Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning - PubMed (original) (raw)

Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning

Jeffrey A Kleim et al. J Neurosci. 2004.

Abstract

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.

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Figures

Figure 1.

Figure 1.

A, Performance of animals on the skilled reaching task after 3, 7, or10 d of training. Closed circles represent performance on the first day of training (Baseline), and open squares represent performance on the last day of training (Test). In comparison with baseline levels, all animals showed a significant increase in the percentage of successful reaches on the test day (*p < 0.05; Student's dependent t test). B, Performance on the last day of training for all three training durations. Reaching accuracy did not significantly differ between the 7 and 10 d animals, but both were significantly higher than the 3 d animals (*p < 0.05; Fisher's PLSD).

Figure 2.

Figure 2.

Representative motor maps from SRC and URC animals after 3, 7, and 10 d of training. SRC animals exhibited a significant increase in the proportion of the CFA occupied by distal movement (green) representations in comparison with URC animals after 10 d of training. URC animals had a significantly greater proportion of CFA occupied by proximal movement (blue) than SRC animals after 10 d of training. Vibrissae representations are shown in purple, head/neck representations are shown in yellow, and nonresponse sites are shown in gray. Bregma is indicated by a red line.

Figure 3.

Figure 3.

Left, Total area of the CFA in SRC and URC animals in the three different training schedules. The mean percentage of the CFA ± SEM occupied by distal (middle) and proximal (right) forelimb movement representations. SRC animals had a significantly greater proportion of the CFA occupied by distal movement representations than the URC animals after 10 d of training (*p < 0.05; Fisher's PLSD). Conversely, URC animals had a significantly greater proportion of the CFA occupied by proximal movement representations than SRC animals after 10 d (*p < 0.05; PLSD).

Figure 4.

Figure 4.

Neuron density (Nvneuron) (A), synapse density (Nvsynapse) (B), and number of synapses per neuron (Syn/Neuron) (C) within layer V of the CFA. SRC animals had a significantly lower density of neurons than URC animals after 7 and 10 d of training (*p < 0.05; Fisher's PLSD). No significant differences in synapse density were found between SRC and URC animals in any of the three training schedules. SRC animals had significantly more synapses per neuron than URC animals after 7 and 10 d of training (*p < 0.05; Fisher's PLSD).

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