Visual and auditory cue integration for the generation of saccadic eye movements in monkeys and lever pressing in humans

This study examined how effectively visual and auditory cues can be integrated in the brain for the generation of motor responses. The latencies with which saccadic eye movements are produced in humans and monkeys form, under certain conditions, a bimodal distribution, the first mode of which has been termed express saccades. In humans, a much higher percentage of express saccades is generated when both visual and auditory cues are provided compared with the single presentation of these cues [H. C. Hughes et al. (1994) J. Exp. Psychol. Hum. Percept. Perform., 20, 131–153]. In this study, we addressed two questions: first, do monkeys also integrate visual and auditory cues for express saccade generation as do humans and second, does such integration take place in humans when, instead of eye movements, the task is to press levers with fingers? Our results show that (i) in monkeys, as in humans, the combined visual and auditory cues generate a much higher percentage of express saccades than do singly presented cues and (ii) the latencies with which levers are pressed by humans are shorter when both visual and auditory cues are provided compared with the presentation of single cues, but the distribution in all cases is unimodal; response latencies in the express range seen in the execution of saccadic eye movements are not obtained with lever pressing.

[1]  J. Todd,et al.  Reaction To Multiple Stimuli... , 2012 .

[2]  P. H. Schiller,et al.  The integration of disparity, shading and motion parallax cues for depth perception in humans and monkeys , 2011, Brain Research.

[3]  Geoffrey L. Kendall,et al.  Conditions that alter saccadic eye movement latencies and affect target choice to visual stimuli and to electrical stimulation of area V1 in the monkey , 2008, Visual Neuroscience.

[4]  S. Celebrini,et al.  Visuo-auditory interactions in the primary visual cortex of the behaving monkey: Electrophysiological evidence , 2008, BMC Neuroscience.

[5]  Ying Zhang,et al.  The effect of overall stimulus velocity on motion parallax , 2008, Visual Neuroscience.

[6]  Peter H Schiller,et al.  How the parallel channels of the retina contribute to depth processing , 2007, The European journal of neuroscience.

[7]  Ying Zhang,et al.  Depth from shading and disparity in humans and monkeys , 2007, Visual Neuroscience.

[8]  David A. Bulkin,et al.  Seeing sounds: visual and auditory interactions in the brain , 2006, Current Opinion in Neurobiology.

[9]  Y. Lacasse,et al.  From the authors , 2005, European Respiratory Journal.

[10]  A John Van Opstal,et al.  Crossmodal integration in the primate superior colliculus underlying the preparation and initiation of saccadic eye movements. , 2005, Journal of neurophysiology.

[11]  P. H. Schiller,et al.  Are express saccades generated under natural viewing conditions? , 2004, European Journal of Neuroscience.

[12]  A. Diederich,et al.  Bimodal and trimodal multisensory enhancement: Effects of stimulus onset and intensity on reaction time , 2004, Perception & psychophysics.

[13]  P. H. Schiller,et al.  How do target predictability and precueing affect the production of express saccades in monkeys? , 2004, The European journal of neuroscience.

[14]  P. H. Schiller,et al.  An examination of the variables that affect express saccade generation , 2004, Visual Neuroscience.

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

[16]  Peter H Schiller,et al.  Cortical inhibitory circuits in eye‐movement generation , 2003, The European journal of neuroscience.

[17]  Hans Colonius,et al.  Visual-tactile spatial interaction in saccade generation , 2003, Experimental Brain Research.

[18]  P. H. Schiller,et al.  Neural responses to relative speed in the primary visual cortex of rhesus monkey , 2003, Visual Neuroscience.

[19]  An Cao,et al.  Behavioral assessment of motion parallax and stereopsis as depth cues in rhesus monkeys , 2002, Vision Research.

[20]  Peter H Schiller,et al.  The effects of anterior arcuate and dorsomedial frontal cortex lesions on visually guided eye movements: 2. Paired and multiple targets , 2000, Vision Research.

[21]  Peter H Schiller,et al.  The effects of anterior arcuate and dorsomedial frontal cortex lesions on visually guided eye movements in the rhesus monkey: 1. Single and sequential targets , 2000, Vision Research.

[22]  H. Hughes,et al.  Spatial characteristics of visual-auditory summation in human saccades , 1998, Vision Research.

[23]  B. Stein Neural mechanisms for synthesizing sensory information and producing adaptive behaviors , 1998, Experimental Brain Research.

[24]  P. H. Schiller,et al.  The effects of V4 and middle temporal (MT) area lesions on visual performance in the rhesus monkey , 1993, Visual Neuroscience.

[25]  John H. R. Maunsell,et al.  The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey. , 1987, Journal of neurophysiology.

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

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

[28]  B. Fischer,et al.  Saccadic eye movements after extremely short reaction times in the monkey , 1983, Brain Research.

[29]  J. L. Conway,et al.  Deficits in eye movements following frontal eye-field and superior colliculus ablations. , 1980, Journal of neurophysiology.

[30]  J. L. Conway,et al.  Effects of frontal eye field and superior colliculus ablations on eye movements. , 1979, Science.

[31]  Peter H. Schiller,et al.  The effect of superior colliculus ablation on saccades elicted by cortical stimulation , 1977, Brain Research.

[32]  P. Schiller,et al.  The role of the monkey superior colliculus in eye movement and vision. , 1972, Investigative ophthalmology.

[33]  M. T. Wallace,et al.  Visual, auditory and somatosensory convergence in output neurons of the cat superior colliculus: multisensory properties of the tecto-reticulo-spinal projection , 2005, Experimental Brain Research.

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

[35]  B. Fischer,et al.  Further observations on the occurrence of express-saccades in the monkey , 2004, Experimental Brain Research.

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

[37]  P H Schiller,et al.  Look and see: how the brain moves your eyes about. , 2001, Progress in brain research.

[38]  D. Sparks,et al.  Saccades to somatosensory targets. I. behavioral characteristics. , 1996, Journal of neurophysiology.

[39]  J M Groh,et al.  Saccades to somatosensory targets. II. motor convergence in primate superior colliculus. , 1996, Journal of neurophysiology.

[40]  J M Groh,et al.  Saccades to somatosensory targets. III. eye-position-dependent somatosensory activity in primate superior colliculus. , 1996, Journal of neurophysiology.

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

[42]  B Fischer,et al.  The preparation of visually guided saccades. , 1987, Reviews of physiology, biochemistry and pharmacology.

[43]  D L Sparks,et al.  Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. , 1986, Physiological reviews.

[44]  J. E. Albano,et al.  Visual-motor function of the primate superior colliculus. , 1980, Annual review of neuroscience.

[45]  P. H. Schiller The Primate Superior Colliculus and its Sensory Inputs , 1978 .