Anthony B Lapsansky, Philipp Kreyenmeier, Miriam Spering, Douglas R Wylie, Douglas L Altshuler
{"title":"蜂鸟使用补偿性眼球运动来稳定旋转和平移的视觉运动。","authors":"Anthony B Lapsansky, Philipp Kreyenmeier, Miriam Spering, Douglas R Wylie, Douglas L Altshuler","doi":"10.1098/rspb.2024.2015","DOIUrl":null,"url":null,"abstract":"<p><p>To maintain stable vision, behaving animals make compensatory eye movements in response to image slip, a reflex known as the optokinetic response (OKR). Although OKR has been studied in several avian species, eye movements during flight are expected to be minimal. This is because vertebrates with laterally placed eyes typically show weak OKR to nasal-to-temporal motion (NT), which simulates typical forward locomotion, compared with temporal-to-nasal motion (TN), which simulates atypical backward locomotion. This OKR asymmetry is also reflected in the pretectum, wherein neurons sensitive to global visual motion also exhibit a TN bias. Hummingbirds, however, stabilize visual motion in all directions through whole-body movements and are unique among vertebrates in that they lack a pretectal bias. We therefore predicted that OKR in hummingbirds would be symmetrical. We measured OKR in restrained hummingbirds by presenting gratings drifting across a range of speeds. OKR in hummingbirds was asymmetrical, although the direction of asymmetry varied with stimulus speed. Hummingbirds moved their eyes largely independently of one another. Consistent with weak eye-to-eye coupling, hummingbirds also exhibited disjunctive OKR to visual motion simulating forward and backward translation. This unexpected oculomotor behaviour, previously unexplored in birds, suggests a potential role for compensatory eye movements during flight.</p>","PeriodicalId":20589,"journal":{"name":"Proceedings of the Royal Society B: Biological Sciences","volume":"292 2038","pages":"20242015"},"PeriodicalIF":3.8000,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11732407/pdf/","citationCount":"0","resultStr":"{\"title\":\"Hummingbirds use compensatory eye movements to stabilize both rotational and translational visual motion.\",\"authors\":\"Anthony B Lapsansky, Philipp Kreyenmeier, Miriam Spering, Douglas R Wylie, Douglas L Altshuler\",\"doi\":\"10.1098/rspb.2024.2015\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>To maintain stable vision, behaving animals make compensatory eye movements in response to image slip, a reflex known as the optokinetic response (OKR). Although OKR has been studied in several avian species, eye movements during flight are expected to be minimal. This is because vertebrates with laterally placed eyes typically show weak OKR to nasal-to-temporal motion (NT), which simulates typical forward locomotion, compared with temporal-to-nasal motion (TN), which simulates atypical backward locomotion. This OKR asymmetry is also reflected in the pretectum, wherein neurons sensitive to global visual motion also exhibit a TN bias. Hummingbirds, however, stabilize visual motion in all directions through whole-body movements and are unique among vertebrates in that they lack a pretectal bias. We therefore predicted that OKR in hummingbirds would be symmetrical. We measured OKR in restrained hummingbirds by presenting gratings drifting across a range of speeds. OKR in hummingbirds was asymmetrical, although the direction of asymmetry varied with stimulus speed. Hummingbirds moved their eyes largely independently of one another. Consistent with weak eye-to-eye coupling, hummingbirds also exhibited disjunctive OKR to visual motion simulating forward and backward translation. This unexpected oculomotor behaviour, previously unexplored in birds, suggests a potential role for compensatory eye movements during flight.</p>\",\"PeriodicalId\":20589,\"journal\":{\"name\":\"Proceedings of the Royal Society B: Biological Sciences\",\"volume\":\"292 2038\",\"pages\":\"20242015\"},\"PeriodicalIF\":3.8000,\"publicationDate\":\"2025-01-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11732407/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Proceedings of the Royal Society B: Biological Sciences\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1098/rspb.2024.2015\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2025/1/15 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q1\",\"JCRName\":\"BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Proceedings of the Royal Society B: Biological Sciences","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1098/rspb.2024.2015","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/1/15 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"BIOLOGY","Score":null,"Total":0}
Hummingbirds use compensatory eye movements to stabilize both rotational and translational visual motion.
To maintain stable vision, behaving animals make compensatory eye movements in response to image slip, a reflex known as the optokinetic response (OKR). Although OKR has been studied in several avian species, eye movements during flight are expected to be minimal. This is because vertebrates with laterally placed eyes typically show weak OKR to nasal-to-temporal motion (NT), which simulates typical forward locomotion, compared with temporal-to-nasal motion (TN), which simulates atypical backward locomotion. This OKR asymmetry is also reflected in the pretectum, wherein neurons sensitive to global visual motion also exhibit a TN bias. Hummingbirds, however, stabilize visual motion in all directions through whole-body movements and are unique among vertebrates in that they lack a pretectal bias. We therefore predicted that OKR in hummingbirds would be symmetrical. We measured OKR in restrained hummingbirds by presenting gratings drifting across a range of speeds. OKR in hummingbirds was asymmetrical, although the direction of asymmetry varied with stimulus speed. Hummingbirds moved their eyes largely independently of one another. Consistent with weak eye-to-eye coupling, hummingbirds also exhibited disjunctive OKR to visual motion simulating forward and backward translation. This unexpected oculomotor behaviour, previously unexplored in birds, suggests a potential role for compensatory eye movements during flight.
期刊介绍:
Proceedings B is the Royal Society’s flagship biological research journal, accepting original articles and reviews of outstanding scientific importance and broad general interest. The main criteria for acceptance are that a study is novel, and has general significance to biologists. Articles published cover a wide range of areas within the biological sciences, many have relevance to organisms and the environments in which they live. The scope includes, but is not limited to, ecology, evolution, behavior, health and disease epidemiology, neuroscience and cognition, behavioral genetics, development, biomechanics, paleontology, comparative biology, molecular ecology and evolution, and global change biology.