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Extended practice of a motor skill is associated with reduced metabolic activity in M1.

Picard N, Matsuzaka Y, Strick PL - Nat. Neurosci. (2013)

Bottom Line: After extended practice, we observed a profound reduction of metabolic activity in M1 for the performance of internally generated compared to visually guided tasks.These findings suggest that the development of skill through extended practice results in a reduction in the synaptic activity required to produce internally generated, but not visually guided, sequences of movements.Thus, practice leading to skilled performance results in more efficient generation of neuronal activity in M1.

View Article: PubMed Central - PubMed

Affiliation: Center for the Neural Basis of Cognition and Systems Neuroscience Institute, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.

ABSTRACT
How does long-term training and the development of motor skills modify the activity of the primary motor cortex (M1)? To address this issue, we trained monkeys for ~1-6 years to perform visually guided and internally generated sequences of reaching movements. Then, we used [(14)C]2-deoxyglucose (2DG) uptake and single-neuron recording to measure metabolic and neuron activity in M1. After extended practice, we observed a profound reduction of metabolic activity in M1 for the performance of internally generated compared to visually guided tasks. In contrast, measures of neuron firing displayed little difference during the two tasks. These findings suggest that the development of skill through extended practice results in a reduction in the synaptic activity required to produce internally generated, but not visually guided, sequences of movements. Thus, practice leading to skilled performance results in more efficient generation of neuronal activity in M1.

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Activation during the Random and Repeating tasks. Each panel shows the 2DG uptake in M1 of one animal who performed the Random (a,b) or Repeating (c,d) task for the 2DG experiment. See Fig. 1 for conventions. Monkeys N15 (b) and N14 (d) were involved in single neuron recording as well as 2DG experiments. For monkey N15, numbers mark penetrations in regions of high (1) and lower (2) 2DG uptake. The activity of some neurons recorded at these penetration sites is illustrated in Supplementary Figs. 2–3. For monkey N14, letters mark penetrations in regions of high (a) and lower (b) 2DG uptake. The activity of some neurons recorded at these penetration sites is illustrated in Supplementary Figs. 4–5.
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Figure 3: Activation during the Random and Repeating tasks. Each panel shows the 2DG uptake in M1 of one animal who performed the Random (a,b) or Repeating (c,d) task for the 2DG experiment. See Fig. 1 for conventions. Monkeys N15 (b) and N14 (d) were involved in single neuron recording as well as 2DG experiments. For monkey N15, numbers mark penetrations in regions of high (1) and lower (2) 2DG uptake. The activity of some neurons recorded at these penetration sites is illustrated in Supplementary Figs. 2–3. For monkey N14, letters mark penetrations in regions of high (a) and lower (b) 2DG uptake. The activity of some neurons recorded at these penetration sites is illustrated in Supplementary Figs. 4–5.

Mentions: We compared the average 2DG uptake in arm M1 on the precentral gyrus and in the anterior bank of the central sulcus during the tasks (2-way ANOVA with post-hoc comparison of means and Bonferroni correction). Task was a significant factor for 2DG uptake in arm M1 (d.f. = 4, 14, p < 0.01 × 10−4), as was area (gyrus, sulcus) (d.f. = 1, 14, p = 0.02). There was no interaction between task and area (d.f. = 4, 14, p = 0.48). Compared to the Lick task, there was marked 2DG uptake in arm M1 during visually-guided reaching movements (Fig. 2a–b, Fig. 3a–b, Table 1 (ANOVA, d.f. = 4, 14; Track vs Lick, p = 0.01 × 10−4; Random vs Lick, p = 0.05 × 10−4).


Extended practice of a motor skill is associated with reduced metabolic activity in M1.

Picard N, Matsuzaka Y, Strick PL - Nat. Neurosci. (2013)

Activation during the Random and Repeating tasks. Each panel shows the 2DG uptake in M1 of one animal who performed the Random (a,b) or Repeating (c,d) task for the 2DG experiment. See Fig. 1 for conventions. Monkeys N15 (b) and N14 (d) were involved in single neuron recording as well as 2DG experiments. For monkey N15, numbers mark penetrations in regions of high (1) and lower (2) 2DG uptake. The activity of some neurons recorded at these penetration sites is illustrated in Supplementary Figs. 2–3. For monkey N14, letters mark penetrations in regions of high (a) and lower (b) 2DG uptake. The activity of some neurons recorded at these penetration sites is illustrated in Supplementary Figs. 4–5.
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Related In: Results  -  Collection

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Figure 3: Activation during the Random and Repeating tasks. Each panel shows the 2DG uptake in M1 of one animal who performed the Random (a,b) or Repeating (c,d) task for the 2DG experiment. See Fig. 1 for conventions. Monkeys N15 (b) and N14 (d) were involved in single neuron recording as well as 2DG experiments. For monkey N15, numbers mark penetrations in regions of high (1) and lower (2) 2DG uptake. The activity of some neurons recorded at these penetration sites is illustrated in Supplementary Figs. 2–3. For monkey N14, letters mark penetrations in regions of high (a) and lower (b) 2DG uptake. The activity of some neurons recorded at these penetration sites is illustrated in Supplementary Figs. 4–5.
Mentions: We compared the average 2DG uptake in arm M1 on the precentral gyrus and in the anterior bank of the central sulcus during the tasks (2-way ANOVA with post-hoc comparison of means and Bonferroni correction). Task was a significant factor for 2DG uptake in arm M1 (d.f. = 4, 14, p < 0.01 × 10−4), as was area (gyrus, sulcus) (d.f. = 1, 14, p = 0.02). There was no interaction between task and area (d.f. = 4, 14, p = 0.48). Compared to the Lick task, there was marked 2DG uptake in arm M1 during visually-guided reaching movements (Fig. 2a–b, Fig. 3a–b, Table 1 (ANOVA, d.f. = 4, 14; Track vs Lick, p = 0.01 × 10−4; Random vs Lick, p = 0.05 × 10−4).

Bottom Line: After extended practice, we observed a profound reduction of metabolic activity in M1 for the performance of internally generated compared to visually guided tasks.These findings suggest that the development of skill through extended practice results in a reduction in the synaptic activity required to produce internally generated, but not visually guided, sequences of movements.Thus, practice leading to skilled performance results in more efficient generation of neuronal activity in M1.

View Article: PubMed Central - PubMed

Affiliation: Center for the Neural Basis of Cognition and Systems Neuroscience Institute, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.

ABSTRACT
How does long-term training and the development of motor skills modify the activity of the primary motor cortex (M1)? To address this issue, we trained monkeys for ~1-6 years to perform visually guided and internally generated sequences of reaching movements. Then, we used [(14)C]2-deoxyglucose (2DG) uptake and single-neuron recording to measure metabolic and neuron activity in M1. After extended practice, we observed a profound reduction of metabolic activity in M1 for the performance of internally generated compared to visually guided tasks. In contrast, measures of neuron firing displayed little difference during the two tasks. These findings suggest that the development of skill through extended practice results in a reduction in the synaptic activity required to produce internally generated, but not visually guided, sequences of movements. Thus, practice leading to skilled performance results in more efficient generation of neuronal activity in M1.

Show MeSH