Disruptions in functional network connectivity during alcohol intoxicated driving.

BACKGROUND Driving while under the influence of alcohol is a major public health problem whose neural basis is not well understood. In a recently published functional magnetic resonance imaging (fMRI) study (Meda et al., 2009), our group identified 5, independent critical driving-associated brain circuits whose inter-regional connectivity was disrupted by alcohol intoxication. However, the functional connectivity between these circuits has not yet been explored in order to determine how these networks communicate with each other during sober and alcohol-intoxicated states. METHODS In the current study, we explored such differences in connections between the above brain circuits and driving behavior, under the influence of alcohol versus placebo. Forty social drinkers who drove regularly underwent fMRI scans during virtual reality driving simulations following 2 alcohol doses, placebo and an individualized dose producing blood alcohol concentrations (BACs) of 0.10%. RESULTS At the active dose, we found specific disruptions of functional network connectivity between the frontal-temporal-basal ganglia and the cerebellar circuits. The temporal connectivity between these 2 circuits was found to be less correlated (p < 0.05) when driving under the influence of alcohol. This disconnection was also associated with an abnormal driving behavior (unstable motor vehicle steering). CONCLUSIONS Connections between frontal-temporal-basal ganglia and cerebellum have recently been explored; these may be responsible in part for maintaining normal motor behavior by integrating their overlapping motor control functions. These connections appear to be disrupted by alcohol intoxication, in turn associated with an explicit type of impaired driving behavior.

[1]  V. Calhoun,et al.  Changes in the interaction of resting‐state neural networks from adolescence to adulthood , 2009, Human brain mapping.

[2]  Philip G. F. Browning,et al.  Dissociable Components of Rule-Guided Behavior Depend on Distinct Medial and Prefrontal Regions , 2009, Science.

[3]  W. Todd Maddox,et al.  Rule-based category learning in patients with Parkinson's disease , 2009, Neuropsychologia.

[4]  Godfrey D Pearlson,et al.  Alcohol dose effects on brain circuits during simulated driving: An fMRI study , 2009, Human brain mapping.

[5]  Godfrey D Pearlson,et al.  Effects of alcohol on performance on a distraction task during simulated driving. , 2009, Alcoholism, clinical and experimental research.

[6]  Vince D. Calhoun,et al.  A review of group ICA for fMRI data and ICA for joint inference of imaging, genetic, and ERP data , 2009, NeuroImage.

[7]  S. Haber,et al.  Cognitive and limbic circuits that are affected by deep brain stimulation. , 2009, Frontiers in bioscience.

[8]  Jeremy D. Schmahmann,et al.  Disconnection syndromes of basal ganglia, thalamus, and cerebrocerebellar systems , 2008, Cortex.

[9]  H A Jinnah,et al.  The basal ganglia and cerebellum interact in the expression of dystonic movement. , 2008, Brain : a journal of neurology.

[10]  J. Doyon Motor sequence learning and movement disorders , 2008, Current opinion in neurology.

[11]  Vince D. Calhoun,et al.  A method for functional network connectivity among spatially independent resting-state components in schizophrenia , 2008, NeuroImage.

[12]  J. Krakauer,et al.  A computational neuroanatomy for motor control , 2008, Experimental Brain Research.

[13]  Julie A. Fiez,et al.  Cerebellar contributions to verbal working memory: beyond cognitive theory , 2008, The Cerebellum.

[14]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[15]  V. Calhoun,et al.  Functional neural circuits for mental timekeeping , 2007, Human brain mapping.

[16]  Ravi S. Menon,et al.  Ventral medial prefrontal cortex and cardiovagal control in conscious humans , 2007, NeuroImage.

[17]  D. Sakas,et al.  Connections of the basal ganglia with the limbic system: implications for neuromodulation therapies of anxiety and affective disorders. , 2007, Acta neurochirurgica. Supplement.

[18]  R. Levy,et al.  Apathy and the basal ganglia , 2006, Journal of Neurology.

[19]  Eleanor A. Maguire,et al.  Thoughts, behaviour, and brain dynamics during navigation in the real world , 2006, NeuroImage.

[20]  T. Adali,et al.  Unmixing fMRI with independent component analysis , 2006, IEEE Engineering in Medicine and Biology Magazine.

[21]  Godfrey D Pearlson,et al.  Simulated Driving and Brain Imaging: Combining Behavior, Brain Activity, and Virtual Reality , 2006, CNS Spectrums.

[22]  J. Muir,et al.  Frontal-striatal disconnection disrupts cognitive performance of the frontal-type in the rat , 2005, Neuroscience.

[23]  Catalin V. Buhusi,et al.  What makes us tick? Functional and neural mechanisms of interval timing , 2005, Nature Reviews Neuroscience.

[24]  G. D. Pearlson,et al.  Using Virtual Reality to Study Alcohol Intoxication Effects on the Neural Correlates of Simulated Driving , 2005, Applied psychophysiology and biofeedback.

[25]  S. Swinnen,et al.  The role of anterior cingulate cortex and precuneus in the coordination of motor behaviour , 2005, The European journal of neuroscience.

[26]  G. Pearlson,et al.  Driving Simulator Performance in Schizophrenia , 2005, Schizophrenia Research.

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

[28]  Warren H Meck,et al.  Frontal-striatal circuitry activated by human peak-interval timing in the supra-seconds range. , 2004, Brain research. Cognitive brain research.

[29]  Jennie Connor,et al.  The Contribution of Alcohol to Serious Car Crash Injuries , 2004, Epidemiology.

[30]  R. Ivry,et al.  The neural representation of time , 2004, Current Opinion in Neurobiology.

