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A Microsaccadic Account of Attentional Capture and Inhibition of Return in Posner Cueing

Microsaccades exhibit systematic oscillations in direction after spatial cueing, and these oscillations correlate with facilitatory and inhibitory changes in behavioral performance in the same tasks. However, independent of cueing, facilitatory and inhibitory changes in visual sensitivity also arise...

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Autores principales: Tian, Xiaoguang, Yoshida, Masatoshi, Hafed, Ziad M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4779940/
https://www.ncbi.nlm.nih.gov/pubmed/27013991
http://dx.doi.org/10.3389/fnsys.2016.00023
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author Tian, Xiaoguang
Yoshida, Masatoshi
Hafed, Ziad M.
author_facet Tian, Xiaoguang
Yoshida, Masatoshi
Hafed, Ziad M.
author_sort Tian, Xiaoguang
collection PubMed
description Microsaccades exhibit systematic oscillations in direction after spatial cueing, and these oscillations correlate with facilitatory and inhibitory changes in behavioral performance in the same tasks. However, independent of cueing, facilitatory and inhibitory changes in visual sensitivity also arise pre-microsaccadically. Given such pre-microsaccadic modulation, an imperative question to ask becomes: how much of task performance in spatial cueing may be attributable to these peri-movement changes in visual sensitivity? To investigate this question, we adopted a theoretical approach. We developed a minimalist model in which: (1) microsaccades are repetitively generated using a rise-to-threshold mechanism, and (2) pre-microsaccadic target onset is associated with direction-dependent modulation of visual sensitivity, as found experimentally. We asked whether such a model alone is sufficient to account for performance dynamics in spatial cueing. Our model not only explained fine-scale microsaccade frequency and direction modulations after spatial cueing, but it also generated classic facilitatory (i.e., attentional capture) and inhibitory [i.e., inhibition of return (IOR)] effects of the cue on behavioral performance. According to the model, cues reflexively reset the oculomotor system, which unmasks oscillatory processes underlying microsaccade generation; once these oscillatory processes are unmasked, “attentional capture” and “IOR” become direct outcomes of pre-microsaccadic enhancement or suppression, respectively. Interestingly, our model predicted that facilitatory and inhibitory effects on behavior should appear as a function of target onset relative to microsaccades even without prior cues. We experimentally validated this prediction for both saccadic and manual responses. We also established a potential causal mechanism for the microsaccadic oscillatory processes hypothesized by our model. We used retinal-image stabilization to experimentally control instantaneous foveal motor error during the presentation of peripheral cues, and we found that post-cue microsaccadic oscillations were severely disrupted. This suggests that microsaccades in spatial cueing tasks reflect active oculomotor correction of foveal motor error, rather than presumed oscillatory covert attentional processes. Taken together, our results demonstrate that peri-microsaccadic changes in vision can go a long way in accounting for some classic behavioral phenomena.
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spelling pubmed-47799402016-03-24 A Microsaccadic Account of Attentional Capture and Inhibition of Return in Posner Cueing Tian, Xiaoguang Yoshida, Masatoshi Hafed, Ziad M. Front Syst Neurosci Neuroscience Microsaccades exhibit systematic oscillations in direction after spatial cueing, and these oscillations correlate with facilitatory and inhibitory changes in behavioral performance in the same tasks. However, independent of cueing, facilitatory and inhibitory changes in visual sensitivity also arise pre-microsaccadically. Given such pre-microsaccadic modulation, an imperative question to ask becomes: how much of task performance in spatial cueing may be attributable to these peri-movement changes in visual sensitivity? To investigate this question, we adopted a theoretical approach. We developed a minimalist model in which: (1) microsaccades are repetitively generated using a rise-to-threshold mechanism, and (2) pre-microsaccadic target onset is associated with direction-dependent modulation of visual sensitivity, as found experimentally. We asked whether such a model alone is sufficient to account for performance dynamics in spatial cueing. Our model not only explained fine-scale microsaccade frequency and direction modulations after spatial cueing, but it also generated classic facilitatory (i.e., attentional capture) and inhibitory [i.e., inhibition of return (IOR)] effects of the cue on behavioral performance. According to the model, cues reflexively reset the oculomotor system, which unmasks oscillatory processes underlying microsaccade generation; once these oscillatory processes are unmasked, “attentional capture” and “IOR” become direct outcomes of pre-microsaccadic enhancement or suppression, respectively. Interestingly, our model predicted that facilitatory and inhibitory effects on behavior should appear as a function of target onset relative to microsaccades even without prior cues. We experimentally validated this prediction for both saccadic and manual responses. We also established a potential causal mechanism for the microsaccadic oscillatory processes hypothesized by our model. We used retinal-image stabilization to experimentally control instantaneous foveal motor error during the presentation of peripheral cues, and we found that post-cue microsaccadic oscillations were severely disrupted. This suggests that microsaccades in spatial cueing tasks reflect active oculomotor correction of foveal motor error, rather than presumed oscillatory covert attentional processes. Taken together, our results demonstrate that peri-microsaccadic changes in vision can go a long way in accounting for some classic behavioral phenomena. Frontiers Media S.A. 2016-03-07 /pmc/articles/PMC4779940/ /pubmed/27013991 http://dx.doi.org/10.3389/fnsys.2016.00023 Text en Copyright © 2016 Tian, Yoshida and Hafed. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Tian, Xiaoguang
Yoshida, Masatoshi
Hafed, Ziad M.
A Microsaccadic Account of Attentional Capture and Inhibition of Return in Posner Cueing
title A Microsaccadic Account of Attentional Capture and Inhibition of Return in Posner Cueing
title_full A Microsaccadic Account of Attentional Capture and Inhibition of Return in Posner Cueing
title_fullStr A Microsaccadic Account of Attentional Capture and Inhibition of Return in Posner Cueing
title_full_unstemmed A Microsaccadic Account of Attentional Capture and Inhibition of Return in Posner Cueing
title_short A Microsaccadic Account of Attentional Capture and Inhibition of Return in Posner Cueing
title_sort microsaccadic account of attentional capture and inhibition of return in posner cueing
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4779940/
https://www.ncbi.nlm.nih.gov/pubmed/27013991
http://dx.doi.org/10.3389/fnsys.2016.00023
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