Resting-State Neural Activity across Face-Selective Cortical Regions Is Behaviorally Relevant

Abstract

Interest has increased recently in correlations across brain regions in the resting-state fMRI blood oxygen level-dependent (BOLD) response, but little is known about the functional significance of these correlations. Here we directly test the behavioral relevance of the resting-state correlation between two face-selective regions in human brain, the occipital face area (OFA) and the fusiform face area (FFA). We found that the magnitude of the resting-state correlation, henceforth called functional connectivity (FC), between OFA and FFA correlates with an individual's performance on a number of face-processing tasks, not non-face tasks. Further, we found that the behavioral significance of the OFA/FFA FC is independent of the functional activation and the anatomical size of either the OFA or FFA, suggesting that face processing depends not only on the functionality of individual face-selective regions, but also on the synchronized spontaneous neural activity between them. Together, these findings provide strong evidence that the functional correlations in the BOLD response observed at rest reveal functionally significant properties of cortical processing. IntroductionRecently a number of functional magnetic resonance imaging (fMRI) studies have investigated neural activity in the human brain during periods of rest (when no stimuli are presented and no tasks are performed), and found that the spontaneous blood oxygenation level-dependent (BOLD) fluctuations are not random, but correlated across cortical regions with similar functional properties [for review, see Fox and Raichle (2007) and Greicius (2008)]. Further, these functional correlations are thought to reflect functional relationships mediated by anatomical connections (e.g., Vincent et al., 2007;Greicius et al., 2009;Honey et al., 2009). However, despite the abundance of work finding such correlations across cortical regions, little is known about the functional significance of these correlations: is synchronized spontaneous neural activity across cortical regions relevant for behavior, or is it merely epiphenomenal? Here we addressed this question by directly testing the behavioral significance of the resting-state correlations between two face-selective regions in the occipitotemporal cortex that are primarily involved in recognition of individual identity (Haxby et al., 2000;Calder and Young, 2005;Ishai, 2008)-the occipital face area (OFA) (Gauthier et al., 2000) and the fusiform face area (FFA) (Kanwisher et al., 1997)-found to be functionally correlated using resting-state fMRI (Nir et al., 2006;Zhang et al., 2009).First, we calculated the correlation in spontaneous BOLD fluctuations between OFA and FFA during the resting state in participants, and then behaviorally tested the same participants outside the scanner on a number of face and non-face tasks. If the correlation in spontaneous BOLD fluctuations between OFA and FFA, henceforth referred to as functional connectivity (FC), is behaviorally relevant, then we predict that the magnitude of the OF...

Individual variability in functional connectivity predicts performance of a perceptual task

“…Several previous studies have reported correlations between performance measures and fMRI FC (22)(23)(24)(25)(26). However, this study, as far as we are aware, is the first to demonstrate that FC, before any exposure, is predictive of performance and acquisition on a novel task.…”

“…Hence, resting-state functional connectivity offers a plausible neural correlate of behavioral predisposition to perform a novel task. Moreover, resting-state measures have been correlated with individual performance variability in several cognitive domains (22)(23)(24)(25)(26). However, to our knowledge, no study to date has shown that functional connectivity, measured before training, within cortical circuits later recruited by a novel task, is predictive of future performance.…”

The Hierarchical Structure of the Face Network Revealed by Its Functional Connectivity Pattern

“…Participants completed two computer-based tasks: the old/new recognition task (Zhu et al, 2011; and the face-inversion task (Zhu et al, 2011), and one paper-based test, the Raven's Advanced Progressive Matrices (RAPM) (Raven et al, 1998). The RAPM test was conducted on a separate day from the computer-based tasks.…”

“…Neuroimaging studies have revealed a well-described face network (FN) comprising brain regions that are coactivated in a variety of face processing tasks (for reviews, see Haxby et al, 2000;Gobbini and Haxby, 2007;Ishai, 2008;Pitcher et al, 2011a), including the fusiform face area (FFA), occipital face area (OFA), superior temporal sulcus (STS), amygdala (AMG), inferior frontal gyrus (IFG), anterior temporal cortex (ATC), and visual cortex (VC) (Calder and Young, 2005;Kanwisher and Yovel, 2006;Gobbini and Haxby, 2007;Liu et al, 2010;Zhang et al, 2012;Zhen et al, 2013). Recent FC studies have shown that some face-selective regions are strongly connected (e.g., the FFA-OFA, FFA-STS, FFA-VC, and STS-AMG) under both task-state and resting-state in the adult brain (Zhang et al, 2009;Turk-Browne et al, 2010;Zhu et al, 2011;DaviesThompson and Andrews, 2012;O'Neil et al, 2014), and effective connectivity of the FFA-OFA and the OFA-STS increases from childhood to adulthood (Cohen Kadosh et al, 2011). Therefore, the coactivated face-selective regions are likely integrated through strengthened FC to form the FN.…”

“…Furthermore, FC between the face-selective regions can be read out for behavioral performance. For example, stronger FFA-OFA FC is related to better performance in a variety of face tasks (Zhu et al, 2011), and stronger FC between the FFA and a face region in the perirhinal cortex is associated with a larger face inversion effect (O'Neil et al, 2014). However, these studies only focused on specific regions within the FN, and did not investigate the integration of the FN as a whole.…”