Cell-Type-Specific Outcome Representation in the Primary Motor Cortex

Abstract

Highlights d Populations of layer 2-3 pyramidal neurons in M1 report motor performance outcome d Success and failure activity is late, prolonged, and dissociated from kinematics and reward d At trial start, layer 5 pyramidal tract activity is affected by previous outcome d Post-movement activity in M1 is required for motor performance and learning

Reward boosts reinforcement-based motor learning

“…Consistent with a dissociable role of reinforcement and reward in motor learning, previous research has shown that certain subpopulations of neurons in the motor cortex ( i.e. , a key region of the motor learning network; Krakauer et al, 2019) are responsive to the outcome of previous movements irrespective of reward (Levy et al, 2020), while others respond to reward regardless of the previous outcome (Ramkumar et al, 2016). Put together, these elements indicate that estimating the net impact of reward on motor learning requires controlling for the effect of the reinforcement feedback on the learning process.…”

Spatiotemporal organization of movement-invariant and movement-specific signaling in the output layer of motor cortex

“…Volitional forelimb movements are thought to be represented by relatively dense activity patterns in both superficial and deep layers of motor cortex (Dacre et al, 2019;Estebanez et al, 2017;Hira et al, 2013;Isomura et al, 2009;Levy et al, 2020;Park et al, 2019;Sauerbrei et al, 2019;Wang et al, 2017), but whether these patterns represent specific actions (Galiñanes et al, 2018) or a more generalised motor signal (Kaufman et al, 2016) remains unresolved. By combining population imaging with single neuron / population-based classifiers and dimensionality reduction in mice, we find that most layer 5B neurons display actioninvariant signalling, while action-specific representations are restricted to sparse, spatially heterogeneous subpopulations of neurons.…”

“…In rodents, volitional forelimb movements such as reach-to-grasp (Estebanez et al, 2017;Galiñanes et al, 2018;Guo et al, 2015;Levy et al, 2020;Sauerbrei et al, 2019;Wang et al, 2017) or pulling / pushing a grasped lever (Dacre et al, 2019;Hira et al, 2013;Isomura et al, 2009;Miri et al, 2017;Morandell and Huber, 2017;Park et al, 2019) have been associated with widespread, bidirectional neuronal modulation in both superficial and deep layers of sensorimotor cortex, driven by long-range inputs from motor thalamus (Dacre et al, 2019;Sauerbrei et al, 2019;Tanaka et al, 2018). Both excitatory and inhibitory neurons display dense task-related activity which emerges across learning and correlates with enhanced limb coordination (Hwang et al, 2019;Laubach et al, 2000;Masamizu et al, 2014;Peters et al, 2014).…”

“…Given the high trial-to-trial variability in ∆F/F0 and resultant moderate decoding scores in individual neurons (see Figure 2I), we reasoned that population responses could provide a more robust movement-related signal that would enhance decoding of action type (Levy et al, 2020;Masamizu et al, 2014;Wei et al, 2019). By applying logistic regression ( Figure 3A Figure 3B).…”

“…Recent advances in viral tools and optical imaging have enabled access to laminar-specific spatiotemporal dynamics of interconnected neuronal populations in rodent motor cortex (Park et al, 2019;Peters et al, 2014;Peters et al, 2017;Wang et al, 2017). During the execution of single forelimb actions, principal neurons in both superficial and deep layers display dense activity patterns that causally relate to the initiation and/or ongoing evolution of movements (Dacre et al, 2019;Estebanez et al, 2017;Hira et al, 2013;Isomura et al, 2009;Levy et al, 2020;Park et al, 2019;Sauerbrei et al, 2019;Wang et al, 2017). These reproducible, laminar-specific activity patterns emerge across motor learning and correlate with enhanced limb coordination (Laubach et al, 2000;Masamizu et al, 2014;Peters et al, 2014;Peters et al, 2017).…”