Brain dynamics during natural viewing conditions--a new guide for mapping connectivity in vivo

We describe here a new way of obtaining maps of connectivity in the human brain based on interregional correlations of blood oxygen level-dependent (BOLD) signal during natural viewing conditions. We propose that anatomical connections are reflected in BOLD signal correlations during natural brain dynamics. This may provide a powerful approach to chart connectivity, more so than that based on the 'resting state' of the human brain, and it may complement diffusion tensor imaging. Our approach relies on natural brain dynamics and is therefore experimentally unbiased and independent of hypothesis-driven, specialized stimuli. It has the advantage that natural viewing leads to considerably stronger cortical activity than rest, thus facilitating detection of weaker connections. To validate our technique, we used functional magnetic resonance imaging (fMRI) to record BOLD signal while volunteers freely viewed a movie that was interrupted by resting periods. We used independent component analysis (ICA) to segregate cortical areas before characterizing the dynamics of their BOLD signal during free viewing and rest. Natural viewing and rest each revealed highly specific correlation maps, which reflected known anatomical connections. Examples are homologous regions in visual and auditory cortices in the two hemispheres and the language network consisting of Wernicke's area, Broca's area, and a premotor region. Correlations between regions known to be directly connected were always substantially higher than between nonconnected regions. Furthermore, compared to rest, natural viewing specifically increased correlations between anatomically connected regions while it decreased correlations between nonconnected regions. Our findings therefore demonstrate that natural viewing conditions lead to particularly specific interregional correlations and thus provide a powerful environment to reveal anatomical connectivity in vivo.