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

Abstract

As skill on a sequence of movements is acquired through practice, each movement in the sequence becomes seamlessly associated with another. To study the neural basis of acquired skills, we trained two monkeys (Cebus apella) to perform two sequential reaching tasks. In one task, sequential movements were instructed by visual cues, whereas in the other task, movements were generated from memory after extended practice. Then, we examined neural activity in the dorsal premotor area (PMd) and the effects of its local inactivation during performance of each task. Comparable numbers of neurons in the PMd were active during the two tasks. However, inactivation of the PMd had a marked effect only on the performance of sequential movements that were guided by memory. These results emphasize the importance of the PMd in the internal generation of sequential movements, perhaps through maintaining arbitrary motor-motor associations.

The Role of the Dorsal Premotor Cortex in Skilled Action Sequences

“…Indeed, the finding that PMd inactivation did not impair visually guided sequence performance appears to be in stark contrast with previous accounts of PMd involvement in controlling basic movement kinematics (Caminiti et al, 1991;Davare et al, 2015) and visually guided movements (Johnson et al, 1996). However, we believe that this apparent discrepancy may be explained by the presence of constant visual feedback during the task used by Ohbayashi et al (2016), which, by allowing on-line correction of movement kinematics, may have concealed subtle inaccuracies in the initial movement parameters (Archambault et al, 2015;Davare et al, 2015). Given that the task design used in this study allowed the authors to measure only the accuracy and timing of the movement end point, but not of the whole trajectory, these disruptions of the reaching movement parameters could have gone unnoticed (Fig.…”

“…Electrophysiological and lesion studies in monkeys, along with virtual lesion studies and neuroimaging data in humans, have shown that both the primary motor cortex (Lu and Ashe, 2005;Matsuzaka et al, 2007) and the non-primary motor cortex (Tanji and Shima, 1994;Wiestler and Diedrichsen, 2013;Wymbs and Grafton, 2013) are involved in sequential actions. Similar to other complex skills, movement sequences arise from multifaceted neural processing (Hardwick et al, 2013) involving the storage of the sequence in memory, the preparation of the movement kinematics, and the on-line movement correction.…”

“…One such study was recently conducted by Ohbayashi et al (2016), who investigated the role of dorsal premotor cortex (PMd) in the execution of internally generated and visually guided sequences. Two monkeys were trained to execute visually cued movements, which were either random or belonged to a set of extensively trained sequences.…”

“…However, cell specificity was not determined according to statistical significance but following a liberal attribution criterion, making it difficult to determine the importance of the reported tuning properties. Therefore, Ohbayashi et al (2016) used the GABA agonist muscimol to disrupt PMd activity to examine whether this brain region plays a causal role in sequence encoding. Importantly, they found that PMd inactivation led to reductions in the number of anticipatory movements and to increases in spatial error only during the execution of highly practiced sequences, suggesting that this region is involved in the control of internally generated sequences, but not visually guided movements.…”

“…As discussed by Ohbayashi et al (2016), their study provides a new perspective on the specific role of PMd in sequence encoding by questioning the importance of the supplementary motor area (SMA) to this function (Tanji and Shima, 1994). The authors propose to frame the functional roles of the two areas in terms of spatial and temporal sequence processing for PMd and SMA, respectively (Ohbayashi et al, 2016).…”