Dissociable Cortical and Subcortical Mechanisms for Mediating the Influences of Visual Cues on Microsaccadic Eye Movements
Visual selection in primates is intricately linked to eye movements, which are generated by a network of cortical and subcortical neural circuits. When visual selection is performed covertly, without foveating eye movements toward the selected targets, a class of fixational eye movements, called mic...
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| Format: | Article |
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Frontiers Media S.A.
2021-03-01
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| Series: | Frontiers in Neural Circuits |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fncir.2021.638429/full |
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| author | Ziad M. Hafed Ziad M. Hafed Masatoshi Yoshida Xiaoguang Tian Antimo Buonocore Antimo Buonocore Tatiana Malevich Tatiana Malevich Tatiana Malevich |
| author_facet | Ziad M. Hafed Ziad M. Hafed Masatoshi Yoshida Xiaoguang Tian Antimo Buonocore Antimo Buonocore Tatiana Malevich Tatiana Malevich Tatiana Malevich |
| author_sort | Ziad M. Hafed |
| collection | DOAJ |
| description | Visual selection in primates is intricately linked to eye movements, which are generated by a network of cortical and subcortical neural circuits. When visual selection is performed covertly, without foveating eye movements toward the selected targets, a class of fixational eye movements, called microsaccades, is still involved. Microsaccades are small saccades that occur when maintaining precise gaze fixation on a stationary point, and they exhibit robust modulations in peripheral cueing paradigms used to investigate covert visual selection mechanisms. These modulations consist of changes in both microsaccade directions and frequencies after cue onsets. Over the past two decades, the properties and functional implications of these modulations have been heavily studied, revealing a potentially important role for microsaccades in mediating covert visual selection effects. However, the neural mechanisms underlying cueing effects on microsaccades are only beginning to be investigated. Here we review the available causal manipulation evidence for these effects’ cortical and subcortical substrates. In the superior colliculus (SC), activity representing peripheral visual cues strongly influences microsaccade direction, but not frequency, modulations. In the cortical frontal eye fields (FEF), activity only compensates for early reflexive effects of cues on microsaccades. Using evidence from behavior, theoretical modeling, and preliminary lesion data from the primary visual cortex and microstimulation data from the lower brainstem, we argue that the early reflexive microsaccade effects arise subcortically, downstream of the SC. Overall, studying cueing effects on microsaccades in primates represents an important opportunity to link perception, cognition, and action through unaddressed cortical-subcortical neural interactions. These interactions are also likely relevant in other sensory and motor modalities during other active behaviors. |
| first_indexed | 2024-12-17T08:44:16Z |
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| id | doaj.art-92ce4b663ca746079b30af0ec15b9c26 |
| institution | Directory Open Access Journal |
| issn | 1662-5110 |
| language | English |
| last_indexed | 2024-12-17T08:44:16Z |
| publishDate | 2021-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neural Circuits |
| spelling | doaj.art-92ce4b663ca746079b30af0ec15b9c262022-12-21T21:56:15ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102021-03-011510.3389/fncir.2021.638429638429Dissociable Cortical and Subcortical Mechanisms for Mediating the Influences of Visual Cues on Microsaccadic Eye MovementsZiad M. Hafed0Ziad M. Hafed1Masatoshi Yoshida2Xiaoguang Tian3Antimo Buonocore4Antimo Buonocore5Tatiana Malevich6Tatiana Malevich7Tatiana Malevich8Physiology of Active Vision Laboratory, Werner Reichardt Centre for Integrative Neuroscience, Tübingen University, Tübingen, GermanyHertie Institute for Clinical Brain Research, Tübingen University, Tübingen, GermanyCenter for Human Nature, Artificial Intelligence, and Neuroscience, Hokkaido University, Sapporo, JapanDepartment of Neurobiology, University of Pittsburgh Brain Institute, University of Pittsburgh, Pittsburgh, PA, United StatesPhysiology of Active Vision Laboratory, Werner Reichardt Centre for Integrative Neuroscience, Tübingen University, Tübingen, GermanyHertie Institute for Clinical Brain Research, Tübingen University, Tübingen, GermanyPhysiology of Active Vision Laboratory, Werner Reichardt Centre for Integrative Neuroscience, Tübingen University, Tübingen, GermanyHertie Institute for Clinical Brain Research, Tübingen University, Tübingen, GermanyGraduate School of Neural and Behavioural Sciences, International Max-Planck Research School, Tübingen University, Tübingen, GermanyVisual selection in primates is intricately linked to eye movements, which are generated by a network of cortical and subcortical neural circuits. When visual selection is performed covertly, without foveating eye movements toward the selected targets, a class of fixational eye movements, called microsaccades, is still involved. Microsaccades are small saccades that occur when maintaining precise gaze fixation on a stationary point, and they exhibit robust modulations in peripheral cueing paradigms used to investigate covert visual selection mechanisms. These modulations consist of changes in both microsaccade directions and frequencies after cue onsets. Over the past two decades, the properties and functional implications of these modulations have been heavily studied, revealing a potentially important role for microsaccades in mediating covert visual selection effects. However, the neural mechanisms underlying cueing effects on microsaccades are only beginning to be investigated. Here we review the available causal manipulation evidence for these effects’ cortical and subcortical substrates. In the superior colliculus (SC), activity representing peripheral visual cues strongly influences microsaccade direction, but not frequency, modulations. In the cortical frontal eye fields (FEF), activity only compensates for early reflexive effects of cues on microsaccades. Using evidence from behavior, theoretical modeling, and preliminary lesion data from the primary visual cortex and microstimulation data from the lower brainstem, we argue that the early reflexive microsaccade effects arise subcortically, downstream of the SC. Overall, studying cueing effects on microsaccades in primates represents an important opportunity to link perception, cognition, and action through unaddressed cortical-subcortical neural interactions. These interactions are also likely relevant in other sensory and motor modalities during other active behaviors.https://www.frontiersin.org/articles/10.3389/fncir.2021.638429/fullsuperior colliculusfrontal eye fieldsprimary visual cortexbrainstem omnipause neuronsvisual attentionmicrosaccades |
| spellingShingle | Ziad M. Hafed Ziad M. Hafed Masatoshi Yoshida Xiaoguang Tian Antimo Buonocore Antimo Buonocore Tatiana Malevich Tatiana Malevich Tatiana Malevich Dissociable Cortical and Subcortical Mechanisms for Mediating the Influences of Visual Cues on Microsaccadic Eye Movements Frontiers in Neural Circuits superior colliculus frontal eye fields primary visual cortex brainstem omnipause neurons visual attention microsaccades |
| title | Dissociable Cortical and Subcortical Mechanisms for Mediating the Influences of Visual Cues on Microsaccadic Eye Movements |
| title_full | Dissociable Cortical and Subcortical Mechanisms for Mediating the Influences of Visual Cues on Microsaccadic Eye Movements |
| title_fullStr | Dissociable Cortical and Subcortical Mechanisms for Mediating the Influences of Visual Cues on Microsaccadic Eye Movements |
| title_full_unstemmed | Dissociable Cortical and Subcortical Mechanisms for Mediating the Influences of Visual Cues on Microsaccadic Eye Movements |
| title_short | Dissociable Cortical and Subcortical Mechanisms for Mediating the Influences of Visual Cues on Microsaccadic Eye Movements |
| title_sort | dissociable cortical and subcortical mechanisms for mediating the influences of visual cues on microsaccadic eye movements |
| topic | superior colliculus frontal eye fields primary visual cortex brainstem omnipause neurons visual attention microsaccades |
| url | https://www.frontiersin.org/articles/10.3389/fncir.2021.638429/full |
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