Modes of cognition: evidence from metastable brain dynamics

Abstract

Managing cognitive load depends on adequate resource allocation by the human brain through the engagement of metastable substates, which are large-scale functional networks that change over time. We employed a novel analysis method, deep autoencoder dynamical analysis (DADA), with 100 healthy adults selected from the Human Connectome Project (HCP) data set in rest and six cognitive tasks. The deep autoencoder of DADA described seven recurrent stochastic metastable substates from the functional connectome of BOLD phase coherence matrices. These substates were significantly differentiated in terms of their probability of appearance, time duration, and spatial attributes. We found that during different cognitive tasks, there was a higher probability of having more connected substates dominated by a high degree of connectivity in the thalamus. In addition, compared with those during tasks, resting brain dynamics have a lower level of predictability, indicating a more uniform distribution of metastability between substates, quantified by higher entropy. These novel findings provide empirical evidence for the philosophically motivated cognitive theory, suggesting on-line and off-line as two fundamentally distinct modes of cognition. On-line cognition refers to task-dependent engagement with the sensory input, while off-line cognition is a slower, environmentally detached mode engaged with decision and planning. Overall, the DADA framework provides a bridge between neuroscience and cognitive theory that can be further explored in the future.

G.D. was supported by the Spanish Research Project AWAKENING: using whole-brain models perturbational approaches for predicting external stimulation to force transitions between different brain states, ref. PID2019-105772GB-I00 /AEI/10.13039/501100011033, financed by the Spanish Ministry of Science, Innovation and Universities (MCIU), State Research Agency (AEI); and K.C and G.D. were also supported by the European Union's Horizon 2020 FET Flagship Human Brain Project (grant agreement number 945539, HBP SGA3). M.L.K. was supported by the ERC Consolidator Grant: CAREGIVING (No. 615539), Center for Music in the Brain, funded by the Danish National Research Foundation (DNRF117), and Centre for Eudaimonia and Human Flourishing funded by the Pettit and Carlsberg Foundations.