Auditory and visual attention modulate motion processing in area MT+.

Behavioral and physiological studies have established that visual attention to a given feature or location can modulate early visual processing. In the present experiment, we asked whether auditory attention can likewise influence visual processing. We used a visual illusion, the motion aftereffect (MAE), to assess the effects of visual and auditory attention on motion processing in human area MT+. We acquired psychophysical and functional magnetic resonance imaging (fMRI) data while subjects fixated and viewed moving and stationary stimuli in alternating blocks. For each of four motion conditions, we measured the duration of the subsequent MAE, the time for activity in MT+ to return to baseline after motion adaptation (decay time), and the magnitude of MT+ activity during motion adaptation. For each subject, we first obtained measures of motion processing in the absence of attentional demands, by comparing reversing and expanding motion conditions. Subjects perceived the MAE following adaptation to expanding but not reversing motion, as observed previously, and decay times in MT+ were selectively prolonged after expanding motion. We then assessed the effects of performing either a visual or an auditory attentional task during expanding motion adaptation. Performance of the attentional task, whether visual or auditory, produced a significant reduction of subsequent MAE perception and associated decay times in MT+, as compared to expanding motion with fixation only. Both attentional tasks also reduced the magnitude of activation during motion adaptation. These data show that auditory attention, like visual attention, can modify sensory processing at a remarkably early stage of the visual hierarchy.

[1]  D. Somers,et al.  Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Richard S. J. Frackowiak,et al.  Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. , 1993, Cerebral cortex.

[3]  S. Miyauchi,et al.  Attention-regulated activity in human primary visual cortex. , 1998, Journal of neurophysiology.

[4]  T. Hendler,et al.  Visuo-haptic object-related activation in the ventral visual pathway , 2001, Nature Neuroscience.

[5]  C. Gilbert,et al.  Attention Modulates Contextual Influences in the Primary Visual Cortex of Alert Monkeys , 1999, Neuron.

[6]  Leslie G. Ungerleider,et al.  The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[8]  R. Desimone,et al.  Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. , 1997, Journal of neurophysiology.

[9]  B. Seltzer,et al.  Overlapping and nonoverlapping cortical projections to cortex of the superior temporal sulcus in the rhesus monkey: Double anterograde tracer studies , 1996 .

[10]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: congruent visual and somatic response properties. , 1998, Journal of neurophysiology.

[11]  Pieter R. Roelfsema,et al.  Object-based attention in the primary visual cortex of the macaque monkey , 1998, Nature.

[12]  A. Dale,et al.  The Retinotopy of Visual Spatial Attention , 1998, Neuron.

[13]  T. Raij Patterns of Brain Activity during Visual Imagery of Letters , 1999, Journal of Cognitive Neuroscience.

[14]  M Corbetta,et al.  Attentional modulation of neural processing of shape, color, and velocity in humans. , 1990, Science.

[15]  C D Frith,et al.  Modulating irrelevant motion perception by varying attentional load in an unrelated task. , 1997, Science.

[16]  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.

[17]  S. Shimojo,et al.  Illusions: What you see is what you hear , 2000, Nature.

[18]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[19]  P. Goldman-Rakic,et al.  Auditory belt and parabelt projections to the prefrontal cortex in the Rhesus monkey , 1999, The Journal of comparative neurology.

[20]  G. V. Simpson,et al.  Parieto‐occipital ∼1 0Hz activity reflects anticipatory state of visual attention mechanisms , 1998 .

[21]  John Duncan,et al.  Restricted attentional capacity within but not between sensory modalities , 1997, Nature.

[22]  G A Orban,et al.  Attention-dependent suppression of metabolic activity in the early stages of the macaque visual system. , 2000, Cerebral cortex.

[23]  James K. Kroger,et al.  Cross-modal and cross-temporal association in neurons of frontal cortex , 2000, Nature.

[24]  C. Schroeder,et al.  Intermodal selective attention in monkeys. I: distribution and timing of effects across visual areas. , 2000, Cerebral cortex.

[25]  M. Goldberg,et al.  Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. , 1996, Journal of neurophysiology.

[26]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  Ravi S. Menon,et al.  Recovery of fMRI activation in motion area MT following storage of the motion aftereffect. , 1999, Journal of neurophysiology.

[28]  Jon Driver,et al.  Inhibition of return is supramodal: a demonstration between all possible pairings of vision, touch, and audition , 2000, Experimental Brain Research.

[29]  M. Mesulam,et al.  Cortical afferent input to the principals region of the rhesus monkey , 1985, Neuroscience.

[30]  S. Hillyard,et al.  Intra-modal and cross-modal spatial attention to auditory and visual stimuli. An event-related brain potential study. , 1999, Brain research. Cognitive brain research.

[31]  K. Zilles,et al.  Polymodal Motion Processing in Posterior Parietal and Premotor Cortex A Human fMRI Study Strongly Implies Equivalencies between Humans and Monkeys , 2001, Neuron.

[32]  A. Chaudhuri Modulation of the motion aftereffect by selective attention , 1990, Nature.

[33]  E. DeYoe,et al.  Graded effects of spatial and featural attention on human area MT and associated motion processing areas. , 1997, Journal of neurophysiology.

[34]  Karl J. Friston,et al.  The physiological basis of attentional modulation in extrastriate visual areas , 1999, Nature Neuroscience.

[35]  C. Schroeder,et al.  Intermodal selective attention in monkeys. II: physiological mechanisms of modulation. , 2000, Cerebral cortex.

[36]  R. Desimone,et al.  Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. , 1981, Journal of neurophysiology.

[37]  E. Ziegel,et al.  Proceedings in Computational Statistics , 1998 .

[38]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[39]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

[40]  John H. R. Maunsell,et al.  Attentional modulation of visual motion processing in cortical areas MT and MST , 1996, Nature.

[41]  A. Dale,et al.  Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging , 1995, Nature.

[42]  Masataka Watanabe Frontal units of the monkey coding the associative significance of visual and auditory stimuli , 2004, Experimental Brain Research.

[43]  E. R. Cohen,et al.  Close correlation between activity in brain area MT/V5 and the perception of a visual motion aftereffect , 1998, Current Biology.

[44]  Frans A. J. Verstraten,et al.  The Motion Aftereffect:A Modern Perspective , 1998 .

[45]  J M Fuster,et al.  Behavioral electrophysiology of the prefrontal cortex of the primate. , 1990, Progress in brain research.

[46]  Christopher R. Genovese,et al.  A Bayesian Time-Course Model for Functional Magnetic Resonance Imaging Data , 2000 .

[47]  G. V. Simpson,et al.  Anticipatory Biasing of Visuospatial Attention Indexed by Retinotopically Specific α-Bank Electroencephalography Increases over Occipital Cortex , 2000, The Journal of Neuroscience.

[48]  B. Stein,et al.  Enhancement of Perceived Visual Intensity by Auditory Stimuli: A Psychophysical Analysis , 1996, Journal of Cognitive Neuroscience.

[49]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[50]  J. Vroomen,et al.  Sound enhances visual perception: cross-modal effects of auditory organization on vision. , 2000, Journal of experimental psychology. Human perception and performance.

[51]  A. Treisman,et al.  Voluntary Attention Modulates fMRI Activity in Human MT–MST , 1997, Neuron.

[52]  Martin Eimer,et al.  Can attention be directed to opposite locations in different modalities? An ERP study , 1999, Clinical Neurophysiology.

[53]  Martin A. Giese,et al.  Evidence for multi-functional interactions in early visual motion processing , 1999, Trends in Neurosciences.

[54]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.