Neural substrates of driving behaviour

Abstract

Driving a vehicle is an indispensable daily behaviour for many people, yet we know little about how it is supported by the brain. Given that driving in the real world involves the engagement of many cognitive systems that rapidly change to meet varying environmental demands, identifying its neural basis presents substantial problems. By employing a unique combination of functional magnetic resonance imaging (fMRI), an accurate interactive virtual simulation of a bustling central London (UK) and a retrospective verbal report protocol, we surmounted these difficulties. We identified different events that characterise the driving process on a second by second basis and the brain regions that underlie them. Prepared actions such as starting, turning, reversing and stopping were associated with a common network comprised of premotor, parietal and cerebellar regions. Each prepared action also recruited additional brain areas. We also observed unexpected hazardous events such as swerving and avoiding collisions that were associated with activation of lateral occipital and parietal regions, insula, as well as a more posterior region in the medial premotor cortex than prepared actions. By contrast, planning future actions and monitoring fellow road users were associated with activity in superior parietal, lateral occipital cortices and the cerebellum. The anterior pre-SMA was also recruited during action planning. The right lateral prefrontal cortex was specifically engaged during the processing of road traffic rules. By systematically characterising the brain dynamics underlying naturalistic driving behaviour in a real city, our findings may have implications for how driving competence is considered in the context of neurological damage.

Fig. 1

Example views from within the video game “The Getaway” © 2002 Sony Computer Entertainment Europe. Upper panel shows a view at Trafalgar Square, middle panel a view at Piccadilly Circus, lower panel a view looking towards the London Eye/Millennium Wheel. These images are reproduced with the kind permission of Sony Computer Entertainment Europe. The vehicle subjects drove during the experiment was a London taxi cab, visible in the lower middle of each image.

Fig. 2

Locations of peak voxel activations lying on or near the midline for each condition versus coasting. See the Results section for details of activations in lateral regions and Appendix A for full details of peak coordinates and Z-scores. MNI coordinates are given here and all locations were identified at a threshold of P < 0.001 uncorrected. (A) Locations for peak coordinates (x, y, z) of activations during prepared actions are pre-SMA/SMA starts moving (SM) = 6, 9, 69, turning (T) = − 3, 0, 60, reversing (R) = − 3, 6, 54; stopping (ST) = 3, 12, 60; precuneus/parietal/posterior cingulate SM = 0, − 51, 45, T = 9, − 51, 54, R = 9, − 60, 60; ST = − 12, − 84, 48; posterior cingulate SM = − 6, − 24, 42, T = 9, − 27, 45, R = 12, − 27, 39; and medial occipital region SM = 6, − 81, − 9, T = 9, − 75, − 6, R = − 3, − 78, 15; ST = 15, − 69, 0. (B) Locations of peak coordinates for locations active during unprepared actions are SMA swerving (Sw) = 9, − 15, 51, anterior cingulate avoiding collisions (ACol) = − 3, 42, 33; mid cingulate Sw = − 6, 3, 42, ACol = − 9, − 21, 42; parietal cortex Sw = − 15, − 81, 39, ACol = 15, − 84, 36; and medial occipital cortex Sw = 0, − 75, 3, ACol = − 6, − 72, − 3. (C) Locations for peak coordinates of activations for the other categories of interest are pre-SMA action planning (AP) = 6, 21, 48, traffic rules = 6, 33, 42; medial parietal/precuneus AP = − 3, − 57, 51, monitoring traffic (MT) = 6, − 66, 51; medial occipital AP = 9, − 84, − 9, MT = 12, − 87, 3.

Fig. 3

Brain activity related to turning corners. Significant activations for all turning events versus coasting events, shown for (A) the right hemisphere and (B) the left hemisphere. Images are shown at a threshold of P < 0.001. (C) Significant activation in left medial occipital cortex for turning left versus turning right and right medial occipital cortex for turning right versus turning left. Shown on the SPM2 template brain at a threshold of P < 0.05 corrected in order to illustrate the activity peaks more clearly.

Fig. 4

Brain regions more active during collision avoidance events than coasting events. Activations are shown on an axial (A) and sagittal section (B) of the SPM2 template brain at a threshold of P < 0.001. Regions circled are the middle occipital gyrus (mOG) bilaterally and the left anterior insula (insula). See Fig. 2B and Appendix A for details of other regions active.

Fig. 5

Activation in the right lateral prefrontal cortex during rule-related retrieval/processing relative to coasting events. Location of the peak coordinate in right lateral prefrontal cortex (45, 15, 33), shown at threshold of P < 0.001 on the SPM2 template brain. See also Fig. 2C for details of the activation in the pre-SMA.