Cortical Synaptogenesis and Motor Map Reorganization Occur during Late, But Not Early, Phase of Motor Skill Learning

By J. Kleim, T. M. Hogg, P. VandenBerg, N. R. Cooper, R. Bruneau, M. Remple. Journal of Neuroscience, 2004

611 citations recorded by the source corpus.

Extensive motor skill training induces reorganization of movement representations and synaptogenesis within adult motor cortex. Motor skill does not, however, develop uniformly across training sessions. It is characterized by an initial fast phase, followed by a later slow phase of learning. How cortical plasticity emerges during these phases is unknown. Here, we examine motor map topography and synapse number within rat motor cortex during the early and late phases of motor learning. Adult rats were placed in either a skilled or unskilled reaching condition (SRC and URC, respectively) for 3, 7, or 10 d. Intracortical microstimulation of layer V was used to determine the topography of forelimb movement representations within caudal forelimb area of motor cortex contralateral to the trained paw. Quantitative electron microscopy was used to measure the number of synapses per neuron within layer V. SRC animals showed significant increases in reaching accuracy after 3, 7, and 10 d of training. In comparison with URC animals, SRC animals had significantly larger distal forelimb representations after 10 d of training only. Furthermore, SRC animals had significantly more synapses per neuron than URC animals after 7 and 10 d of training. These results show that both motor map reorganization and synapse formation occur during the late phase of skill learning. Furthermore, synaptogenesis precedes map reorganization. We propose that motor map reorganization and synapse formation do not contribute to the initial acquisition of motor skills but represent the consolidation of motor skill that occurs during late stages of training.

Subfields: Cognitive Neuroscience

View Paper: https://www.semanticscholar.org/paper/52df550e79f054b658d04e86e06cbc22de03be39

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In Cognitive Neuroscience

Citations in the corpus

Human functional neuroimaging of brain changes associated with practice. (2005, background): “A number of researchers suggest that there is a particular signature of neural change associated with practice in primary motor or sensory cortex (e.g. Hikosaka et al., 1998; Karni et al., 1998; Hikosaka et al., 2002; Ungerleider et al., 2002; Korman et al., 2003; Kleim et al., 2004).”
The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture. (2011, background): “While we did not see an effect of 17--21 days of behavioral training on the motor map, map changes are slow to occur and require repetitive practice to instigate (Kleim et al. 2004; Adkins et al. 2006), and recent data indicate that a substantially longer duration of training on these tests results ”
Spine Plasticity in the Motor Cortex (2010, result): “For example, EM analysis has indicated that motor learning has no effect on synapse density, but increases the synapse/neuron ratio in both layer II/III and layer V motor cortex contralateral to the trained forelimb [1,25].”
Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill (2009, neutral): “0 0 5 10 Naive, 14 (7) Early, 14 (9) Late, 16 (6) DLS”
Activity-dependent structural plasticity. (2009, background): “Kleim et al. (2002, 2004) reported a specific enlargement of the cortical paw representation (at the expense of foreleg representation, which shrinks) associated with synapse formation after seven days of motor skill learning.”
Differential Modulation of Motor Cortical Plasticity and Excitability in Early and Late Phases of Human Motor Learning (2007, background): “It is thought that different mechanisms support these short- and long-term learning processes (Karni et al., 1998; Kleim et al., 2004).”
Sleep-Dependent Reactivation of Ensembles in Motor Cortex Promotes Skill Consolidation (2015, background): “By contrast, later phases of skill learning seem to be more strongly associated with changes within motor cortex [31,41,64,64] and between dorso-lateral striatum (i.”
Frontiers in Computational Neuroscience a Model for Cortical Rewiring following Deafferentation and Focal Stroke (2009, neutral): “…in an activity-dependent fashion during development (Hensch, 2005; Mrsic-Flogel et al., 2007), following a lesion (Darian-Smith and Gilbert, 1995; Giannikopoulos and Eysel, 2006; Merzenich et al., 1984) and due to extensive training (Bangert and Altenmüller, 2003; Kleim et al., 2002, 2004, 2007).”
Neuroplasticity subserving motor skill learning (2011, neutral): “On the other hand, it should be noted that other animal studies demonstrated significant increases in synapse numbers in the rat M1 only after extensive training (Kleim et al., 1996, 2004).”