Targeted stimulation of motor cortex neural ensembles drives learned movements

Kavli Affiliate: Takaki Komiyama

| Authors: An Wu, Qiyu Chen, Bin Yu, Soyoung Chae, Zijing Tan, Assaf Ramot and Takaki Komiyama

| Summary:

During the execution of learned motor skills, the neural population in the layer 2/3 (L2/3) of the primary motor cortex (M1) expresses a reproducible spatiotemporal activity pattern. It is debated whether M1 actively participates in generating the activity pattern or it only passively reflects patterned inputs. Furthermore, it is unclear whether this learned activity pattern causally drives the learned movement. We addressed these issues using in vivo two-photon calcium imaging combined with holographic optogenetic stimulation of specific ensembles of M1 L2/3 neurons in mice engaged in a skilled lever-press task. We briefly and synchronously stimulated ~20 neurons whose activity onset in voluntary trials precedes movement onsets. This stimulation, despite lacking temporal patterns, induced movements that resembled the learned movement, while producing spatiotemporal activity patterns in other M1 neurons not directly stimulated that resembled the activity during the voluntary learned movement. Trial-by-trial variability of optogenetically triggered population activity in the non-target neurons correlated with the variability in the induced movements. These trial-by-trial variabilities were predicted by the initial state of M1 population activity immediately preceding the optogenetic stimulation. Stimulation of the neurons whose activity followed voluntary movement onsets failed to induce the learned movement. Thus, the learned activity pattern in M1 L2/3 can be generated when the M1 network is prepared at the optimal initial state and receives precise triggering inputs, supporting the active role of M1 in learned activity generation. The resulting activity pattern then causally drives the learned movement.

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