SearcharxivSearch

arXiv subjects

Eli J. Cornblath

Publications and source records attributed to Eli J. Cornblath.

5 recordsLinked to original sources

The information content of brain states is explained by structural constraints on state energetics

Signal propagation along the structural connectome of the brain induces changes in the patterns of activity. These activity patterns define global brain states and contain information in accordance with their expected probability of occurrence. The structural connectome, in conjunction with the dynamics, determines the set of possible brain states and constrains the transition between accessible states. Yet, precisely how these structural constraints on state-transitions relate to their information content remains unexplored. To address this gap in knowledge, we defined the information content as a function of the activation distribution, where statistically rare values of activation correspond to high information content. With this numerical definition in hand, we studied the spatiotemporal distribution of information content in fMRI data from the Human Connectome Project during different tasks, and report four key findings. First, information content strongly depends on the cognitive task. Second, while information content shows similarities to other measures of brain activity, it is distinct from both Neurosynth maps and task contrast maps generated by a general linear model applied to the fMRI data. Third, the brain's structural wiring constrains the cost to control its state, where the cost to transition into high information content states is larger than that to transition into low information content states. Finally, all state transitions - especially those to high information content states - are less costly than expected from random network null models, thereby indicating the brain's marked efficiency. Taken together, our findings establish an explanatory link between the information contained in a brain state and the energetic cost of attaining that state, thereby laying important groundwork for our understanding of large-scale cognitive computations.

q-bio.NC

Is the brain macroscopically linear? A system identification of resting state dynamics

A central challenge in the computational modeling of neural dynamics is the trade-off between accuracy and simplicity. At the level of individual neurons, nonlinear dynamics are both experimentally established and essential for neuronal functioning. An implicit assumption has thus formed that an accurate computational model of whole-brain dynamics must also be highly nonlinear, whereas linear models may provide a first-order approximation. Here, we provide a rigorous and data-driven investigation of this hypothesis at the level of whole-brain blood-oxygen-level-dependent (BOLD) and macroscopic field potential dynamics by leveraging the theory of system identification. Using functional MRI (fMRI) and intracranial EEG (iEEG), we model the resting state activity of 700 subjects in the Human Connectome Project (HCP) and 122 subjects from the Restoring Active Memory (RAM) project using state-of-the-art linear and nonlinear model families. We assess relative model fit using predictive power, computational complexity, and the extent of residual dynamics unexplained by the model. Contrary to our expectations, linear auto-regressive models achieve the best measures across all three metrics, eliminating the trade-off between accuracy and simplicity. To understand and explain this linearity, we highlight four properties of macroscopic neurodynamics which can counteract or mask microscopic nonlinear dynamics: averaging over space, averaging over time, observation noise, and limited data samples. Whereas the latter two are technological limitations and can improve in the future, the former two are inherent to aggregated macroscopic brain activity. Our results, together with the unparalleled interpretability of linear models, can greatly facilitate our understanding of macroscopic neural dynamics and the principled design of model-based interventions for the treatment of neuropsychiatric disorders.

q-bio.NC

Broken detailed balance and entropy production in the human brain

Living systems break detailed balance at small scales, consuming energy and producing entropy in the environment in order to perform molecular and cellular functions. However, it remains unclear how broken detailed balance manifests at macroscopic scales, and how such dynamics support higher-order biological functions. Here we present a framework to quantify broken detailed balance by measuring entropy production in macroscopic systems. We apply our method to the human brain, an organ whose immense metabolic consumption drives a diverse range of cognitive functions. Using whole-brain imaging data, we demonstrate that the brain nearly obeys detailed balance when at rest, but strongly breaks detailed balance when performing physically and cognitively demanding tasks. Using a dynamic Ising model, we show that these large-scale violations of detailed balance can emerge from fine-scale asymmetries in the interactions between elements, a known feature of neural systems. Together, these results suggest that violations of detailed balance are vital for cognition, and provide a general tool for quantifying entropy production in macroscopic systems.

physics.bio-ph

Temporal sequences of brain activity at rest are constrained by white matter structure and modulated by cognitive demands

A diverse white matter network and finely tuned neuronal membrane properties allow the brain to transition seamlessly between cognitive states. However, it remains unclear how static structural connections guide the temporal progression of large-scale brain activity patterns in different cognitive states. Here, we analyze the brain's trajectories through a high-dimensional activity space at the level of single time point activity patterns from functional magnetic resonance imaging data acquired during passive visual fixation (rest) and an n-back working memory task. We find that specific state space trajectories, which represent temporal sequences of brain activity, are modulated by cognitive load and related to task performance. Using diffusion-weighted imaging acquired from the same subjects, we use tools from network control theory to show that linear spread of activity along white matter connections constrains the brain's state space trajectories at rest. Additionally, accounting for stimulus-driven visual inputs explains the different trajectories taken during the n-back task. We also used models of network rewiring to show that these findings are the result of non-trivial geometric and topological properties of white matter architecture. Finally, we examine associations between age and time-resolved brain state dynamics, revealing new insights into functional changes in the default mode and executive control networks. Overall, these results elucidate the structural underpinnings of cognitively and developmentally relevant spatiotemporal brain dynamics.

q-bio.NC

Sex differences in network controllability as a predictor of executive function in youth

Executive function emerges late in development and displays different developmental trends in males and females. Sex differences in executive function in youth have been linked to vulnerability to psychopathology as well as to behaviors that impinge on health. Yet, the neurobiological basis of these differences is not well understood. Here we test the hypothesis that sex differences in executive function in youth stem from sex differences in the controllability of structural brain networks as they rewire over development. Combining methods from network neuroscience and network control theory, we characterize the network control properties of structural brain networks estimated from diffusion imaging data acquired in males and females in a sample of 882 youth aged 8-22 years. We summarize the control properties of these networks by estimating average and modal controllability, two statistics that probe the ease with which brain areas can drive the network towards easy- versus difficult-to-reach states. We find that females have higher modal controllability in frontal, parietal, and subcortical regions while males have higher average controllability in frontal and subcortical regions. Furthermore, average controllability values in the medial frontal cortex and subcortex, both higher in males, are negatively related to executive function. Finally, we find that average controllability predicts sex-dependent individual differences in activation during an n-back working memory task. Taken together, our findings support the notion that sex differences in the controllability of structural brain networks can partially explain sex differences in executive function. Controllability of structural brain networks also predicts features of task-relevant activation, suggesting the potential for controllability to represent context-specific constraints on network state more generally.

q-bio.NC