[31]  Boris Suchan,et al.  Cortico-subcortical contributions to executive control. , 2004, Acta psychologica.

[32]  Katya Rubia,et al.  The neural correlates of cognitive time management: a review. , 2004, Acta neurobiologiae experimentalis.

[33]  N. Volkow,et al.  Relationship between ethanol-induced changes in brain regional metabolism and its motor, behavioural and cognitive effects. , 2004, Alcohol and alcoholism.

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

[35]  S Lehéricy,et al.  Basal ganglia and supplementary motor area subtend duration perception: an fMRI study , 2003, NeuroImage.

[36]  R. Miall,et al.  Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging , 2003, Current Opinion in Neurobiology.

[37]  Margarete Delazer,et al.  Basal Ganglia Lesions and the Theory of Fronto-Subcortical Loops: Neuropsychological Findings in Two Patients with Left Caudate Lesions , 2003, Neurocase.

[38]  Shawn W. Ell,et al.  Category learning deficits in Parkinson's disease. , 2003, Neuropsychology.

[39]  Jean-Francois Mangin,et al.  What is the best similarity measure for motion correction in fMRI time series? , 2002, IEEE Transactions on Medical Imaging.

[40]  M. Herrero,et al.  Functional anatomy of thalamus and basal ganglia , 2002, Child’s Nervous System.

[41]  W. Meck,et al.  Dissecting the Brain's Internal Clock: How Frontal–Striatal Circuitry Keeps Time and Shifts Attention , 2002, Brain and Cognition.

[42]  F. Vidal,et al.  Activation of the supplementary motor area and of attentional networks during temporal processing , 2002, Experimental Brain Research.

[43]  M. S. Salman Topical Review : The Cerebellum: It's About Time! But Timing Is Not Everything-New Insights Into the Role of the Cerebellum in Timing Motor and Cognitive Tasks , 2002, Journal of child neurology.

[44]  M. First,et al.  Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research version (SCID-I RV) , 2002 .

[45]  M. Shipp Understanding Driving: Applying Cognitive Psychology to a Complex Everyday Task , 2001 .

[46]  T R Miller,et al.  Costs of alcohol-related crashes: New Zealand estimates and suggested measures for use internationally. , 2001, Accident; analysis and prevention.

[47]  Paul Van Hecke,et al.  Brain Areas Involved in Interlimb Coordination: A Distributed Network , 2001, NeuroImage.

[48]  L. Freire,et al.  Motion Correction Algorithms May Create Spurious Brain Activations in the Absence of Subject Motion , 2001, NeuroImage.

[49]  A. Maclean,et al.  How do prolonged wakefulness and alcohol compare in the decrements they produce on a simulated driving task? , 2001, Accident; analysis and prevention.

[50]  F. Happé Clinical Neuropsychology: Behavioral and Brain Science , 2001 .

[51]  Vince D. Calhoun,et al.  ASSESSMENT OF INTOXICATED DRIVING WITH A SIMULATOR : A PILOT VALIDATION STUDY WITH ON-ROAD DRIVING , 2001 .

[52]  P. Zador,et al.  Alcohol-related relative risk of driver fatalities and driver involvement in fatal crashes in relation to driver age and gender: an update using 1996 data. , 2000, Journal of studies on alcohol.

[53]  J. Hollerman,et al.  Involvement of basal ganglia and orbitofrontal cortex in goal-directed behavior. , 2000, Progress in brain research.

[54]  G S Watson,et al.  Effects of fexofenadine, diphenhydramine, and alcohol on driving performance. A randomized, placebo-controlled trial in the Iowa driving simulator. , 2000, Annals of internal medicine.

[55]  T. Rammsayer,et al.  Neuropharmacological Evidence for Different Timing Mechanisms in Humans , 1999, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[56]  C. Gallistel,et al.  Toward a neurobiology of temporal cognition: advances and challenges , 1997, Current Opinion in Neurobiology.

[57]  T. Rammsayer,et al.  Are there dissociable roles of the mesostriatal and mesolimbocortical dopamine systems on temporal information processing in humans? , 1997, Neuropsychobiology.

[58]  P. Strick,et al.  Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. , 1994, Science.

[59]  T. Rammsayer,et al.  On dopaminergic modulation of temporal information processing , 1993, Biological Psychology.

[60]  R. Hammersley,et al.  Alcohol placebos: you can only fool some of the people all of the time. , 1992, British journal of addiction.

[61]  I Hindmarch,et al.  The effects of alcohol and other drugs on psychomotor performance and cognitive function. , 1991, Alcohol and alcoholism.

[62]  R. Neill,et al.  Discrimination of motion in depth trajectory following acute alcohol ingestion , 1990, Biological Psychology.

[63]  L. Standing,et al.  Impairment of Cognition, Risk-Taking, and Self-Perception by Alcohol , 1989, Perceptual and Motor Skills.

[64]  M. Mitchell,et al.  Alcohol-induced impairment of central nervous system function: behavioral skills involved in driving. , 1985, Journal of studies on alcohol. Supplement.

[65]  L J Rosen,et al.  Acute and chronic effects of alcohol use on organizational processes in memory. , 1976, Journal of abnormal psychology.

[66]  H. Moskowitz,et al.  Effects of Alcohol on Peripheral Vision as a Function of Attention , 1974, Human factors.

[67]  M J Mattila,et al.  Interaction of alcohol and drugs on psychomotor skills as demonstrated by a driving simulator. , 1973, British journal of pharmacology.

[68]  R. Tarter,et al.  Absence of intellectual deterioration in chronic alcoholics. , 1971, Journal of clinical psychology.