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Rapid formation and selective stabilization of synapses for enduring motor memories - PubMed

  • ️Thu Jan 01 2009

. 2009 Dec 17;462(7275):915-9.

doi: 10.1038/nature08389. Epub 2009 Nov 29.

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Rapid formation and selective stabilization of synapses for enduring motor memories

Tonghui Xu et al. Nature. 2009.

Abstract

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.

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Figures

Figure 1
Figure 1. Motor skill learning in adolescent mice promotes immediate spine formation in the contralateral motor cortex

a, A cartoon of motor training. b, Average success rates during training for learning and non-learning mice (mean ± s.e.m., 42 learners and 5 no learners). c, An intracortical microstimulation map indicates that the imaged region is within the motor cortex. Scale bar, 1 mm. d, e, Repeated imaging of the same dendritic branches over one-day intervals reveals spine elimination (arrows) and formation (arrowheads), and filopodia (asterisks) in a general control (d) and a trained (e) mouse. Scale bar, 2 μm. f, Percentage of spines formed and eliminated under various control and training conditions immediately following the first training session (mean ± s.d., ***P < 0.001). g, The degree of spine formation observed following the first training session is linearly correlated with the number of successful reaches during this session (r2 = 0.77).

Figure 2
Figure 2. Enhanced spine dynamics during adolescent motor training is region- and learning-specific

a, b, Percentage of spines formed (a) and eliminated (b) under control and training conditions. c, Total spine number increases during initial learning, but returns to normal levels with prolonged training. d, e, Imaging of the same dendritic branches over 4 days in the ipsilateral primary motor cortex (d) and the contralateral sensory cortex (e) of the trained mice. f, Imaging of the same dendritic branches over 4 days in the contralateral motor cortex of a mouse that failed to learn the task. Data are presented as mean ± s.d., *P < 0.05, **P < 0.01, ***P < 0.001. Scale bar, 2 μm.

Figure 3
Figure 3. Motor skill learning stabilizes newly formed spines

a, Timeline of experiments, showing possible outcomes. b, c, Repeated imaging of dendritic branches at 0, 4 and 120 days in a control (b) and a trained (c) mouse. Scale bar, 2 μm. d, Percentages of surviving new and pre-existing spines, as a function of time, for control and trained animals (mean ± s.d., *P < 0.05 and ***P < 0.001). Numbers of animals examined at each time point are indicated below new spine data points.

Figure 4
Figure 4. Novel motor skill training promotes spine formation and elimination in adult mice

a, Pre-trained mice start with high success rates during adult retraining (mean ± s.e.m., 10 naive trained and 14 retrained adults).b–f, Repetitive imaging of dendritic branches over 4 days in a control adult (b), naive adults training with the reaching task (c) and capellini handling task (d), and pre-trained adults retraining with the same reaching task and the new capellini handling task (f). Scale bar, 2 μm. g, Percentages of spines formed and eliminated over 4 days in adult mice under different conditions (mean ± s.d., ***P < 0.001).

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