Functional structure of correlated cortical activity in human visual areas

Abstract

The cerebral cortex is a large-scale network, where processing units are intimately connected. In the sensory system, a sensory organ and downstream cortical regions communicate through hierarchical connections, and local sites within the regions communicate through horizontal connections. In such interconnected networks, neural activities at local sites are likely to influence one another in complex ways and thus are intricately correlated. Recognizing the functional importance of correlated population activity in sensory representation, the neural activities arising spontaneously without the external stimuli have been studied via diverse local or global measures in various time scales. Here, measuring functional magnetic resonance imaging (fMRI) signals in human early visual cortex, we studied the structure of correlated population activity. Guided by previously known biases in anatomical connection patterns, we evaluated and compared the contributions of three relational factors to the correlated fMRI activities. Namely, all possible pairs of gray matter sites in visual areas were characterized (i) in terms of how far the receptive fields of two sites are from each other over retinotopic space, (ii) in terms of how far two sites are over cortical surface, and (iii) in terms of how similarly two sites are tuned to visual features, spatial frequency and orientation. We found that, although the three relational factors all have their own contributions in accounting for the structure of correlated fMRI activity, the tuning similarity factors overrode the distance factors. The predominance of tuning similarity was evident both within and between V1, V2, and V3, irrespective of the presence or degree of visual stimulation. We also found that the stimulus-tuned covariability systematically varied depending on the angular positions and the eccentricity in the visual field. Moreover, we found that the pairwise covariability of spontaneous fMRI activities fluctuated dynamically over time, and that this temporal dynamics was governed by both the distance factors and the tuning similarity factors. In general, our findings suggest that the spontaneous cortical activities in the human early visual areas can be understood as the interplays among local sites constituting a multilayered network, where different layers are governed by different distance or function factors. In specific, our study demonstrated that the layers governed by the stimulus tuning similarity are far more dominant than those governed by the distance factors.