Functional connectivity architecture of the human brain: not all the same

Abstract

Imaging studies suggest that individual differences in cognition and behavior might relate to differences in brain connectivity, particularly in the higher order association regions. Understanding the extent to which two brains can differ is crucial in clinical and basic neuroscience research. Here we highlight two major sources of variance that contribute to intersubject variability in connectivity measurements but are often mixed: the spatial distribution variability and the connection strength variability. We then offer a hypothesis about how the cortical surface expansion during human evolution may have led to remarkable intersubject variability in brain connectivity. We propose that a series of changes in connectivity architecture occurred in response to the pressure for processing efficiency in the enlarged brain. These changes not only distinguish us from our evolutionary ancestors, but also enable each individual to develop more uniquely. This hypothesis may gain support from the significant spatial correlations among evolutionary cortical expansion, the density of long-range connections, hemispheric functional specialization, and intersubject variability in connectivity.

Keywords: association cortex; evolution; fMRI; functional connectivity; individual differences; lateralization.

Conflict of interest statement

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

© The Author(s) 2014.

Figures

Figure 1

Resting-state functional connectivity suggests that great individual variability exists in a circuit related to obsessive-compulsive disorder (OCD). Previous studies on OCD have indicated connectivity abnormalities in a specific neural circuit that involves the orbital frontal cortex, the dorsal anterior cingulate cortex (dACC), and the striatum. We computed resting-state functional connectivity maps in 50 healthy subjects based on a dorsal striatum seed. The group-averaged connectivity maps (Z-transformed) are shown in the top row. The connectivity maps of three individual subjects are shown in the bottom rows. The maps demonstrate that the dorsal striatum seed can connect to different subregions in the dACC area in different subjects.

Figure 2

(A) The evolutionary cortical expansion was estimated by interspecies surface-based registration between an adult macaque and the average human adult PALS-B12 atlas, according to regions known or strongly suspected to be homologous as registration constraints. Distributed association regions in the temporal, parietal, and frontal lobes demonstrated disproportionate expansion, whereas the motor and sensory areas showed a lower rate of expansion. Data were provided by Van Essen and colleagues (Van Essen and Dierker 2007). (B) A map of distant connectivity. Distant connectivity was defined as the connection (r > 0.25) between two regions with a distance larger than 25 mm. Local connectivity was defined as the connection (r > 0.25) within 12 mm. The percentage of distant connectivity was then estimated at each brain voxel and projected to the brain surface (Mueller and others 2013). (C) A map of hemispheric specialization. Hemispheric specialization was calculated at each vertex by subtracting the count of cross-hemispheric connections from the count of within-hemispheric connections based on 1000 healthy subjects (Wang and others 2012). The counts of connections were normalized by the total number of vertices in each hemisphere. The specialization index is denoted as a percentage. Regions with higher within-hemispheric connectivity than cross-hemispheric connectivity are shown in warm colors. Regions with higher cross-hemispheric connectivity are shown in cold colors. (D) Intersubject variability was quantified at each surface vertex across 23 subjects after correction for underlying intrasubject variability (Mueller and others 2013).