Cross‐modal sensory processing in the anterior cingulate and medial prefrontal cortices

One of the principal functions of the nervous system is to synthesize information from multiple sensory channels into a coherent behavioral and perceptual gestalt. A critical feature of this multisensory synthesis is the sorting and coupling of information derived from the same event. One of the singular features of stimuli conveying such information is their contextual or semantic congruence. Illustrating this fact, subjects are typically faster and more accurate when performing tasks that include congruent compared to incongruent cross‐modal stimuli. Using functional magnetic resonance imaging, we demonstrate that activity in select brain areas is sensitive to the contextual congruence among cross‐modal cues and to task difficulty. The anterior cingulate gyrus and adjacent medial prefrontal cortices showed significantly greater activity when visual and auditory stimuli were contextually congruent (i.e., matching) than when they were nonmatching. Although activity in these regions was also dependent on task difficulty, showing decreased activity with decreasing task difficulty, the activity changes associated with stimulus congruence predominated. Hum. Brain Mapping 19:213–223, 2003. © 2003 Wiley‐Liss, Inc.

[1]  B. Stein,et al.  Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  R. Kikinis,et al.  Computer-assisted interactive three-dimensional planning for neurosurgical procedures. , 1996, Neurosurgery.

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

[4]  Zhong-Lin Lu,et al.  Modification of sudden onset auditory ERP by involuntary attention to visual stimuli. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[5]  Jeff Miller,et al.  Divided attention: Evidence for coactivation with redundant signals , 1982, Cognitive Psychology.

[6]  R. Kawashima,et al.  Selective Visual and Auditory Attention Toward Utterances—A PET Study , 1999, NeuroImage.

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

[8]  Alan C. Evans,et al.  Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions , 1999, Nature Neuroscience.

[9]  G. Ettlinger,et al.  Cross-modal performance: behavioural processes, phylogenetic considerations and neural mechanisms , 1990, Behavioural Brain Research.

[10]  M. Alex Meredith,et al.  Neurons and behavior: the same rules of multisensory integration apply , 1988, Brain Research.

[11]  Hans Forssberg,et al.  Increased Brain Activity in Frontal and Parietal Cortex Underlies the Development of Visuospatial Working Memory Capacity during Childhood , 2002, Journal of Cognitive Neuroscience.

[12]  Peter G. Aitken,et al.  Lesion effects on tactual to visual cross-modal matching in the rhesus monkey , 1980, Neuropsychologia.

[13]  Michael C. Dorris,et al.  Combined eye-head gaze shifts to visual and auditory targets in humans , 1996, Experimental Brain Research.

[14]  M T Wallace,et al.  Mechanisms of within- and cross-modality suppression in the superior colliculus. , 1997, Journal of neurophysiology.

[15]  J. Stroop Studies of interference in serial verbal reactions. , 1992 .

[16]  I H Bernstein,et al.  Effects of an auditory signal on visual reaction time. , 1969, Journal of experimental psychology.

[17]  J. Downar,et al.  A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. , 2002, Journal of neurophysiology.

[18]  R. Hari,et al.  Seeing speech: visual information from lip movements modifies activity in the human auditory cortex , 1991, Neuroscience Letters.

[19]  S. Shimojo,et al.  Sound alters visual evoked potentials in humans , 2001, Neuroreport.

[20]  M. Giard,et al.  Auditory-Visual Integration during Multimodal Object Recognition in Humans: A Behavioral and Electrophysiological Study , 1999, Journal of Cognitive Neuroscience.

[21]  B. Vogt,et al.  Pain Processing in Four Regions of Human Cingulate Cortex Localized with Co‐registered PET and MR Imaging , 1996, The European journal of neuroscience.

[22]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[23]  Y. Yen,et al.  Deactivation of Sensory-Specific Cortex by Cross-Modal Stimuli , 2002, Journal of Cognitive Neuroscience.

[24]  P E Roland,et al.  Cross-Modal Transfer of Information between the Tactile and the Visual Representations in the Human Brain: A Positron Emission Tomographic Study , 1998, The Journal of Neuroscience.

