Cortex controls multisensory depression in superior colliculus.

Multisensory depression is a fundamental index of multisensory integration in superior colliculus (SC) neurons. It is initiated when one sensory stimulus (auditory) located outside its modality-specific receptive field degrades or eliminates the neuron's responses to another sensory stimulus (visual) presented within its modality-specific receptive field. The present experiments demonstrate that the capacity of SC neurons to engage in multisensory depression is strongly dependent on influences from two cortical areas (the anterior ectosylvian and rostral lateral suprasylvian sulci). When these cortices are deactivated, the ability of SC neurons to synthesize visual-auditory inputs in this way is compromised; multisensory responses are disinhibited, becoming more vigorous and in some cases indistinguishable from responses to the visual stimulus alone. Although obtaining a more robust multisensory SC response when cortex is nonfunctional than when it is functional may seem paradoxical, these data may help explain previous observations that the loss of these cortical influences permits visual orientation behavior in the presence of a normally disruptive auditory stimulus.

[1]  J. Rauschecker Compensatory plasticity and sensory substitution in the cerebral cortex , 1995, Trends in Neurosciences.

[2]  Thomas J. Anastasio,et al.  Using Bayes' Rule to Model Multisensory Enhancement in the Superior Colliculus , 2000, Neural Computation.

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

[4]  E. Macaluso,et al.  Supramodal Effects of Covert Spatial Orienting Triggered by Visual or Tactile Events , 2002, Journal of Cognitive Neuroscience.

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

[6]  M T Wallace,et al.  Comparisons of cross-modality integration in midbrain and cortex. , 1996, Progress in brain research.

[7]  B. Stein,et al.  Interactions among converging sensory inputs in the superior colliculus. , 1983, Science.

[8]  L. Mucke,et al.  Physiologic and anatomic investigation of a visual cortical area situated in the ventral bank of the anterior ectosylvian sulcus of the cat , 2004, Experimental Brain Research.

[9]  D. Buonomano,et al.  Cortical plasticity: from synapses to maps. , 1998, Annual review of neuroscience.

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

[11]  M T Wallace,et al.  Development of Multisensory Neurons and Multisensory Integration in Cat Superior Colliculus , 1997, The Journal of Neuroscience.

[12]  D. Barth,et al.  The spatiotemporal organization of auditory, visual, and auditory-visual evoked potentials in rat cortex , 1995, Brain Research.

[13]  C. R. Michael,et al.  Integration of auditory information in the cat's visual cortex. , 1973, Vision research.

[14]  Stephen G. Lomber,et al.  The cryoloop: an adaptable reversible cooling deactivation method for behavioral or electrophysiological assessment of neural function , 1999, Journal of Neuroscience Methods.

[15]  Kota Takahashi,et al.  Integration of Visual and Auditory Information , 1990 .

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

[17]  P. Sterling,et al.  Effect on the Superior Colliculus of Cortical Removal in Visually Deprived Cats , 1969, Nature.

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

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

[20]  O D Creutzfeldt,et al.  Anterior ectosylvian visual area (AEV) of the cat: physiological properties. , 1988, Progress in brain research.

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

[22]  Josef P. Rauschecker,et al.  Auditory cortical plasticity: a comparison with other sensory systems , 1999, Trends in Neurosciences.

[23]  C. K. Peck Visual-auditory interactions in cat superior colliculus: their role in the control of gaze , 1987, Brain Research.

[24]  Lawrence G. McDade,et al.  Behavioral Indices of Multisensory Integration: Orientation to Visual Cues is Affected by Auditory Stimuli , 1989, Journal of Cognitive Neuroscience.

[25]  B E Stein,et al.  Corticotectal and corticothalamic efferent projections of SIV somatosensory cortex in cat. , 1983, Journal of neurophysiology.

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

[27]  nasa Representation and Integration of Scientific Information , 2004 .

[28]  Christopher T. Lovelace,et al.  An irrelevant light enhances auditory detection in humans: a psychophysical analysis of multisensory integration in stimulus detection. , 2003, Brain research. Cognitive brain research.

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

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

[31]  B. Stein,et al.  Spatial determinants of multisensory integration in cat superior colliculus neurons. , 1996, Journal of neurophysiology.

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

[33]  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.

