The neural network sustaining crossmodal integration is impaired in alcohol-dependence: An fMRI study

INTRODUCTION Crossmodality (i.e., the integration of stimulations coming from different sensory modalities) is a crucial ability in everyday life and has been extensively explored in healthy adults. Still, it has not yet received much attention in psychiatry, and particularly in alcohol-dependence. The present study investigates the cerebral correlates of crossmodal integration deficits in alcohol-dependence to assess whether these deficits are due to the mere accumulation of unimodal impairments or rather to specific alterations in crossmodal areas. METHODS Twenty-eight subjects [14 alcohol-dependent subjects (ADS), 14 paired controls] were scanned using fMRI while performing a categorization task on faces (F), voices (V) and face-voice pairs (FV). A subtraction contrast [FV-(F+V)] and a conjunction analysis [(FV-F) ∩ (FV-V)] isolated the brain areas specifically involved in crossmodal face-voice integration. The functional connectivity between unimodal and crossmodal areas was explored using psycho-physiological interactions (PPI). RESULTS ADS presented only moderate alterations during unimodal processing. More centrally, in the subtraction contrast and conjunction analysis, they did not show any specific crossmodal brain activation while controls presented activations in specific crossmodal areas (inferior occipital gyrus, middle frontal gyrus, superior parietal lobule). Moreover, PPI analyses showed reduced connectivity between unimodal and crossmodal areas in alcohol-dependence. CONCLUSIONS This first fMRI exploration of crossmodal processing in alcohol-dependence showed a specific face-voice integration deficit indexed by reduced activation of crossmodal areas and reduced connectivity in the crossmodal integration network. Using crossmodal paradigms is thus crucial to correctly evaluate the deficits presented by ADS in real-life situations.

[1]  R. Turner,et al.  Form and motion coherence activate independent, but not dorsal/ventral segregated, networks in the human brain , 2000, Current Biology.

[2]  P. Bertelson,et al.  Multisensory integration, perception and ecological validity , 2003, Trends in Cognitive Sciences.

[3]  B. Gelder,et al.  Audiovisual emotion recognition in schizophrenia: Reduced integration of facial and vocal affect , 2009, Schizophrenia Research.

[4]  田中 佐.  Research article , 2000, Hydrobiologia.

[5]  J. Vroomen,et al.  Multisensory integration of emotional faces and voices in schizophrenics , 2005, Schizophrenia Research.

[6]  Xavier Noël,et al.  Is two better than one? A cross-modal oddball paradigm reveals greater sensitivity of the P300 to emotional face-voice associations , 2010, Clinical Neurophysiology.

[7]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[8]  S. Campanella,et al.  Integrating face and voice in person perception , 2007, Trends in Cognitive Sciences.

[9]  Anne Lacheret,et al.  FMRI study of emotional speech comprehension. , 2006, Cerebral cortex.

[10]  Susan M. Courtney,et al.  Functional topography of working memory for face or voice identity , 2005, NeuroImage.

[11]  C. Spence,et al.  Assessing the effects of audiovisual semantic congruency on the perception of a bistable figure , 2012, Consciousness and Cognition.

[12]  Karl J. Friston.  Functional and effective connectivity in neuroimaging: A synthesis , 1994 .

[13]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[14]  Rufin VanRullen,et al.  Top-down and bottom-up modulation in processing bimodal face/voice stimuli , 2010, BMC Neuroscience.

[15]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[16]  P. Philippot,et al.  A validated battery of vocal emotional expressions. , 2007 .

[17]  D. Basu,et al.  Audiovestibular dysfunction in alcohol dependence. Are we worried? , 2006, American journal of otolaryngology.

[18]  Michael Erb,et al.  Audiovisual integration of emotional signals in voice and face: An event-related fMRI study , 2007, NeuroImage.

[19]  C. Harper,et al.  Ethanol and brain damage. , 2005, Current opinion in pharmacology.

[20]  Ruth Campbell,et al.  Audio–visual speech perception in schizophrenia: an fMRI study , 2001, Psychiatry Research: Neuroimaging.

[21]  M. Crommelinck,et al.  When audition alters vision: an event-related potential study of the cross-modal interactions between faces and voices , 2004, Neuroscience Letters.

[22]  C. Harper.  The neuropathology of alcohol-related brain damage. , 2009, Alcohol and alcoholism.

[23]  J. Martinot,et al.  Imaging of language-related brain regions in detoxified alcoholics. , 2009, Alcoholism, clinical and experimental research.

