Evolutionary shaping of human brain dynamics

Abstract

The human brain is distinct from those of other species in terms of size, organization, and connectivity. How do structural evolutionary differences drive patterns of neural activity enabling brain function? Here, we combine brain imaging and biophysical modeling to show that the anatomical wiring of the human brain distinctly shapes neural dynamics. This shaping is characterized by a narrower distribution of dynamic ranges across brain regions compared with that of chimpanzees, our closest living primate relatives. We find that such a narrow dynamic range distribution supports faster integration between regions, particularly in transmodal systems. Conversely, a broad dynamic range distribution as seen in chimpanzees facilitates brain processes relying more on neural interactions within specialized local brain systems. These findings suggest that human brain dynamics have evolved to foster rapid associative processes in service of complex cognitive functions and behavior.

Geometric constraints on human brain function

“…Indeed, recent estimates indicate that long-range cortical connections are rare 53 -they may therefore represent a relatively minor perturbation of the dominant effect imposed by EDR-like connectivity. Nonetheless the topological centrality, metabolic cost and tight genetic control of such connections 54,55 suggest that they provide important functional and evolutionary advantages beyond wave-like dynamics 56 (Supplementary Information 11). The limited resolution and sensitivity to preprocessing pipelines of dMRI and fMRI data 57,58 complicate attempts to fully uncover the functional role of these connections.…”

Geometric constraints on human brain function

“…Indeed, recent estimates indicate that long-range cortical connections are relatively rare 65 ; they may therefore represent a relatively minor perturbation of the dominant effect imposed by EDR-like connectivity. Nonetheless, the topological centrality, metabolic cost, and tight genetic control of such connections [66][67][68] suggest that they provide important functional and evolutionary advantages beyond wave-like dynamics 69 . The limited resolution and sensitivity to preprocessing pipelines 70,71 of dMRI and fMRI data complicate attempts to uncover the role of long-range connections, but high-quality animal tract-tracing and electrophysiological data may be helpful in this regard.…”

From local properties to brain‐wide organization: A review of intraregional temporal features in functional magnetic resonance imaging data

“…For example, gene expression analysis showed that the transcriptomic basis of the INTs significantly correlates with the expression of synaptic and ion channel genes; accordingly (see Figure 2d , the hierarchy of gene expression), hierarchical neural timescales depend on a macroscopic gradient of synaptic excitation and synaptic inhibition (S. Li & Wang, 2022 ). Regions with high neuronal densities and myelin content have simpler dendritic arbors and smaller somas (See Figure 2d , the hierarchy of T1/T2 and cortical thickness), which is beneficial to the highly parallel processing of sensory input in unimodal areas and leads to quick responses to stimuli; neurons with long‐range projections in multimodal areas help integrate inputs among spread regions and lead to slower and longer neural dynamics (Cahalane et al, 2012 ; Gao et al, 2020 ; Pang et al, 2022 ). These findings help us to understand how IRTFs and even brain functions emerge from neuronal constrains.…”