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Ocular following responses of the marmoset monkey are dependent on postsaccadic delay, spatiotemporal frequency, and saccade direction

Ocular following is a short-latency, reflexive eye movement that tracks wide-field visual motion. It has been studied extensively in humans and macaques and is an appealing behavior for studying sensory-motor transformations in the brain because of its rapidity and rigidity. We explored ocular follo...

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Autores principales: Yip, Hoi Ming Ken, Allison-Walker, Timothy John, Cloherty, Shaun Liam, Hagan, Maureen Ann, Price, Nicholas Seow Chiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Physiological Society 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10435071/
https://www.ncbi.nlm.nih.gov/pubmed/37377195
http://dx.doi.org/10.1152/jn.00126.2023
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author Yip, Hoi Ming Ken
Allison-Walker, Timothy John
Cloherty, Shaun Liam
Hagan, Maureen Ann
Price, Nicholas Seow Chiang
author_facet Yip, Hoi Ming Ken
Allison-Walker, Timothy John
Cloherty, Shaun Liam
Hagan, Maureen Ann
Price, Nicholas Seow Chiang
author_sort Yip, Hoi Ming Ken
collection PubMed
description Ocular following is a short-latency, reflexive eye movement that tracks wide-field visual motion. It has been studied extensively in humans and macaques and is an appealing behavior for studying sensory-motor transformations in the brain because of its rapidity and rigidity. We explored ocular following in the marmoset, an emerging model in neuroscience because their lissencephalic brain allows direct access to most cortical areas for imaging and electrophysiological recordings. In three experiments, we tested ocular following responses in three adult marmosets. First, we varied the delay between saccade end and stimulus motion onset, from 10 to 300 ms. As in other species, tracking had shorter onset latencies and higher eye speeds with shorter postsaccadic delays. Second, using sine-wave grating stimuli, we explored the dependence of eye speed on spatiotemporal frequency. The highest eye speed was evoked at ∼16 Hz and ∼0.16 cycles per degree (cpd); however, the highest gain was elicited at ∼1.6 Hz and ∼1.2 cpd. The highest eye speed for each spatial frequency was observed at a different temporal frequency, but this interdependence was not consistent with complete speed tuning of the ocular following response. Finally, we found the highest eye speeds when saccade and stimulus motion directions were identical, although latencies were unaffected by direction difference. Our results showed qualitatively similar ocular following in marmosets, humans, and macaques, despite over an order of magnitude variation in body and eye size across species. This characterization will help future studies examining the neural basis of sensory-motor transformations. NEW & NOTEWORTHY Previous ocular following studies focused on humans and macaques. We examined the properties of ocular following responses in marmosets in three experiments, in which postsaccadic delay, spatial-temporal frequency of stimuli, and congruence of saccade and motion directions were manipulated. We have demonstrated short-latency ocular following in marmosets and discuss the similarities across three species that vary markedly in eye and head size. Our findings will help future studies examining the neural mechanism of sensory-motor transformations.
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spelling pubmed-104350712023-08-18 Ocular following responses of the marmoset monkey are dependent on postsaccadic delay, spatiotemporal frequency, and saccade direction Yip, Hoi Ming Ken Allison-Walker, Timothy John Cloherty, Shaun Liam Hagan, Maureen Ann Price, Nicholas Seow Chiang J Neurophysiol Research Article Ocular following is a short-latency, reflexive eye movement that tracks wide-field visual motion. It has been studied extensively in humans and macaques and is an appealing behavior for studying sensory-motor transformations in the brain because of its rapidity and rigidity. We explored ocular following in the marmoset, an emerging model in neuroscience because their lissencephalic brain allows direct access to most cortical areas for imaging and electrophysiological recordings. In three experiments, we tested ocular following responses in three adult marmosets. First, we varied the delay between saccade end and stimulus motion onset, from 10 to 300 ms. As in other species, tracking had shorter onset latencies and higher eye speeds with shorter postsaccadic delays. Second, using sine-wave grating stimuli, we explored the dependence of eye speed on spatiotemporal frequency. The highest eye speed was evoked at ∼16 Hz and ∼0.16 cycles per degree (cpd); however, the highest gain was elicited at ∼1.6 Hz and ∼1.2 cpd. The highest eye speed for each spatial frequency was observed at a different temporal frequency, but this interdependence was not consistent with complete speed tuning of the ocular following response. Finally, we found the highest eye speeds when saccade and stimulus motion directions were identical, although latencies were unaffected by direction difference. Our results showed qualitatively similar ocular following in marmosets, humans, and macaques, despite over an order of magnitude variation in body and eye size across species. This characterization will help future studies examining the neural basis of sensory-motor transformations. NEW & NOTEWORTHY Previous ocular following studies focused on humans and macaques. We examined the properties of ocular following responses in marmosets in three experiments, in which postsaccadic delay, spatial-temporal frequency of stimuli, and congruence of saccade and motion directions were manipulated. We have demonstrated short-latency ocular following in marmosets and discuss the similarities across three species that vary markedly in eye and head size. Our findings will help future studies examining the neural mechanism of sensory-motor transformations. American Physiological Society 2023-07-01 2023-06-28 /pmc/articles/PMC10435071/ /pubmed/37377195 http://dx.doi.org/10.1152/jn.00126.2023 Text en Copyright © 2023 The Authors. https://creativecommons.org/licenses/by/4.0/Licensed under Creative Commons Attribution CC-BY 4.0 (https://creativecommons.org/licenses/by/4.0/) . Published by the American Physiological Society.
spellingShingle Research Article
Yip, Hoi Ming Ken
Allison-Walker, Timothy John
Cloherty, Shaun Liam
Hagan, Maureen Ann
Price, Nicholas Seow Chiang
Ocular following responses of the marmoset monkey are dependent on postsaccadic delay, spatiotemporal frequency, and saccade direction
title Ocular following responses of the marmoset monkey are dependent on postsaccadic delay, spatiotemporal frequency, and saccade direction
title_full Ocular following responses of the marmoset monkey are dependent on postsaccadic delay, spatiotemporal frequency, and saccade direction
title_fullStr Ocular following responses of the marmoset monkey are dependent on postsaccadic delay, spatiotemporal frequency, and saccade direction
title_full_unstemmed Ocular following responses of the marmoset monkey are dependent on postsaccadic delay, spatiotemporal frequency, and saccade direction
title_short Ocular following responses of the marmoset monkey are dependent on postsaccadic delay, spatiotemporal frequency, and saccade direction
title_sort ocular following responses of the marmoset monkey are dependent on postsaccadic delay, spatiotemporal frequency, and saccade direction
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10435071/
https://www.ncbi.nlm.nih.gov/pubmed/37377195
http://dx.doi.org/10.1152/jn.00126.2023
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