Crossmodal Integration in the Primate Superior Colliculus Underlying the Preparation and Initiation of Saccadic Eye Movements
1 Centre for Neuroscience Studies, Canadian Institutes of Health Research Group in Sensory-Motor Systems, Department of Physiology, Queens University, Kingston, Ontario, Canada; 2 Department of Anatomy and Neurobiology, Virginia Commonwealth University School of Medicine, Richmond, Virginia; and 3...
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Veröffentlicht in: | Journal of neurophysiology 2005-06, Vol.93 (6), p.3659-3673 |
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creator | Bell, Andrew H Meredith, M. Alex Van Opstal, A. John Munoz, Douglas P |
description | 1 Centre for Neuroscience Studies, Canadian Institutes of Health Research Group in Sensory-Motor Systems, Department of Physiology, Queens University, Kingston, Ontario, Canada; 2 Department of Anatomy and Neurobiology, Virginia Commonwealth University School of Medicine, Richmond, Virginia; and 3 Institute for Neuroscience, Department of Biophysics, Radboud University Nijmegen, Nijmegen, The Netherlands
Submitted 29 November 2004;
accepted in final form 5 February 2005
Saccades to combined audiovisual stimuli often have reduced saccadic reaction times (SRTs) compared with those to unimodal stimuli. Neurons in the intermediate/deep layers of the superior colliculus (dSC) are capable of integrating converging sensory inputs to influence the time to saccade initiation. To identify how neural processing in the dSC contributes to reducing SRTs to audiovisual stimuli, we recorded activity from dSC neurons while monkeys generated saccades to visual or audiovisual stimuli. To evoke crossmodal interactions of varying strength, we used auditory and visual stimuli of different intensities, presented either in spatial alignment or to opposite hemifields. Spatially aligned audiovisual stimuli evoked the shortest SRTs. In the case of low-intensity stimuli, the response to the auditory component of the aligned audiovisual target increased the activity preceding the response to the visual component, accelerating the onset of the visual response and facilitating the generation of shorter-latency saccades. In the case of high-intensity stimuli, the auditory and visual responses occurred much closer together in time and so there was little opportunity for the auditory stimulus to influence previsual activity. Instead, the reduction in SRT for high-intensity, aligned audiovisual stimuli was correlated with increased premotor activity (activity after visual burst but preceding saccade-aligned burst). These data provide a link between changes in neural activity related to stimulus modality with changes in behavior. They further demonstrate how crossmodal interactions are not limited to the initial sensory activity but can also influence premotor activity in the SC.
Address for reprint requests and other correspondence: D. Munoz, Centre for Neuroscience Studies, Queens University, Kingston, Ontario, Canada K7L 3N6 (E-mail: doug{at}eyeml.queensu.ca ) |
doi_str_mv | 10.1152/jn.01214.2004 |
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Submitted 29 November 2004;
accepted in final form 5 February 2005
Saccades to combined audiovisual stimuli often have reduced saccadic reaction times (SRTs) compared with those to unimodal stimuli. Neurons in the intermediate/deep layers of the superior colliculus (dSC) are capable of integrating converging sensory inputs to influence the time to saccade initiation. To identify how neural processing in the dSC contributes to reducing SRTs to audiovisual stimuli, we recorded activity from dSC neurons while monkeys generated saccades to visual or audiovisual stimuli. To evoke crossmodal interactions of varying strength, we used auditory and visual stimuli of different intensities, presented either in spatial alignment or to opposite hemifields. Spatially aligned audiovisual stimuli evoked the shortest SRTs. In the case of low-intensity stimuli, the response to the auditory component of the aligned audiovisual target increased the activity preceding the response to the visual component, accelerating the onset of the visual response and facilitating the generation of shorter-latency saccades. In the case of high-intensity stimuli, the auditory and visual responses occurred much closer together in time and so there was little opportunity for the auditory stimulus to influence previsual activity. Instead, the reduction in SRT for high-intensity, aligned audiovisual stimuli was correlated with increased premotor activity (activity after visual burst but preceding saccade-aligned burst). These data provide a link between changes in neural activity related to stimulus modality with changes in behavior. They further demonstrate how crossmodal interactions are not limited to the initial sensory activity but can also influence premotor activity in the SC.
