Miri, A. | bioRxiv Science

bioRxiv2022

Motor cortical influence relies on task-specific activity covariation

During limb movement, spinal circuits facilitate the alternating activation of antagonistic flexor and extensor muscles. Yet antagonist cocontraction is often required to stabilize joints, like when loads are handled. Previous results suggest that these different muscle activation patterns are mediated by separate flexion- and extension-related motor cortical output populations, while others suggest recruitment of task-specific populations. To distinguish between hypotheses, we developed a paradigm in which mice toggle between forelimb tasks requiring antagonist alternation or cocontraction and measured activity in motor cortical layer 5b. Our results conformed to neither hypothesis: consistent flexion- and extension-related activity was not observed across tasks, and no task-specific populations were observed. Instead, activity covariation among motor cortical neurons dramatically changed between tasks, thereby altering the relation between neural and muscle activity. This was also observed specifically for corticospinal neurons. Collectively, our findings indicate that motor cortex drives different muscle activation patterns via task-specific activity covariation. HIGHLIGHTSO_LIMice perform two forelimb tasks involving distinct antagonist muscle activity in a novel paradigm C_LIO_LIL5b motor cortical neurons are not organized by task-specific activity C_LIO_LIL5b motor cortical neurons do not encode muscle activity consistently across tasks C_LIO_LITask-specific muscle activity is driven by a change in motor cortical activity covariation C_LI eTOC BLURBWarriner et al. simultaneously measured muscle and motor cortical activity in mouse during antagonist forelimb muscle alternation and cocontraction, revealing that these distinct muscle activation patterns are not driven through consistent flexion and extension programs nor through the activity of discrete, task-specific neuronal subsets. Instead, distinct patterns involve task-specific changes in firing pattern covariation among layer 5b neurons, and corticospinal neurons in particular, which change their relationship to muscle activity across tasks.

neuroscience↗

bioRxiv2021

Oculomotor plant and neural dynamics suggest gaze control requires integration on distributed timescales

A fundamental principle of biological motor control is that the neural commands driving movement must conform to the response properties of the motor plants they control. In the oculomotor system, characterizations of oculomotor plant dynamics traditionally supported models in which the plant responds to neural drive to extraocular muscles on exclusively short, subsecond timescales. These models predict that the stabilization of gaze during fixations between saccades requires neural drive that approximates eye position on longer timescales and is generated through the temporal integration of brief eye velocity-encoding signals that cause saccades. However, recent measurements of oculomotor plant behaviour have revealed responses on longer timescales. Furthermore, measurements of firing patterns in the oculomotor integrator have revealed a more complex encoding of eye movement dynamics. Yet, the link between these observations has remained unclear. Here we use measurements from the larval zebrafish to link dynamics in the oculomotor plant to dynamics in the neural integrator. The oculomotor plant in both anaesthetized and awake larval zebrafish was characterized by a broad distribution of response timescales, including those much longer than one second. Analysis of the firing patterns of oculomotor integrator neurons, which exhibited a broadly distributed range of decay time constants, demonstrates the sufficiency of this activity for stabilizing gaze given an oculomotor plant with distributed response timescales. This work suggests that leaky integration on multiple, distributed timescales by the oculomotor integrator reflects an inverse model for generating oculomotor commands, and that multi-timescale dynamics may be a general feature of motor circuitry. KEY POINTSO_LIRecent observations of oculomotor plant response properties and neural activity across the oculomotor system have called into question classical formulations of both the oculomotor plant and the oculomotor integrator. C_LIO_LIHere we use measurements from new and published experiments in the larval zebrafish together with modelling to reconcile recent oculomotor plant observations with oculomotor integrator function. C_LIO_LIWe developed computational techniques to characterize oculomotor plant responses over several seconds in awake animals, demonstrating that long timescale responses seen in anesthetized animals extend to the awake state. C_LIO_LIAnalysis of firing patterns of oculomotor integrator neurons demonstrates the sufficiency of this activity for stabilizing gaze given an oculomotor plant with multiple, distributed response timescales. C_LIO_LIOur results support a formulation of gaze stabilization by the oculomotor system in which commands for stabilizing gaze are generated through integration on multiple, distributed timescales. C_LI

neuroscience↗