Investigating signal integration with canonical correlation analysis of fMRI brain activation data

How the brain integrates signals from specific areas has been a longstanding critical question for neurobiologists. Two recent observations suggest a new approach to fMRI data analysis of this question. First, in many instances, the brain analyzes inputs by decomposing the information along several salient dimensions. For example, earlier work demonstrated that the brain splits a monetary gamble in terms of expected reward (ER) and variance of the reward (risk) [Preuschoff, K., Bossaerts, P., Quartz, S., 2006. Neural differentiation of expected reward and risk in human subcortical structures. Neuron 51, 381-390]. However, since ER and risk activate separate brain regions, the brain needs to integrate these activations to obtain an overall evaluation of the gamble. Second, recent evidence suggests that the correlation of the activity between neurons may serve a specific organizational purpose [Romo, R., Hernandez, A., Zainos, A., Salinas, E., 2003. Correlated neuronal discharges that increase coding efficiency during perceptual discrimination. Neuron 38, 649-657; Salinas, E., Sejnowski, T.J., 2001. Correlated neuronal activity and the flow of neural information. Nat. Rev. Neurosci. 2, 539]. Specifically, it is hypothesized that correlations allow brain regions to integrate several signals in a way that minimizes noise. Under this hypothesis, we show here that canonical correlation analysis of fMRI data identifies how the signals from several regions are combined. A general linear model then verifies whether the identified combination indeed activates a projection area in the brain. We illustrate the proposed procedure on data recorded while human subjects played a simple card game. We show that the brain adds the signals of ER and risk to form a measure that activates the medial prefrontal cortex, consistent with the role of this brain structure in the evaluation of monetary gambles.