Single-trial neural dynamics are dominated by richly varied movements

• Published in: Nature neuroscience Vol. 22; no. 10; pp. 1677 - 1686
• Main Authors: Musall, Simon, Kaufman, Matthew T., Juavinett, Ashley L., Gluf, Steven, Churchland, Anne K.
• Format: Journal Article
• Language: English
• Published: New York Nature Publishing Group US 01.10.2019; Nature Publishing Group
• Subjects: 14/63; 14/69; 631/378; 631/378/116/2395; 631/378/2649; 631/378/2649/1409; 64/60; Analysis; Animal cognition; Animal Genetics and Genomics; Animals; Auditory Perception - physiology; Behavioral Sciences; Biological Techniques; Biomedical and Life Sciences; Biomedicine; Cerebral Cortex - diagnostic imaging; Cerebral Cortex - physiology; Cognition; Cognition - physiology; Cognitive ability; Cognitive tasks; Decision making; Decision Making - physiology; Human mechanics; Laboratories; Linear Models; Mice; Mice, Inbred C57BL; Movement - physiology; Neural circuitry; Neurobiology; Neuroimaging; Neurons - physiology; Neurosciences; Physiological aspects; Psychological aspects; Psychomotor Performance - physiology; Variables; Variation; Visual Perception - physiology; United States
• ISSN: 1097-6256; 1546-1726
• DOI: 10.1038/s41593-019-0502-4

When experts are immersed in a task, do their brains prioritize task-related activity? Most efforts to understand neural activity during well-learned tasks focus on cognitive computations and task-related movements. We wondered whether task-performing animals explore a broader movement landscape and how this impacts neural activity. We characterized movements using video and other sensors and measured neural activity using widefield and two-photon imaging. Cortex-wide activity was dominated by movements, especially uninstructed movements not required for the task. Some uninstructed movements were aligned to trial events. Accounting for them revealed that neurons with similar trial-averaged activity often reflected utterly different combinations of cognitive and movement variables. Other movements occurred idiosyncratically, accounting for trial-by-trial fluctuations that are often considered ‘noise’. This held true throughout task-learning and for extracellular Neuropixels recordings that included subcortical areas. Our observations argue that animals execute expert decisions while performing richly varied, uninstructed movements that profoundly shape neural activity. The authors use a linear model to reveal how neural activity patterns are related to cognition or movements. They find that uninstructed movements dominate single-cell and population activity throughout the brain, outpacing task-related activity.