[24]  Lynne E. Bernstein,et al.  Spatiotemporal dynamics of audiovisual speech processing , 2008, NeuroImage.

[25]  Gregory G. Brown,et al.  fMRI BOLD response to alcohol stimuli in alcohol dependent young women. , 2004, Addictive behaviors.

[26]  C. Spence,et al.  Multisensory perception: Beyond modularity and convergence , 2000, Current Biology.

[27]  A. Giraud,et al.  Implicit Multisensory Associations Influence Voice Recognition , 2006, PLoS biology.

[28]  Pierre Maurage,et al.  The auditory-visual integration of anger is impaired in alcoholism: an event-related potentials study. , 2008, Journal of psychiatry & neuroscience : JPN.

[29]  D. Dietrich,et al.  Audiovisual integration of speech is disturbed in schizophrenia: An fMRI study , 2009, Schizophrenia Research.

[30]  E. Bullmore,et al.  Response amplification in sensory-specific cortices during crossmodal binding. , 1999, Neuroreport.

[31]  Abraham Weizman,et al.  Differences in audiovisual integration, as measured by McGurk phenomenon, among adult and adolescent patients with schizophrenia and age-matched healthy control groups. , 2009, Comprehensive psychiatry.

[32]  Pierre Maurage,et al.  The neural network sustaining the crossmodal processing of human gender from faces and voices: An fMRI study , 2011, NeuroImage.

[33]  I. Daum,et al.  Processing of Affective Stimuli in Alcoholism , 2005, Cortex.

[34]  P. Philippot,et al.  Is the P 300 deficit in alcoholism associated with early visual impairments ( P 100 , N 170 ) ? An oddball paradigm , 2006 .

[35]  R. Dolan,et al.  Crossmodal binding of fear in voice and face , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[36]  S. Iversen,et al.  Detection of Audio-Visual Integration Sites in Humans by Application of Electrophysiological Criteria to the BOLD Effect , 2001, NeuroImage.

[37]  Reza Momenan,et al.  Blunted rostral anterior cingulate response during a simplified decoding task of negative emotional facial expressions in alcoholic patients. , 2007, Alcoholism, clinical and experimental research.

[38]  X. Delbeuck,et al.  Is Alzheimer's disease a disconnection syndrome? Evidence from a crossmodal audio-visual illusory experiment , 2007, Neuropsychologia.

[39]  C. Mcintosh,et al.  Alcohol and the nervous system , 1997, Journal of Neurology, Neurosurgery & Psychiatry.

[40]  C. Spence,et al.  Crossmodal facilitation of masked visual target identification , 2010, Attention, perception & psychophysics.

[41]  Mark T. Wallace,et al.  Frontiers in Integrative Neuroscience Integrative Neuroscience , 2022 .

[42]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

[43]  S. Schweinberger,et al.  Auditory Long term Memory: Repetition Priming of Voice Recognition , 1997 .

[44]  H. Engeland,et al.  Brief Report: Can You See What is Not There? Low-level Auditory–visual Integration in Autism Spectrum Disorder , 2007, Journal of autism and developmental disorders.

[45]  Frank Schneider,et al.  Incongruence effects in crossmodal emotional integration , 2011, NeuroImage.

[46]  J. Lorenceau,et al.  Crossmodal integration for perception and action , 2004, Journal of Physiology-Paris.

[47]  Konstantin Voronin,et al.  Differential Brain Activity in Alcoholics and Social Drinkers to Alcohol Cues: Relationship to Craving , 2004, Neuropsychopharmacology.

[48]  P. Ekman.  Pictures of Facial Affect , 1976 .

[49]  P. Philippot,et al.  The crossmodal facilitation effect is disrupted in alcoholism: a study with emotional stimuli. , 2007, Alcohol and alcoholism.

[50]  Thorsten Kahnt,et al.  Brain activation elicited by affectively positive stimuli is associated with a lower risk of relapse in detoxified alcoholic subjects. , 2007, Alcoholism, clinical and experimental research.

[51]  G. Rhodes,et al.  Is the Fusiform Face Area Specialized for Faces, Individuation, or Expert Individuation? , 2004, Journal of Cognitive Neuroscience.

[52]  C. Kornreich,et al.  Supervisory attentional system in nonamnesic alcoholic men. , 2001, Archives of general psychiatry.

[53]  Karl Mann,et al.  Alcohol and the human brain: a systematic review of different neuroimaging methods. , 2011, Alcoholism, clinical and experimental research.

[54]  Gilles Pourtois,et al.  Investigating audiovisual integration of emotional signals in the human brain. , 2006, Progress in brain research.

