Disengagement of motor cortex from movement control during long-term learning

Abstract

Motor learning involves reorganization of the primary motor cortex (M1). However, it remains unclear how the involvement of M1 in movement control changes during long-term learning. To address this, we trained mice in a forelimb-based motor task over months and performed optogenetic inactivation and two-photon calcium imaging in M1 during the long-term training. We found that M1 inactivation impaired the forelimb movements in the early and middle stages, but not in the late stage, indicating that the movements that initially required M1 became independent of M1. As previously shown, M1 population activity became more consistent across trials from the early to middle stage while task performance rapidly improved. However, from the middle to late stage, M1 population activity became again variable despite consistent expert behaviors. This later decline in activity consistency suggests dissociation between M1 and movements. These findings suggest that long-term motor learning can disengage M1 from movement control.

Remembrance of things practiced: Fast and slow learning in cortical and subcortical pathways

“…Second, because motor cortex plays less of a role in driving striatum as behaviors become highly practiced, lesioning, inactivating, or randomly perturbing activity in motor cortex during behavior should have a decreasingly small effect on the behavior the more that it has been trained (Figure 7b). This effect has in fact already been observed in very recent experiments using optogenetic inactivation throughout learning of a targeted forelimb task [48].…”

“…As described in the previous section, the transfer of control from corticostriatal to thalamostriatal inputs would suggest that motor cortex should be necessary for the initial learning of a behavior, but not for the production of the behavior after a sufficient amount of practice. Evidence for this has recently been found in studies using lesions [47] or inactivations [48] to test the involvement of motor cortex in rodents performing skilled forelimb tasks. In addition, studies of learned motor behaviors in humans have suggested that motor cortex becomes less involved in driving behaviors with practice [49,50], consistent with the proposed sensorimotor implementation of the two-pathway model.…”

Multi-dimensional tuning in motor cortical neurons during active behavior

“…For instance, skill learning, disease or trauma can induce experiencedependent changes in motor cortical representations, including expansions of motor maps that may reflect functional reorganization to support newly learned movements (Sanes and Donoghue, 2000;Li et al, 2001;Conner et al, 2005;Xu et al, 2009;Makino et al, 2016;Peters et al, 2017;Papale and Hooks, 2018). Moreover, while the necessity of motor cortex for performance of learned skills can vary depending on factors such as the level of dexterity required or the amount of time spent training, motor cortex is required for the acquisition of new motor skills across a variety of movements and training paradigms (Whishaw et al, 1991;Whishaw, 2000;Darling et al, 2011;Guo et al, 2015;Kawai et al, 2015;Hwang et al, 2019).…”

A distributed neocortical action map associated with reach-to-grasp

“…Within the context of motor control, our findings also encourage to study the role of areas found to be active during movement (such as the visual areas) commonly disregarded in the association to forelimb movement, at the cellular-level (Galiñanes et al, 2018, Karandell and Huber, 2017, Ebina et al, 2018). In the future, it would also be relevant to assess the neocortical dynamics during RtG in a freely moving condition or during performance refinement, considering that cortical areas undergo functional reorganization during learning (Makino et al, 2017; Whishaw et al, 2017; Bollu et al, 2019; Hwang et al, 2019). In sum, our investigation identified a global network of neocortical area associated to successful RtG execution.…”