Task-Driven Activity Reduces the Cortical Activity Space of the Brain: Experiment and Whole-Brain Modeling

How a stimulus or a task alters the spontaneous dynamics of the brain remains a fundamental open question in neuroscience. One of the most robust hallmarks of task/stimulus-driven brain dynamics is the decrease of variability with respect to the spontaneous level, an effect seen across multiple experimental conditions and in brain signals observed at different spatiotemporal scales. Recently, it was observed that the trial-to-trial variability and temporal variance of functional magnetic resonance imaging (fMRI) signals decrease in the task-driven activity. Here we examined the dynamics of a large-scale model of the human cortex to provide a mechanistic understanding of these observations. The model allows computing the statistics of synaptic activity in the spontaneous condition and in putative tasks determined by external inputs to a given subset of brain regions. We demonstrated that external inputs decrease the variance, increase the covariances, and decrease the autocovariance of synaptic activity as a consequence of single node and large-scale network dynamics. Altogether, these changes in network statistics imply a reduction of entropy, meaning that the spontaneous synaptic activity outlines a larger multidimensional activity space than does the task-driven activity. We tested this model’s prediction on fMRI signals from healthy humans acquired during rest and task conditions and found a significant decrease of entropy in the stimulus-driven activity. Altogether, our study proposes a mechanism for increasing the information capacity of brain networks by enlarging the volume of possible activity configurations at rest and reliably settling into a confined stimulus-driven state to allow better transmission of stimulus-related information.Author Summary: Task- or stimulus-related changes of brain dynamics have been the subject of intense investigation during the last years. One of the most robust hallmarks of task/stimulus-driven brain dynamics, as measured using diverse recording techniques, is the decrease of variability with respect to the spontaneous level. This has led several researchers to focus on the second-order statistics of evoked activity and to study their functional consequences for information processing. In particular, it was observed that the trial-to-trial variability (related to variable responses to an identical stimulus from one presentation to the next) and the temporal variance of functional magnetic resonance imaging (fMRI) signals decrease in the task-driven activity. Here, we built a computational model of the whole brain to understand how local and large-scale brain dynamics contribute to these effects. The model allowed us to derive equations for the network statistics of both spontaneous and evoked activity. We observed that, as a consequence of single node and network dynamics, stimulus input impacts network statistics in such a way that the entropy of the stimulus-driven activity is lower than that during spontaneous activity. We confirmed this model prediction using empirical fMRI data and we further discuss its functional implications.