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Submitted 29 November 2004;
accepted in final form 5 February 2005
Saccades to combined audiovisual stimuli often have reduced saccadic reaction times (SRTs) compared with those to unimodal stimuli. Neurons in the intermediate/deep layers of the superior colliculus (dSC) are capable of integrating converging sensory inputs to influence the time to saccade initiation. To identify how neural processing in the dSC contributes to reducing SRTs to audiovisual stimuli, we recorded activity from dSC neurons while monkeys generated saccades to visual or audiovisual stimuli. To evoke crossmodal interactions of varying strength, we used auditory and visual stimuli of different intensities, presented either in spatial alignment or to opposite hemifields. Spatially aligned audiovisual stimuli evoked the shortest SRTs. In the case of low-intensity stimuli, the response to the auditory component of the aligned audiovisual target increased the activity preceding the response to the visual component, accelerating the onset of the visual response and facilitating the generation of shorter-latency saccades. In the case of high-intensity stimuli, the auditory and visual responses occurred much closer together in time and so there was little opportunity for the auditory stimulus to influence previsual activity. Instead, the reduction in SRT for high-intensity, aligned audiovisual stimuli was correlated with increased premotor activity (activity after visual burst but preceding saccade-aligned burst). These data provide a link between changes in neural activity related to stimulus modality with changes in behavior. They further demonstrate how crossmodal interactions are not limited to the initial sensory activity but can also influence premotor activity in the SC.
Address for reprint requests and other correspondence: D. Munoz, Centre for Neuroscience Studies, Queens University, Kingston, Ontario, Canada K7L 3N6 (E-mail: doug{at}eyeml.queensu.ca )</description><subject>Acoustic Stimulation - methods</subject><subject>Animals</subject><subject>Auditory Pathways - physiology</subject><subject>Brain Mapping</subject><subject>Cell Count - methods</subject><subject>Dose-Response Relationship, Radiation</subject><subject>Macaca mulatta</subject><subject>Male</subject><subject>Models, Neurological</subject><subject>Neurons - classification</subject><subject>Neurons - physiology</subject><subject>Photic Stimulation - methods</subject><subject>Reaction Time - physiology</subject><subject>Saccades - physiology</subject><subject>Sensory Thresholds</subject><subject>Statistics as Topic</subject><subject>Superior Colliculi - cytology</subject><subject>Time Factors</subject><subject>Visual Pathways - physiology</subject><issn>0022-3077</issn><issn>1522-1598</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2005</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kL1v1DAYhy0EokfbkRV5olMOf8TOZUSnllYqAqntbPniN3c-OXawE2gG_vc6XAQT0_uh5_cbHoTeU7KmVLBPR78mlNFyzQgpX6FV_rGCinrzGq0IyTsnVXWG3qV0JIRUgrC36IyKinDG2Ar93saQUheMdvjOD7CPerDBY-vxcAD8PdpOD4Afxh6iDRFvg3O2Gd2Y8JM3EN1k_X5BoddLWnuT2-xgT2do8YNuGm1sg68nwF_DT-jAD-kCvWm1S3C5zHP0dHP9uL0t7r99udt-vi8aQfhQiEbWOy42smTAtIAyz6rcSM7aitOaGdJqxlrRyp1mhFIiQO5K2XBtuKmk5Ofo46m3j-HHCGlQnU0NOKc9hDEpWnHBuKAZLE5gM2uJ0Kp-NhAnRYmafaujV398q9l35j8sxeOuA_OPXgRn4OoEHOz-8MtGUP1hSja4sJ_mrporqbgUdSb5_8mb0blHeB5y5G9C9ablLwGsnNo</recordid><startdate>20050601</startdate><enddate>20050601</enddate><creator>Bell, Andrew H</creator><creator>Meredith, M. Alex</creator><creator>Van Opstal, A. John</creator><creator>Munoz, Douglas P</creator><general>Am Phys Soc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope></search><sort><creationdate>20050601</creationdate><title>Crossmodal Integration in the Primate Superior Colliculus Underlying the Preparation and Initiation of Saccadic Eye Movements</title><author>Bell, Andrew H ; Meredith, M. Alex ; Van Opstal, A. John ; Munoz, Douglas P</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c503t-5c69b358642e2a5e442e748632f73192d0fa22f5f6ba201105e6b46c3ad3d7663</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2005</creationdate><topic>Acoustic Stimulation - methods</topic><topic>Animals</topic><topic>Auditory Pathways - physiology</topic><topic>Brain Mapping</topic><topic>Cell Count - methods</topic><topic>Dose-Response Relationship, Radiation</topic><topic>Macaca mulatta</topic><topic>Male</topic><topic>Models, Neurological</topic><topic>Neurons - classification</topic><topic>Neurons - physiology</topic><topic>Photic Stimulation - methods</topic><topic>Reaction Time - physiology</topic><topic>Saccades - physiology</topic><topic>Sensory Thresholds</topic><topic>Statistics as Topic</topic><topic>Superior Colliculi - cytology</topic><topic>Time Factors</topic><topic>Visual Pathways - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bell, Andrew H</creatorcontrib><creatorcontrib>Meredith, M. 