Rapid formation and selective stabilization of synapses for enduring motor memories

By Tonghui Xu, Xinzhu Yu, Andrew J. Perlik, Willie F. Tobin, Jonathan A. Zweig, Kelly A. Tennant, Theresa A. Jones, Yi Zuo. 2009

1,174 citations recorded by the source corpus.

Novel motor skills are learned through repetitive practice and, once acquired, persist long after training stops. Earlier studies have shown that such learning induces an increase in the efficacy of synapses in the primary motor cortex, the persistence of which is associated with retention of the task. However, how motor learning affects neuronal circuitry at the level of individual synapses and how long-lasting memory is structurally encoded in the intact brain remain unknown. Here we show that synaptic connections in the living mouse brain rapidly respond to motor-skill learning and permanently rewire. Training in a forelimb reaching task leads to rapid (within an hour) formation of postsynaptic dendritic spines on the output pyramidal neurons in the contralateral motor cortex. Although selective elimination of spines that existed before training gradually returns the overall spine density back to the original level, the new spines induced during learning are preferentially stabilized during subsequent training and endure long after training stops. Furthermore, we show that different motor skills are encoded by different sets of synapses. Practice of novel, but not previously learned, tasks further promotes dendritic spine formation in adulthood. Our findings reveal that rapid, but long-lasting, synaptic reorganization is closely associated with motor learning. The data also suggest that stabilized neuronal connections are the foundation of durable motor memory.

Subfields: Cell Biology, Cellular and Molecular Neuroscience, Cognitive Neuroscience

How researchers see this paper

The researchers whose trusted networks rank it highest, strongest advocate first. Every researcher gets a different order.

In Cell Biology

1. Jan Born
2. Karel Svoboda
3. Ta-Chu Kao
4. J. Noguchi
5. Guillaume Hennequin
6. Haruo Kasai
7. R. Redondo
8. Y. Dudai

In Cellular and Molecular Neuroscience

1. Y. Dudai
2. S. Tonegawa
3. Jan Born
4. E. Kandel
5. M. Mayford
6. Anthony Holtmaat
7. R. Redondo
8. Niels Niethard

In Cognitive Neuroscience

1. Y. Dudai
2. S. Tonegawa
3. Jan Born
4. Gido M. van de Ven
5. E. Kandel
6. M. Mayford
7. Anthony Holtmaat
8. R. Redondo

Citations in the corpus

• Natural continual learning: success is a journey, not (just) a destination (2021, methodology): “This approach can be motivated by findings in the neuroscience literature of increased stability for a subset of synapses after learning (Xu et al., 2009; Yang et al., 2009).”
• Alleviating catastrophic forgetting using context-dependent gating and synaptic stabilization (2018, methodology): “Particularly, skill acquisition and retention is associated with the creation and stabilization of dendritic spines (Yang et al., 2009; Xu et al., 2009).”
• Dynamic reconfiguration of human brain networks during learning (2010, neutral): “ζ ≡∑ t0−1 t1⁄4t0 Uðt;tþ 1Þ t0 − t0 − 1 ; [3]”
• Astrocytes Control Synapse Formation, Function, and Elimination (2015, positive): “…formation Thrombospondin Positive Induces glutamatergic synapse formation; secreted by astrocytes Christopherson et al. 2005; Eroglu et al. 2009; Xu et al. 2009a; Garcia et al. 2010; Hughes et al. Thrombospondin Positive and negative Increases synaptic glycine receptors; decreases synaptic AMPA…”
• Experience-dependent structural synaptic plasticity in the mammalian brain (2009, background): “Training in a forelimb reaching task rapidly induced the growth of new dendritic spines, which were preferentially stabilized by subsequent training session”
• The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture. (2011, background): “Mice, like rats, use their forepaws in an extremely dexterous manner and this capacity is increasingly capitalized upon for studies of motor skill learning (e.g., Tucci et al. 2007; Xu et al. 2009) and”
• Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning (2013, neutral): “unlike the MWM it involves cerebellum and motor cortex 17,18 , and not the hippocampus.”
• The restless engram: consolidations never end. (2012, background): “Rodent models and the application of in vivo two-photon microscopy to image dendritic spine dynamics (Xu et al., 2009; Yang et al., 2009; reviewed in Yu and Zuo, 2011) show that at the cellular level, training leads to rapid formation of enduring postsynaptic dendritic spines on the output pyramidal”
• A theory for how sensorimotor skills are learned and retained in noisy and nonstationary neural circuits (2013, background): “Why should dendritic spines come in and out of existence even when there is no overt learning? Will perpetual synaptic flux destabilize a learning system and erase old memories? A pair of recent two-photon microscopy studies looked at the addition and subtraction of dendritic spines in the primary m”
• The Consolidation and Transformation of Memory. (2015, neutral): “Rodent models and the application of in vivo two-photon microscopy to image dendritic spine dynamics (Xu et al., 2009; Yang et al., 2009; reviewed in Yu and Zuo, 2011) show that at”
• Memory Engram Cells Have Come of Age. (2015, positive): “In one study (Xu et al., 2009), training in a forelimb reaching task resulted in rapid (within an hour) formation of post-synaptic dendritic spines on the output pyramidal neurons in the motor cortex.”