[25]  J. Andreassi,et al.  Effects of bisensory stimulation on reaction time and the evoked cortical potential , 1975 .

[26]  C. K. Peck,et al.  Spatial disparity affects visual-auditory interactions in human sensorimotor processing , 1998, Experimental Brain Research.

[27]  D. Raab DIVISION OF PSYCHOLOGY: STATISTICAL FACILITATION OF SIMPLE REACTION TIMES* , 1962 .

[28]  M HERSHENSON,et al.  Reaction time as a measure of intersensory facilitation. , 1962, Journal of experimental psychology.

[29]  R Kawashima,et al.  Positron-emission tomography studies of cross-modality inhibition in selective attentional tasks: closing the "mind's eye". , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[30]  S. Petersen,et al.  Functional Anatomic Studies of Memory Retrieval for Auditory Words and Visual Pictures , 1996, The Journal of Neuroscience.

[31]  R. Turner,et al.  Characterizing Evoked Hemodynamics with fMRI , 1995, NeuroImage.

[32]  P. Roland,et al.  Right prefrontal activation during encoding, but not during retrieval, in a non-verbal paired-associates task. , 1998, Cerebral cortex.

[33]  E. DeYoe,et al.  A comparison of visual and auditory motion processing in human cerebral cortex. , 2000, Cerebral cortex.

[34]  N. Costes,et al.  Emotional Responses to Pleasant and Unpleasant Olfactory, Visual, and Auditory Stimuli: a Positron Emission Tomography Study , 2000, The Journal of Neuroscience.

[35]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[36]  B. Stein,et al.  Spatial factors determine the activity of multisensory neurons in cat superior colliculus , 1986, Brain Research.

[37]  B. Buchbinder,et al.  Cortical activation MR studies in brain disorders. , 1998, Magnetic resonance imaging clinics of North America.

[38]  E. Bullmore,et al.  Activation of auditory cortex during silent lipreading. , 1997, Science.

[39]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[40]  M. Wallace,et al.  Representation and integration of multiple sensory inputs in primate superior colliculus. , 1996, Journal of neurophysiology.

[41]  Riitta Hari,et al.  Audiovisual Integration of Letters in the Human Brain , 2000, Neuron.

[42]  K. Zilles,et al.  Fast reaction to different sensory modalities activates common fields in the motor areas, but the anterior cingulate cortex is involved in the speed of reaction. , 2000, Journal of neurophysiology.

[43]  P. Reuter-Lorenz,et al.  Visual-auditory interactions in sensorimotor processing: saccades versus manual responses. , 1994, Journal of experimental psychology. Human perception and performance.

[44]  B. Stein,et al.  Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. , 1986, Journal of neurophysiology.

[45]  T. Cizadlo,et al.  Auditory and visual attention assessed with PET , 1997, Human brain mapping.

[46]  R. Schmidt,et al.  On the nature of intersensory facilitation of reaction time , 1983, Perception & psychophysics.

[47]  R. Turner,et al.  Characterizing Dynamic Brain Responses with fMRI: A Multivariate Approach , 1995, NeuroImage.

[48]  J. Ridley Studies of Interference in Serial Verbal Reactions , 2001 .

[49]  C. Frith,et al.  Modulation of human visual cortex by crossmodal spatial attention. , 2000, Science.

[50]  N. Alpert,et al.  Auditory Priming within and across Modalities: Evidence from Positron Emission Tomography , 1999, Journal of Cognitive Neuroscience.

[51]  S. Petersen,et al.  The effects of practice on the functional anatomy of task performance. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[52]  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 .

[53]  J. Maisog,et al.  Pain intensity processing within the human brain: a bilateral, distributed mechanism. , 1999, Journal of neurophysiology.

[54]  P. Roland,et al.  Interference between two concurrent tasks is associated with activation of overlapping fields in the cortex. , 1997, Brain research. Cognitive brain research.

[55]  B. Stein,et al.  The Merging of the Senses , 1993 .

[56]  E. Macaluso,et al.  Spatial attention and crossmodal interactions between vision and touch , 2001, Neuropsychologia.

