Human cognition involves the dynamic integration of neural activity and neuromodulatory systems

• Published in: Nature neuroscience 2019-02, Vol.22 (2), p.289-296
• Main Authors: Shine, James M., Breakspear, Michael, Bell, Peter T., Ehgoetz Martens, Kaylena A., Shine, Richard, Koyejo, Oluwasanmi, Sporns, Olaf, Poldrack, Russell A.
• Format: Article
• Language: English
• Subjects: 45; 59/36; 631/208/199; 631/378/2649; 631/553/2712; Adult; Analysis; Animal Genetics and Genomics; Behavioral Sciences; Biological Techniques; Biomedical and Life Sciences; Biomedicine; Brain; Brain - diagnostic imaging; Brain - physiology; Brain architecture; Brain Mapping; Brain research; Cognition; Cognition & reasoning; Cognition - physiology; Cognitive ability; Cognitive neuroscience; Cognitive tasks; Cognitive tests; Connectome; Controllability; Datasets; Environmental changes; Female; Fluid intelligence; Functional morphology; Gambling; Gene expression; Humans; Integration; Intelligence; Magnetic Resonance Imaging; Male; Mathematical functions; Models, Neurological; Natural language processing; Nerve Net - diagnostic imaging; Nerve Net - physiology; Neurobiology; Neuromodulation; Neurons; Neurons - physiology; Neuropsychological Tests; Neurosciences; Principal components analysis; Receptors; Signatures; Time series; Topology
• ISSN: 1097-6256; 1546-1726
• DOI: 10.1038/s41593-018-0312-0

The human brain integrates diverse cognitive processes into a coherent whole, shifting fluidly as a function of changing environmental demands. Despite recent progress, the neurobiological mechanisms responsible for this dynamic system-level integration remain poorly understood. Here we investigated the spatial, dynamic, and molecular signatures of system-wide neural activity across a range of cognitive tasks. We found that neuronal activity converged onto a low-dimensional manifold that facilitates the execution of diverse task states. Flow within this attractor space was associated with dissociable cognitive functions, unique patterns of network-level topology, and individual differences in fluid intelligence. The axes of the low-dimensional neurocognitive architecture aligned with regional differences in the density of neuromodulatory receptors, which in turn relate to distinct signatures of network controllability estimated from the structural connectome. These results advance our understanding of functional brain organization by emphasizing the interface between neural activity, neuromodulatory systems, and cognitive function. Neuronal activity across task states converges onto a low-dimensional manifold. Flow within this attractor space covaries with network-level topology, fluid intelligence, and regional differences in the density of neuromodulatory receptors.