The geometry of domain-general performance monitoring in the human medial frontal cortex

• Published in: Science (American Association for the Advancement of Science) Vol. 376; no. 6593; p. eabm9922
• Main Authors: Fu, Zhongzheng, Beam, Danielle, Chung, Jeffrey M., Reed, Chrystal M., Mamelak, Adam N., Adolphs, Ralph, Rutishauser, Ueli
• Format: Journal Article
• Language: English
• Published: United States The American Association for the Advancement of Science 06.05.2022
• Subjects: Adaptation; Bayesian analysis; Brain; Clinical trials; Cognitive ability; Cognitive tasks; Cortex (cingulate); Cortex (frontal); Diffusion rate; Drift; Drift rate; Epilepsy; Frontal Lobe - physiology; Generalization; Geometry; Human performance; Humans; Invariants; Mathematical models; Monitoring; Neurons; Neurosurgery; Patients; Population; Population Distribution; Populations; Probability; Psychomotor Performance - physiology; Representations; Retrospective Studies; Specialization; Supplementary motor area; Task complexity
• ISSN: 0036-8075; 1095-9203; 1095-9203
• DOI: 10.1126/science.abm9922

Controlling behavior to flexibly achieve desired goals depends on the ability to monitor one’s own performance. It is unknown how performance monitoring can be both flexible, to support different tasks, and specialized, to perform each task well. We recorded single neurons in the human medial frontal cortex while subjects performed two tasks that involve three types of cognitive conflict. Neurons encoding conflict probability, conflict, and error in one or both tasks were intermixed, forming a representational geometry that simultaneously allowed task specialization and generalization. Neurons encoding conflict retrospectively served to update internal estimates of conflict probability. Population representations of conflict were compositional. These findings reveal how representations of evaluative signals can be both abstract and task-specific and suggest a neuronal mechanism for estimating control demand. What are the neural mechanisms that enable humans to flexibly control and monitor their own actions in various non-routine and novel tasks? Fu et al . recorded the activity of more than 1000 neurons in the medial frontal cortex of human epilepsy patients while they performed complex cognitive tasks. They found that domain-general and domain-specific performance monitoring neurons were intermixed within this brain region. The population activity gave rise to a geometry that allowed domain-general signals to be read out with more than 90% accuracy on single trials while at the same time retaining the ability to separate different conflict conditions. These results show how the human medial frontal cortex resolves the fundamental trade-off between task generalization and specialization, which is critical for cognitive flexibility. —PRS Representations of evaluative signals in human frontal cortex are both abstract and task specific.