[34]  B. Stein,et al.  Two Corticotectal Areas Facilitate Multisensory Orientation Behavior , 2002, Journal of Cognitive Neuroscience.

[35]  H. Burton,et al.  Ipsilateral cortical connections from the second and fourth somatic sensory areas in the cat , 1984, The Journal of comparative neurology.

[36]  M A Meredith,et al.  Descending efferents from the superior colliculus relay integrated multisensory information. , 1985, Science.

[37]  M. Wallace,et al.  Integration of multiple sensory modalities in cat cortex , 2004, Experimental Brain Research.

[38]  J. A. Horel 8 – Use of Cold to Reversibly Suppress Local Brain Function in Behaving Animals , 1991 .

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

[40]  B. Stein,et al.  Corticothalamic and corticotectal somatosensory projections from the anterior ectosylvian sulcus (SIV cortex) in neonatal cats: An anatomical demonstration with HRP and 3H‐leucine , 1988, The Journal of comparative neurology.

[41]  D. Irvine,et al.  Auditory response properties of neurons in the anterior ectosylvian sulcus of the cat , 1986, Brain Research.

[42]  M. Alex Meredith,et al.  The frontal eye fields target multisensory neurons in cat superior colliculus , 1999, Experimental Brain Research.

[43]  R. Lynn,et al.  A secular decline in the strength of Spearman’s g in Japan , 1994 .

[44]  C. Olson,et al.  Ectosylvian visual area of the cat: Location, retinotopic organization, and connections , 1987, The Journal of comparative neurology.

[45]  FRANK MORRELL,et al.  Visual System's View of Acoustic Space , 1972, Nature.

[46]  N. Bolognini,et al.  Enhancement of visual perception by crossmodal visuo-auditory interaction , 2002, Experimental Brain Research.

[47]  M A Meredith,et al.  The influence of stimulus properties on multisensory processing in the awake primate superior colliculus. , 2001, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[48]  E. Schröger,et al.  Speeded responses to audiovisual signal changes result from bimodal integration. , 1998, Psychophysiology.

[49]  Reinhart Jürgens,et al.  Sensor fusion by neural networks using spatially represented information , 2001, Biological Cybernetics.

[50]  B. Stein,et al.  The role of anterior ectosylvian cortex in cross-modality orientation and approach behavior , 1996, Experimental Brain Research.

[51]  E J Engelken,et al.  Saccadic eye movements in response to visual, auditory, and bisensory stimuli. , 1989, Aviation, space, and environmental medicine.

[52]  M. Radeau Auditory-visual spatial interaction and modularity , 1994, Current psychology of cognition = Cahiers de psychologie cognitive : CPC.

[53]  H. R. Clemo,et al.  Somatosensory cortex: a ‘new’ somatotopic representation , 1982, Brain Research.

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

[55]  M T Wallace,et al.  Cross-modal synthesis in the midbrain depends on input from cortex. , 1994, Journal of neurophysiology.

[56]  G. J. Thomas Experimental study of the influence of vision on sound localization. , 1941 .

[57]  Franco Lepore,et al.  Sensory interactions in the anterior ectosylvian cortex of cats , 2004, Experimental Brain Research.

[58]  C. Spence,et al.  Multimodal visual–somatosensory integration in saccade generation , 2003, Neuropsychologia.

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

[60]  H. R. Clemo,et al.  Organization of a fourth somatosensory area of cortex in cat. , 1983, Journal of neurophysiology.

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

[62]  B. Stein,et al.  A chronic headholder minimizing facial obstructions , 1983, Brain Research Bulletin.

[63]  R. Walker,et al.  Multisensory interactions in saccade target selection: Curved saccade trajectories , 2001, Experimental Brain Research.

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

[65]  Franco Lepore,et al.  Sensory modality distribution in the anterior ectosylvian cortex (AEC) of cats , 2004, Experimental Brain Research.

[66]  D P Munoz,et al.  The Influence of Auditory and Visual Distractors on Human Orienting Gaze Shifts , 1996, The Journal of Neuroscience.

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

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

[69]  D. Sparks,et al.  The functional organization of the primate superior colliculus: a motor perspective. , 1986, Progress in brain research.

[70]  R B Welch,et al.  Effect of Degree of Separation of Visual-Auditory Stimulus and Eye Position upon Spatial Interaction of Vision and Audition , 1976, Perceptual and motor skills.