[57]  Ravi S. Menon,et al.  Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model. , 1993, Biophysical journal.

[58]  J. Desmond,et al.  Prefrontal regions involved in keeping information in and out of mind. , 2001, Brain : a journal of neurology.

[59]  B. Vogt,et al.  Pain and Stroop interference tasks activate separate processing modules in anterior cingulate cortex , 1998, Experimental Brain Research.

[60]  M. Frens,et al.  Spatial and temporal factors determine auditory-visual interactions in human saccadic eye movements , 1995, Perception & psychophysics.

[61]  J. Aggleton,et al.  The functional anatomy of visual-tactile integration in man: a study using positron emission tomography , 2000, Neuropsychologia.

[62]  John J. Foxe,et al.  Multisensory auditory-somatosensory interactions in early cortical processing revealed by high-density electrical mapping. , 2000, Brain research. Cognitive brain research.

[63]  Jonathan D. Cohen,et al.  Conflict monitoring versus selection-for-action in anterior cingulate cortex , 1999, Nature.

[64]  G. W. Snedecor Statistical Methods , 1964 .

[65]  R. Campbell,et al.  Evidence from functional magnetic resonance imaging of crossmodal binding in the human heteromodal cortex , 2000, Current Biology.

[66]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[67]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[68]  W. Jiang,et al.  Two cortical areas mediate multisensory integration in superior colliculus neurons. , 2001, Journal of neurophysiology.

[69]  D. Raab Statistical facilitation of simple reaction times. , 1962, Transactions of the New York Academy of Sciences.

[70]  S. Rauch,et al.  The counting stroop: An interference task specialized for functional neuroimaging—validation study with functional MRI , 1998, Human brain mapping.

[71]  M. Posner,et al.  Attention, self-regulation and consciousness. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[72]  B R Rosen,et al.  Modulation of auditory and visual cortex by selective attention is modality-dependent. , 1996, Neuroreport.

[73]  Paul J. Laurienti,et al.  Dietary Caffeine Consumption Modulates fMRI Measures , 2002, NeuroImage.

[74]  R. Turner,et al.  Functional magnetic resonance imaging of the human brain: data acquisition and analysis , 1998, Experimental Brain Research.

[75]  A. Opstal,et al.  Visual-auditory interactions modulate saccade-related activity in monkey superior colliculus , 1998, Brain Research Bulletin.

[76]  J. Sawusch,et al.  Covert Auditory Attention Generates Activation in the Rostral/Dorsal Anterior Cingulate Cortex , 2002, Journal of Cognitive Neuroscience.

[77]  J A Maldjian,et al.  Wavelet transform-based image compression for transmission of MR data. , 1997, AJR. American journal of roentgenology.

[78]  H. C. Hughes,et al.  Parallel and serial processes in the human oculomotor system: bimodal integration and express saccades , 2004, Biological Cybernetics.

[79]  Michael I. Posner,et al.  Mapping the Cingulate Cortex in Response Selection and Monitoring , 1998, NeuroImage.

[80]  Francesco Pavani,et al.  Acoustical Vision of Neglected Stimuli: Interaction among Spatially Converging Audiovisual Inputs in Neglect Patients , 2002, Journal of Cognitive Neuroscience.

[81]  B. Vogt,et al.  The medial pain system, cingulate cortex, and parallel processing of nociceptive information. , 2000, Progress in brain research.

[82]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[83]  K. Saberi,et al.  Auditory psychomotor coordination and visual search performance , 1990, Perception & psychophysics.

[84]  William E. Lorensen,et al.  Computer-assisted Interactive Three-dimensional Planning Neurosurgical Procedures , 1996 .

[85]  Katie L. McMahon,et al.  Orthographic/Phonological Facilitation of Naming Responses in the Picture–Word Task: An Event-Related fMRI Study Using Overt Vocal Responding , 2002, NeuroImage.

[86]  G. Calvert Crossmodal processing in the human brain: insights from functional neuroimaging studies. , 2001, Cerebral cortex.