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

Abstract

How does long-term training and the development of motor skill 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.

Inactivation of the Dorsal Premotor Area Disrupts Internally Generated, But Not Visually Guided, Sequential Movements

“…We demonstrated recently that extended practice on a Repeating sequence results in dramatic alterations in the functional activation and neural responses of M1 (Matsuzaka et al, 2007;Picard et al, 2013). The current results are consistent with the PMd functioning as a major source of input to M1 to guide the performance of internally generated sequences.…”

“…The current results are consistent with the PMd functioning as a major source of input to M1 to guide the performance of internally generated sequences. This conclusion is surprising given the longstanding view that the preparation for and generation of sequential movements depends on the SMA and the pre-SMA (Roland et al, 1980;Tanji and Shima, 1994;Gerloff et al, 1997;Nakamura et al, 1998;Shima and Tanji, 1998;Picard and Strick, 2001;Hikosaka et al, 2002;Dayan and Cohen, 2011). Thus, our results raise an important question: how do the SMA and PMd differ in their contributions to sequential movement control?…”

“…We defined task-related neurons as single units that displayed phasic increases or decreases in discharge temporally coupled to the performance of the task (Matsuzaka et al, 2007;Picard et al, 2013). To compare data from the two tasks, we limited our analysis during the Random task to the same moves that were performed during the Repeating task (e.g., to moves 5 to 3, 3 to 1, .…”

“…Two monkeys (Cebus apella, one male weighing 3.2 kg; one female weighing 1.5 kg) were trained to perform two tasks that required sequential reaching movements with their right arms (Matsuzaka et al, 2007;Picard et al, 2013). Because the two tasks have been described in detail previously, they will only be presented here briefly (Fig.…”

“…In contrast, the supplementary motor area (SMA) and the adjacent pre-SMA have generally been regarded as the cortical areas responsible for the internal generation of sequential movements (Roland et al, 1980;Tanji and Shima, 1994;Gerloff et al, 1997;Nakamura et al, 1998;Shima and Tanji, 1998;Picard and Strick, 2001;Hikosaka et al, 2002;Dayan and Cohen, 2011). Therefore, to explore the function of the PMd, we trained two monkeys to perform two sequential reaching tasks.…”