent adhesion. Importantly, we show that differential cadherin/catenin-dependent adhesion between neighboring spines biased spine fate in vivo. These results suggest that activity-induced inter-spine competition for β-catenin provides specificity for concurrent spine maturation and elimination and thus is critical for the molecular control of spine pruning during neural circuit refinement.

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Section: Inter-spine Competition For B-catenin Biases Spine Fatementioning

confidence: 96%

Coordinated Spine Pruning and Maturation Mediated by Inter-Spine Competition for Cadherin/Catenin Complexes

Bian

Miao

et al. 2015

Cell

145

128

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show abstract

“…Images of the same widow were taken 3, 6, and 10 days after the surgery. the deep cerebellar nuclei, and the structural plasticity of Purkinje cell spines has been of great interest (Black et al 1990;Cesa et al 2005Cesa et al , 2007Kleim et al 1998;Lee et al 2007Lee et al , 2013Sdrulla and Linden 2007;Sugawara et al 2013). However, because of the small size and high density of spines, single spines are not reliably resolved in vivo even with two-photon microscopy.…”

Section: Discussionmentioning

confidence: 99%

Long-term in vivo time-lapse imaging of synapse development and plasticity in the cerebellum

Nishiyama

Colonna

Shen

et al. 2014

Journal of Neurophysiology

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Synapses are continuously formed and eliminated throughout life in the mammalian brain, and emerging evidence suggests that this structural plasticity underlies experience-dependent changes of brain functions such as learning and long-term memory formation. However, it is generally difficult to understand how the rewiring of synaptic circuitry observed in vivo eventually relates to changes in animal's behavior. This is because afferent/efferent connections and local synaptic circuitries are very complicated in most brain regions, hence it is largely unclear how sensorimotor information is conveyed, integrated, and processed through a brain region that is imaged. The cerebellar cortex provides a particularly useful model to challenge this problem because of its simple and welldefined synaptic circuitry. However, owing to the technical difficulty of chronic in vivo imaging in the cerebellum, it remains unclear how cerebellar neurons dynamically change their structures over a long period of time. Here, we showed that the commonly used method for neocortical in vivo imaging was not ideal for long-term imaging of cerebellar neurons, but simple optimization of the procedure significantly improved the success rate and the maximum time window of chronic imaging. The optimized method can be used in both neonatal and adult mice and allows time-lapse imaging of cerebellar neurons for more than 5 mo in ϳ80% of animals. This method allows vital observation of dynamic cellular processes such as developmental refinement of synaptic circuitry as well as long-term changes of neuronal structures in adult cerebellum under longitudinal behavioral manipulations.long-term, time-lapse imaging; two-photon microscopy; development; plasticity IN VIVO TIME-LAPSE MICROSCOPY is now extensively used for imaging fine neuronal structures and activity in the brain of living animals. These experiments have revealed the dynamic nature of synaptic wiring and functional architecture of neuronal ensembles, providing novel insights into experience-dependent changes of brain functions (Bhatt et al. 2009;Chen and Nedivi 2010;Huber et al. 2012). However, it is generally difficult to understand how the formation and elimination of synapses modify the function of local brain circuitry, and eventually, an animal's behavior.The cerebellum provides a unique advantage to challenge this problem. Unlike most other brain regions, extensively characterized anatomical and physiological properties of cerebellar neurons provide testable models regarding how sensorimotor information is conveyed and integrated, and how plas-

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“…At the ultrastructural level, parallel fiber-to-Purkinje cell synapses can be categorized into three types by their distinct synaptic contact features (Kim et al, 2002;Lee et al, 2013a) (Figure 2). Single-synapse boutons (SSBs), contacting one postsynaptic dendritic spine, are most commonly observed, although multiple-synapse boutons (MSBs), contacting spine pairs of Purkinje cells, are also frequently detected.…”

Section: Multiple-synapse Boutons: Learning-induced Local Synaptic Stmentioning

confidence: 99%

“…New evidence suggests that neighboring synapses must be finely regulated to enhance signal-to-noise ratio, allowing appropriate information storage in the brain. Here, we review motor learning-induced synaptic plasticity in the cerebellar cortex and explore the emerging concept that synergistic strengthening and weakening of neighboring synapses in a local dendritic segment is essential for optimal encoding of complex motor skills (Lee et al, 2013a). This line of investigation also led us to propose that coordinated remodeling between nearby synapses is important to homeostatically maintain overall activity levels within local dendritic segments relatively stable.…”

Section: Introduction: Motor Learning and Synapse Plasticity In The Cmentioning

confidence: 99%

Synapses need coordination to learn motor skills

Lee¹,

Rhyu²,

Pak³

2014

Reviews in the Neurosciences

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Motor Skill Training Induces Coordinated Strengthening and Weakening between Neighboring Synapses

Cited by 45 publications

References 39 publications

Coordinated Spine Pruning and Maturation Mediated by Inter-Spine Competition for Cadherin/Catenin Complexes

Coordinated Spine Pruning and Maturation Mediated by Inter-Spine Competition for Cadherin/Catenin Complexes

Long-term in vivo time-lapse imaging of synapse development and plasticity in the cerebellum

Synapses need coordination to learn motor skills

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