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Motor cortex activity across movement speeds is predicted by network-level strategies for generating muscle activity.

ABSTRACT: Learned movements can be skillfully performed at different paces. What neural strategies produce this flexibility? Can they be predicted and understood by network modeling? We trained monkeys to perform a cycling task at different speeds, and trained artificial recurrent networks to generate the empirical muscle-activity patterns. Network solutions reflected the principle that smooth well-behaved dynamics require low trajectory tangling. Network solutions had a consistent form, which yielded quantitative and qualitative predictions. To evaluate predictions, we analyzed motor cortex activity recorded during the same task. Responses supported the hypothesis that the dominant neural signals reflect not muscle activity, but network-level strategies for generating muscle activity. Single-neuron responses were better accounted for by network activity than by muscle activity. Similarly, neural population trajectories shared their organization not with muscle trajectories, but with network solutions. Thus, cortical activity could be understood based on the need to generate muscle activity via dynamics that allow smooth, robust control over movement speed.

SUBMITTER: Saxena S

PROVIDER: S-EPMC9197394 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Motor cortex activity across movement speeds is predicted by network-level strategies for generating muscle activity.

Saxena Shreya S Russo Abigail A AA Cunningham John J Churchland Mark M MM

eLife 20220527

Learned movements can be skillfully performed at different paces. What neural strategies produce this flexibility? Can they be predicted and understood by network modeling? We trained monkeys to perform a cycling task at different speeds, and trained artificial recurrent networks to generate the empirical muscle-activity patterns. Network solutions reflected the principle that smooth well-behaved dynamics require low trajectory tangling. Network solutions had a consistent form, which yielded qua ...[more]

PMID: 35621264

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Project description:BackgroundOne of the mechanisms responsible for enhancing muscular hypertrophy is the high metabolic stress associated with a reduced muscular oxygenation occurring during exercise, which can be achieved by reducing the speed of movement. Studies have tested that lowered muscle oxygenation artificially induced by an inflatable cuff, could provoke changes in prefrontal cortex oxygenation, hence, to central fatigue. It was hypothesized that (1) exercising with a slow speed of movement would result in greater increase in cerebral and greater decrease in muscle oxygenation compared with exercises of faster speed and (2) the amount of oxygenation increase in the ipsilateral prefrontal cortex would be lower than the contralateral one.MethodsAn ISS Imagent frequency domain near infrared spectroscopy (NIRS) system was used to quantify oxygenation changes in the vastus lateralis muscle and prefrontal cortex (contra- and ipsilateral) during unilateral resistance exercises with different speeds of movement to voluntary fatigue. After one maximal repetition (1RM) test, eight subjects performed three sets of unilateral knee extensions (∼50% of 1RM), separated by 2 min rest periods, following the pace of 1 s, 3 s and 5 s for both concentric and eccentric phases, in a random order, during separate sessions. The amount of change for NIRS parameters for muscle (ΔHb: deoxyhemoglobin, ΔHbO: oxyhemoglobin, ΔHbT: total hemoglobin, ΔStO2: oxygen saturation) were quantified and compared between conditions and sets by two-way ANOVA RM. Differences in NIRS parameters between contra- and ipsilateral (lobe) prefrontal cortex and conditions were tested.ResultsExercising with slow speed of movement was associated to larger muscle deoxygenation than normal speed of movement, as revealed by significant interaction (set × condition) for ΔHb (p = 0.01), and by significant main effects of condition for ΔHbO (p = 0.007) and ΔStO2 (p = 0.016). With regards to the prefrontal cortex, contralateral lobe showed larger oxygenation increase than the ipsilateral one for ΔHb, ΔHbO, ΔHbT, ΔStO2 in each set (main effect of lobe: p < 0.05). Main effects of condition were significant only in set1 for all the parameters, and significant interaction lobe × condition was found only for ΔHb in set1 (p < 0.05).DiscussionThese findings provided evidence that speed of movement influences the amount of muscle oxygenation. Since the lack of oxygen in muscle is associated to increased metabolic stress, manipulating the speed of movement may be useful in planning resistance-training programs. Moreover, consistent oxygenation increases in both right and left prefrontal lobes were found, suggesting a complementary interaction between the ipsi- and contralateral prefrontal cortex, which also seems related to fatigue.

Dataset Information

Motor cortex activity across movement speeds is predicted by network-level strategies for generating muscle activity.

Publications

Motor cortex activity across movement speeds is predicted by network-level strategies for generating muscle activity.

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