Different activation dynamics in multiple neural systems during simulated driving

Abstract

Driving is a complex behavior that recruits multiple cognitive elements. We report on an imaging study of simulated driving that reveals multiple neural systems, each of which have different activation dynamics. The neural correlates of driving behavior are identified with fMRI and their modulation with speed is investigated. We decompose the activation into interpretable pieces using a novel, generally applicable approach, based upon independent component analysis. Some regions turn on or off, others exhibit a gradual decay, and yet others turn on transiently when starting or stopping driving. Signal in the anterior cingulate cortex, an area often associated with error monitoring and inhibition, decreases exponentially with a rate proportional to driving speed, whereas decreases in frontoparietal regions, implicated in vigilance, correlate with speed. Increases in cerebellar and occipital areas, presumably related to complex visuomotor integration, are activated during driving but not associated with driving speed.

Figure 1

fMRI‐simulated driving paradigm. The paradigm consisted of 10 1‐min epochs of (a) a fixation target, (b) driving the simulator, and (c) watching a simulation while randomly moving fingers over the controller. The paradigm was presented twice changing the order of the (b) and (c) epochs and counterbalancing the first order across subjects.

Figure 2

Independent components and associated time courses from functional MRI scans. Random effects group fMRI maps are thresholded at P < 0. 00025 (t = 4.5, df = 14). A total of six components are presented. A green component extends on both sides of the parieto‐occipital sulcus including portions of cuneus, precuneus, and the lingual gyrus. A yellow component contains mostly occipital areas. A white component contains bilateral visual association and parietal areas; and a component consisting of cerebellar and motor areas is depicted in red. Orbitofrontal and anterior cingulate areas identified are depicted in pink. Finally, a component including medial frontal, parietal, and posterior cingulate regions is depicted in blue. Group averaged time courses (right) for the fixate‐drive‐watch order are also depicted with similar colors. Standard deviation across the group of 15 scans is indicated for each time course with dotted lines. The epochs are averaged and presented as fixation, drive, and watch.

Figure 3

Components demonstrating significant speed‐related modulation. The anterior cingulate/orbitofrontal component decreased more rapidly for the faster drivers. The frontoparietal component demonstrated decreases during the driving epoch and greater decreases for the faster drivers. The lines connect the three subjects who were scanned during both faster and slower driving.

Figure 4

Interpretation of imaging results. The colors correspond to those used in Figure 2. Components are grouped according to the averaged pattern demonstrated by their time courses. The speed modulated components are indicated with arrows.