Conversation effects on neural mechanisms underlying reaction time to visual events while viewing a driving scene: fMRI analysis and asynchrony model

This neuroimaging study investigated the neural mechanisms of the effect of conversation on visual event detection during a driving-like scenario. The static load paradigm, established as predictive of visual reaction time in on-road driving, measured reaction times to visual events while subjects watched a real-world driving video. Behavioral testing with twenty-eight healthy volunteers determined the reaction time effects from overt and covert conversation tasks in this paradigm. Overt and covert conversation gave rise to longer visual event reaction times in the surrogate driving paradigm compared to just driving with no conversation, with negligible effect on miss rates. The covert conversation task was then undertaken by ten right-handed healthy adults in a 4-Tesla fMRI magnet. We identified a frontal-parietal network that maintained event detection performance during the conversation task while watching the driving video. Increased brain activations for conversation vs. no conversation during such simulated driving was found not only in language regions (Broca's and Wernicke's areas), but also specific regions in bilateral inferior frontal gyrus, bilateral anterior insula and orbitofrontal cortex, bilateral lateral prefrontal cortex (right middle frontal gyrus and left frontal eye field), supplementary motor cortex, anterior and posterior cingulate gyrus, right superior parietal lobe, right intraparietal sulcus, right precuneus, and right cuneus. We propose an Asynchrony Model in which the frontal regions have a top-down influence on the synchrony of neural processes within the superior parietal lobe and extrastriate visual cortex that in turn modulate the reaction time to visual events during conversation while driving.

[1]  Thomas A. Dingus,et al.  An Evaluation of Alternative Methods for Assessing Driver Workload in the Early Development of In-Vehicle Information Systems , 2002 .

[2]  Li Hsieh,et al.  Mind-on-the-drive : Real-time functional neuroimaging of cognitive brain mechanisms underlying driver performance and distraction , 2005 .

[3]  Jeff Allen Greenberg,et al.  EVALUATION OF DRIVER DISTRACTION USING AN EVENT DETECTION PARADIGM , 2003 .

[4]  Ernst Fernando Lopes Da Silva Niedermeyer,et al.  Electroencephalography, basic principles, clinical applications, and related fields , 1982 .

[5]  R. Deichmann,et al.  Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI. , 2008, Cerebral cortex.

[6]  N. Sadato,et al.  The neural substrates of driving at a safe distance: a functional MRI study , 2003, Neuroscience Letters.

[7]  J. Pekar,et al.  Alcohol Intoxication Effects on Simulated Driving: Exploring Alcohol-Dose Effects on Brain Activation Using Functional MRI , 2004, Neuropsychopharmacology.

[8]  M. Just,et al.  A decrease in brain activation associated with driving when listening to someone speak , 2008, Brain Research.

[9]  G. Thut,et al.  Mechanisms of selective inhibition in visual spatial attention are indexed by α‐band EEG synchronization , 2007, The European journal of neuroscience.

[10]  J. Pekar,et al.  Erratum: Different activation dynamics in multiple neural systems during simulated driving (Human Brain Mapping (2002) 16 (158-167)) , 2002 .

[11]  Myra Blanco,et al.  Investigating the Effect of Performing Voice Recognition Tasks on the Detection of Forward and Peripheral Events , 2004 .

[12]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[13]  Li Hsieh,et al.  Visual event detection during simulated driving: Identifying the neural correlates with functional neuroimaging , 2004 .

[14]  G. Hutchins,et al.  Functional Heterogeneity of Inferior Frontal Gyrus Is Shaped by Linguistic Experience , 2001, Brain and Language.

[15]  A. Nobre,et al.  Heterogeneity of Cingulate Contributions to Spatial Attention , 2001, NeuroImage.

[16]  B L Cole,et al.  What attracts attention when driving? , 1986, Ergonomics.

[17]  D. V. von Cramon,et al.  Localization of Executive Functions in Dual-Task Performance with fMRI , 2002, Journal of Cognitive Neuroscience.

[18]  Hamid Soltanian-Zadeh,et al.  Integrated MEG/EEG and fMRI model based on neural masses , 2006, IEEE Transactions on Biomedical Engineering.

[19]  T. Womelsdorf,et al.  The role of neuronal synchronization in selective attention , 2007, Current Opinion in Neurobiology.

[20]  R. Deichmann,et al.  Concurrent TMS-fMRI and Psychophysics Reveal Frontal Influences on Human Retinotopic Visual Cortex , 2006, Current Biology.

[21]  H. Critchley Neural mechanisms of autonomic, affective, and cognitive integration , 2005, The Journal of comparative neurology.

[22]  I. Brown,et al.  Vision in Vehicles III , 1991 .

[23]  Louis Tijerina,et al.  HEAVY VEHICLE DRIVER WORKLOAD ASSESSMENT. TASK 7A, IN-CAB TEXT MESSAGE SYSTEM AND CELLULAR PHONE USE BY HEAVY VEHICLE DRIVERS ON ROAD , 1996 .

[24]  Fernando Lopes da Silva,et al.  Comprar Niedermeyer's Electroencephalography, 6/e (Basic Principles, Clinical Applications, and Related Fields ) | Fernando Lopes Da Silva | 9780781789424 | Lippincott Williams & Wilkins , 2010 .

[25]  L. Shuster,et al.  An fMRI investigation of covertly and overtly produced mono- and multisyllabic words , 2005, Brain and Language.

[26]  N. Kanwisher,et al.  The Generality of Parietal Involvement in Visual Attention , 1999, Neuron.

[27]  D. Strayer,et al.  Cell phone-induced failures of visual attention during simulated driving. , 2003, Journal of experimental psychology. Applied.