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John</au><au>Munoz, Douglas P</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Crossmodal Integration in the Primate Superior Colliculus Underlying the Preparation and Initiation of Saccadic Eye Movements</atitle><jtitle>Journal of neurophysiology</jtitle><addtitle>J Neurophysiol</addtitle><date>2005-06-01</date><risdate>2005</risdate><volume>93</volume><issue>6</issue><spage>3659</spage><epage>3673</epage><pages>3659-3673</pages><issn>0022-3077</issn><eissn>1522-1598</eissn><abstract>1 Centre for Neuroscience Studies, Canadian Institutes of Health Research Group in Sensory-Motor Systems, Department of Physiology, Queens University, Kingston, Ontario, Canada; 2 Department of Anatomy and Neurobiology, Virginia Commonwealth University School of Medicine, Richmond, Virginia; and 3 Institute for Neuroscience, Department of Biophysics, Radboud University Nijmegen, Nijmegen, The Netherlands
Submitted 29 November 2004;
accepted in final form 5 February 2005
Saccades to combined audiovisual stimuli often have reduced saccadic reaction times (SRTs) compared with those to unimodal stimuli. Neurons in the intermediate/deep layers of the superior colliculus (dSC) are capable of integrating converging sensory inputs to influence the time to saccade initiation. To identify how neural processing in the dSC contributes to reducing SRTs to audiovisual stimuli, we recorded activity from dSC neurons while monkeys generated saccades to visual or audiovisual stimuli. To evoke crossmodal interactions of varying strength, we used auditory and visual stimuli of different intensities, presented either in spatial alignment or to opposite hemifields. Spatially aligned audiovisual stimuli evoked the shortest SRTs. In the case of low-intensity stimuli, the response to the auditory component of the aligned audiovisual target increased the activity preceding the response to the visual component, accelerating the onset of the visual response and facilitating the generation of shorter-latency saccades. In the case of high-intensity stimuli, the auditory and visual responses occurred much closer together in time and so there was little opportunity for the auditory stimulus to influence previsual activity. Instead, the reduction in SRT for high-intensity, aligned audiovisual stimuli was correlated with increased premotor activity (activity after visual burst but preceding saccade-aligned burst). These data provide a link between changes in neural activity related to stimulus modality with changes in behavior. They further demonstrate how crossmodal interactions are not limited to the initial sensory activity but can also influence premotor activity in the SC.
Address for reprint requests and other correspondence: D. Munoz, Centre for Neuroscience Studies, Queens University, Kingston, Ontario, Canada K7L 3N6 (E-mail: doug{at}eyeml.queensu.ca )</abstract><cop>United States</cop><pub>Am Phys Soc</pub><pmid>15703222</pmid><doi>10.1152/jn.01214.2004</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Acoustic Stimulation - methods Animals Auditory Pathways - physiology Brain Mapping Cell Count - methods Dose-Response Relationship, Radiation Macaca mulatta Male Models, Neurological Neurons - classification Neurons - physiology Photic Stimulation - methods Reaction Time - physiology Saccades - physiology Sensory Thresholds Statistics as Topic Superior Colliculi - cytology Time Factors Visual Pathways - physiology |
title | Crossmodal Integration in the Primate Superior Colliculus Underlying the Preparation and Initiation of Saccadic Eye Movements |
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