Attentional modulation of effective connectivity from V2 to V5/MT in humans

Abstract

The nonlinear nature of integration among cortical brain areas renders the effective connectivity between them inherently dynamic and context-sensitive. One emerging architectural principle of functional brain organization, which rests explicitly on these nonlinear interactions, is that neuronal responses expressed at any level in a sensory hierarchy reflect an interaction between (i) bottom up "driving" afferents from lower cortical areas and (ii) backwards "modulatory" inputs from higher areas that mediate top-down contextual effects. A compelling example is attentional modulation of responses in functionally specialized sensory areas. The aim of this work was to demonstrate that parietal regions may mediate selective attention to motion by modulating the effective connectivity from early visual cortex to the motion-sensitive area V5/MT. Using functional magnetic resonance imaging, and an analysis of effective connectivity based on nonlinear system identification, we found that backwards modulatory influences from the posterior parietal cortex are sufficient to account for a significant component of attentional modulation of V5/MT responses to "driving" inputs from V2. By explicitly modeling interactions among inputs to V5/MT, we were able to make inferences about the influences of V2 inputs and their concomitant activity-dependent modulation by parietal afferents. The latter effects embody dynamic changes in effective connectivity that may underlie attentional mechanisms. These results speak to the context-sensitive nature of functional integration in the brain and provide empirical evidence that attentional effects may be mediated by backwards connections, of a modulatory sort, in humans.

Figure 1

Schematic depicting the influences included in the nonlinear model of effective connectivity. The model includes driving (with linear and nonlinear terms) cortical (V2) and subcortical (Pul) inputs (arrows). Given the relatively slow speed of the stimuli used (4.7° per second), we anticipated that the functionally expressed input to V5/MT would derive primarily from V2 (12). Consequently, we modeled a modulation of this input by backwards afferents from posterior parietal cortex (PPC) (thick line).

Figure 2

Dynamics of the regions used in the analysis: Data from the first subject are shown in terms of the voxels used (white areas on a standard structural MRI scan) and the associated time-series. The time-series from the pulvinar (Pul), V2, and PPC were used in the subsequent analysis of modulatory effects and correspond to u(t) in the text.

Figure 3

Characterization of effects of V2 inputs on V5/MT and the modulation of these responses by PPC using simulated inputs at different levels of PPC activity. The broken lines represent estimates of C_V5,V2{0} according to Eq. 6, in which the V2 input s(t) was a 500-ms square wave convolved with the hemodynamic response function. The solid curves represent the same response when PPC activity is unity (i.e., C_V5,V2{0} + ∂C_V5,V2/∂u_PPC). The insets show all of the voxels in V5/MT that evidenced a modulatory effect (P < 0.05 uncorrected). These voxels were identified by thresholding SPMs of the F statistic testing for the contribution of second order explanatory variables involving V2 and PPC, while treating all others as confounds. Results for the first three subjects are shown.