[28]  Christopher D. Wickens,et al.  Examining the Impact of Cell Phone Conversations on Driving Using Meta-Analytic Techniques , 2006, Hum. Factors.

[29]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[30]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[31]  N. Lavie,et al.  Frontal control of attentional capture in visual search , 2006 .

[32]  Eleanor A. Maguire,et al.  Neural substrates of driving behaviour , 2007, NeuroImage.

[33]  M. Posner,et al.  Timing the Brain: Mental Chronometry as a Tool in Neuroscience , 2005, PLoS biology.

[34]  M. D’Esposito,et al.  The neural effect of stimulus-response modality compatibility on dual-task performance: an fMRI study , 2006, Psychological research.

[35]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[36]  Juha Silvanto,et al.  Stimulation of the human frontal eye fields modulates sensitivity of extrastriate visual cortex. , 2006, Journal of neurophysiology.

[37]  Gregor Thut,et al.  Prediction of response speed by anticipatory high‐frequency (gamma band) oscillations in the human brain , 2005, Human brain mapping.

[38]  David L. Strayer,et al.  Driven to Distraction: Dual-Task Studies of Simulated Driving and Conversing on a Cellular Telephone , 2001, Psychological science.

[39]  Hermann Ackermann,et al.  The contribution of the insula to motor aspects of speech production: A review and a hypothesis , 2004, Brain and Language.

[40]  M. Milham,et al.  Competition for priority in processing increases prefrontal cortex's involvement in top-down control: an event-related fMRI study of the stroop task. , 2003, Brain research. Cognitive brain research.

[41]  Kazuhiko Yanai,et al.  The neural correlates of driving performance identified using positron emission tomography , 2005, Brain and Cognition.

[42]  Vincent Walsh,et al.  Right parietal cortex plays a critical role in change blindness. , 2006, Cerebral cortex.

[43]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[44]  E A Disbrow,et al.  Functional MRI at 1.5 tesla: a comparison of the blood oxygenation level-dependent signal and electrophysiology. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Ralph D Freeman,et al.  Separate Spatial Scales Determine Neural Activity-Dependent Changes in Tissue Oxygen within Central Visual Pathways , 2005, The Journal of Neuroscience.

[46]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[47]  Johan Engström,et al.  Effects of visual and cognitive load in real and simulated motorway driving , 2005 .

[48]  E. Hoffmann,et al.  Drivers' awareness of traffic sign information , 1991 .

[49]  J. Groeger Understanding Driving: Applying Cognitive Psychology to a Complex Everyday Task , 2000 .

[50]  J A Michon,et al.  Explanatory pitfalls and rule-based driver models. , 1989, Accident; analysis and prevention.

[51]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[52]  J. Pekar,et al.  fMRI Activation in a Visual-Perception Task: Network of Areas Detected Using the General Linear Model and Independent Components Analysis , 2001, NeuroImage.

[53]  Henrik Walter,et al.  The neural correlates of driving , 2001, Neuroreport.

[54]  Scott A. Huettel,et al.  Dissociating the Neural Mechanisms of Visual Attention in Change Detection Using Functional MRI , 2001, Journal of Cognitive Neuroscience.

[55]  M. Steriade,et al.  Discharge rate and excitability of cortically projecting intralaminar thalamic neurons during waking and sleep states , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[57]  Philip K. Hughes,et al.  The Effect of Attentional Demand in Eye Movement Behaviour when Driving , 1988 .

[58]  Li Hsieh,et al.  Conversation effects on neural mechanisms underlying reaction time to visual events while viewing a driving scene using MEG , 2009, Brain Research.

[59]  Marieke Hendrikje Martens,et al.  Does road familiarity change eye fixations? A comparison between watching a video and real driving , 2007 .

[60]  B. Gulyás,et al.  Activation by Attention of the Human Reticular Formation and Thalamic Intralaminar Nuclei , 1996, Science.

[61]  Georg Jahn,et al.  Peripheral detection as a workload measure in driving: Effects of traffic complexity and route guidance system use in a driving study , 2005 .

[62]  J. Pekar,et al.  Different activation dynamics in multiple neural systems during simulated driving , 2002, Human brain mapping.

[63]  Willem J. M. Levelt,et al.  A theory of lexical access in speech production , 1999, Behavioral and Brain Sciences.

[64]  M. Mesulam Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[65]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[66]  Joel L. Davis,et al.  Visual attention and cortical circuits , 2001 .

[67]  Nilli Lavie,et al.  Capacity limits in selective attention: Behavioral evidence and implications for neural activity , 2001 .

[68]  A J McKnight,et al.  The effect of cellular phone use upon driver attention. , 1993, Accident; analysis and prevention.

[69]  Christopher Schreiner,et al.  Real‐World Personal Conversations Using a Hands‐Free Embedded Wireless Device While Driving: Effect on Airbag‐Deployment Crash Rates , 2009, Risk analysis : an official publication of the Society for Risk Analysis.

[70]  R. Freeman,et al.  Single-Neuron Activity and Tissue Oxygenation in the Cerebral Cortex , 2003, Science.

[71]  Li Hsieh,et al.  MEG localization of cortex involved in attention processes during a driving task with conversation , 2007 .

[72]  P. Goldman-Rakic,et al.  Functional neuroanatomy of executive processes involved in dual-task performance. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[73]  Christopher S. Schreiner The Effect of Phone Interface and Dialing Method on Simulated Driving Performance and User Preference , 2006 .

[74]  Randy L. Buckner,et al.  An Event-Related fMRI Study of Overt and Covert Word Stem Completion , 2001, NeuroImage.