[55]  A. Amedi,et al.  Functional imaging of human crossmodal identification and object recognition , 2005, Experimental Brain Research.

[56]  S. Nixon,et al.  Visuospatial perception, construction and memory in alcoholism. , 1996, Journal of studies on alcohol.

[57]  P. Philippot,et al.  Is the P300 deficit in alcoholism associated with early visual impairments (P100, N170)? An oddball paradigm , 2007, Clinical Neurophysiology.

[58]  A. McIntosh,et al.  The co-occurrence of multisensory facilitation and cross-modal conflict in the human brain. , 2011, Journal of neurophysiology.

[59]  F. Gosselin,et al.  Audio-visual integration of emotion expression , 2008, Brain Research.

[60]  B. Milliken,et al.  Audiovisual interactions depend on context of congruency , 2011, Attention, Perception, & Psychophysics.

[61]  U. Habel,et al.  Multisensory integration of emotionally valenced olfactory-visual information in patients with schizophrenia and healthy controls. , 2010, Journal of psychiatry & neuroscience : JPN.

[62]  I. Daum,et al.  Social cognition in alcoholism: a link to prefrontal cortex dysfunction? , 2008, Addiction.

[63]  Andreas Kleinschmidt,et al.  Interaction of Face and Voice Areas during Speaker Recognition , 2005, Journal of Cognitive Neuroscience.

[64]  Dylan M. Jones,et al.  Intra- and inter-modal repetition priming of familiar faces and voices. , 1997, British journal of psychology.

[65]  Clive Harper,et al.  The neurotoxicity of alcohol , 2007, Human & experimental toxicology.

[66]  David B. Pisoni,et al.  Discrete neural substrates underlie complementary audiovisual speech integration processes , 2011, NeuroImage.

[67]  Frank Schneider,et al.  Processing of disgusted faces is facilitated by odor primes: A functional MRI study , 2010, NeuroImage.

[68]  A. Pfefferbaum,et al.  Disruption of Brain White Matter Microstructure by Excessive Intracellular and Extracellular Fluid in Alcoholism: Evidence from Diffusion Tensor Imaging , 2005, Neuropsychopharmacology.

[69]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[70]  P. Belin,et al.  Thinking the voice: neural correlates of voice perception , 2004, Trends in Cognitive Sciences.

[71]  Paul J. Laurienti,et al.  On the use of superadditivity as a metric for characterizing multisensory integration in functional neuroimaging studies , 2005, Experimental Brain Research.

[72]  Steven W Anderson,et al.  Decision-making deficits, linked to a dysfunctional ventromedial prefrontal cortex, revealed in alcohol and stimulant abusers , 2001, Neuropsychologia.

[73]  Marianne Latinus,et al.  Cerebral correlates and statistical criteria of cross-modal face and voice integration. , 2011, Seeing and perceiving.

[74]  P Sterzer,et al.  Contributions of sensory input, auditory search and verbal comprehension to cortical activity during speech processing. , 2004, Cerebral cortex.

[75]  J. Kaiser,et al.  Functional neuroimaging studies in addiction: Multisensory drug stimuli and neural cue reactivity , 2012, Neuroscience & Biobehavioral Reviews.

[76]  John J. Foxe,et al.  Impaired multisensory processing in schizophrenia: Deficits in the visual enhancement of speech comprehension under noisy environmental conditions , 2007, Schizophrenia Research.

[77]  J. Richard Hanley,et al.  Why are Familiar-Only Experiences More Frequent for Voices than for Faces? , 2000, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[78]  J. Haxby,et al.  Human neural systems for face recognition and social communication , 2002, Biological Psychiatry.

[79]  B. de Gelder,et al.  Perceiving emotions from bodily expressions and multisensory integration of emotion cues in schizophrenia , 2011, Social neuroscience.

[80]  Stefan Gazdzinski,et al.  Tract-based spatial statistics (TBSS) of diffusion tensor imaging data in alcohol dependence: Abnormalities of the motivational neurocircuitry , 2009, Psychiatry Research: Neuroimaging.

[81]  S. Campanella,et al.  Cross-modal interactions between human faces and voices involved in person recognition , 2011, Cortex.

[82]  D H Whalen,et al.  Audiovisual Processing in Children with and without Autism Spectrum Disorders , 2008, Journal of autism and developmental disorders.

[83]  Jochen Kaiser,et al.  Smoking experience modulates the cortical integration of vision and haptics , 2012, NeuroImage.