Network-Based Asymmetry of the Human Auditory System

Abstract

Converging evidence from activation, connectivity, and stimulation studies suggests that auditory brain networks are lateralized. Here we show that these findings can be at least partly explained by the asymmetric network embedding of the primary auditory cortices. Using diffusion-weighted imaging in 3 independent datasets, we investigate the propensity for left and right auditory cortex to communicate with other brain areas by quantifying the centrality of the auditory network across a spectrum of communication mechanisms, from shortest path communication to diffusive spreading. Across all datasets, we find that the right auditory cortex is better integrated in the connectome, facilitating more efficient communication with other areas, with much of the asymmetry driven by differences in communication pathways to the opposite hemisphere. Critically, the primacy of the right auditory cortex emerges only when communication is conceptualized as a diffusive process, taking advantage of more than just the topologically shortest paths in the network. Altogether, these results highlight how the network configuration and embedding of a particular region may contribute to its functional lateralization.

Figure 1.

Communication distance from auditory cortices to the rest of the brain. The centrality of left and right auditory cortices was estimated by their topological distance to other brain areas in terms of path length, communicability and spread time. Shorter path length, greater communicability, and shorter spread times indicate greater proximity. Mean values for each distribution are indicated by solid horizontal black lines. For visualization, a random horizontal jitter was added to all points. In the case of path length and spread time, which are discrete-valued variables, an additional vertical jitter was added to all points.

Figure 2.

Simulated spreading from auditory cortices to specific target regions. (a) Spreading times to other nodes of the network, separated by lobe and hemisphere (blue for ipsilateral areas, orange for contralateral areas). (b) Spreading times for left and right auditory seeds projected to the cortical surface. The projected locations of the primary auditory nodes are indicated by white dots.

Figure 3.

Communication distance from primary visual cortices to the rest of the brain. The centrality of left and right visual cortices was estimated by their topological distance to other brain areas in terms of path length, communicability and spread time. Shorter path length, greater communicability, and shorter spread times indicate greater proximity. Mean values for each distribution are indicated by solid horizontal black lines. For visualization, a random horizontal jitter was added to all points. In the case of path length and spread time, which are discrete-valued variables, an additional vertical jitter was added to all points.