Adaptive circuit dynamics across human cortex during evidence accumulation in changing environments

• Published in: Nature neuroscience Vol. 24; no. 7; pp. 987 - 997
• Main Authors: Murphy, Peter R., Wilming, Niklas, Hernandez-Bocanegra, Diana C., Prat-Ortega, Genis, Donner, Tobias H.
• Format: Journal Article
• Language: English
• Published: New York Nature Publishing Group US 01.07.2021; Nature Publishing Group
• Subjects: 631/378/116/1925; 631/378/2649/1409; 631/378/2649/1723; 631/378/3920; Accumulation; Adult; Animal Genetics and Genomics; Arousal; Behavioral Sciences; Bioaccumulation; Biological Techniques; Biomedical and Life Sciences; Biomedicine; Brain research; Cerebral Cortex - physiology; Changing environments; Computation; Cortex (parietal); Decision making; Decision Making - physiology; Feedback; Female; Human acts; Human behavior; Humans; Magnetoencephalography; Male; Models, Neurological; Motor cortex; Neural circuitry; Neurobiology; Neurosciences; Optimization; Physiological aspects; Psychological aspects; Reinforcement; Somatosensory cortex; Temporal cortex; Visual cortex; Germany
• ISSN: 1097-6256; 1546-1726; 1546-1726
• DOI: 10.1038/s41593-021-00839-z

Many decisions under uncertainty entail the temporal accumulation of evidence that informs about the state of the environment. When environments are subject to hidden changes in their state, maximizing accuracy and reward requires non-linear accumulation of evidence. How this adaptive, non-linear computation is realized in the brain is unknown. We analyzed human behavior and cortical population activity (measured with magnetoencephalography) recorded during visual evidence accumulation in a changing environment. Behavior and decision-related activity in cortical regions involved in action planning exhibited hallmarks of adaptive evidence accumulation, which could also be implemented by a recurrent cortical microcircuit. Decision dynamics in action-encoding parietal and frontal regions were mirrored in a frequency-specific modulation of the state of the visual cortex that depended on pupil-linked arousal and the expected probability of change. These findings link normative decision computations to recurrent cortical circuit dynamics and highlight the adaptive nature of decision-related feedback to the sensory cortex. Optimal decision making in a changing world requires non-linear evidence accumulation. Murphy et al. report signatures of this adaptive computation in recurrent dynamics of human parietal and motor cortices, accompanied by feedback to sensory cortex.