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Neurons against Noise : Neural adaptations for dim light vision in hawkmoths

Stöckl, Anna LU (2016)
Abstract
All animals perceive the world through their senses, which form the basis for their decisions and motor actions. However, when these all-important senses reach their limit and cease to provide reliable information, the animal’s survival is threatened. Among the senses, vision is brought to its limits on a daily basis, because its signal strength is diminished as night falls, and increases again as the sun rises. In this thesis, I investigated adaptations that enable the visual system of hawkmoths, a group of insects, to cope with the low light intensities they face at night. I have focused on neural adaptations, manifested in the processing of visual neurons, in contrast to anatomical adaptations, such as modifications of the eye. I showed... (More)
All animals perceive the world through their senses, which form the basis for their decisions and motor actions. However, when these all-important senses reach their limit and cease to provide reliable information, the animal’s survival is threatened. Among the senses, vision is brought to its limits on a daily basis, because its signal strength is diminished as night falls, and increases again as the sun rises. In this thesis, I investigated adaptations that enable the visual system of hawkmoths, a group of insects, to cope with the low light intensities they face at night. I have focused on neural adaptations, manifested in the processing of visual neurons, in contrast to anatomical adaptations, such as modifications of the eye. I showed that neural adaptations exist in the motion vision system of hawkmoths, in the form of integration of visual information in space and time. Furthermore, I demonstrated that a combination of such spatial and temporal summation increased sensitivity and information content in dim light (Paper I). The amount of spatial and temporal summation matched the ecological needs of different hawkmoth species, as well as their anatomical adaptations for visual sensitivity: night active species, and species with less sensitive eyes had more extensive spatial and temporal summation than day-active species and species with very sensitive optics (Paper II). Furthermore, I identified and characterised candidate neurons that carry out spatial and temporal summation in the brain of hawkmoths (Paper III). Finally, I quantified the effects of temporal summation on the ability of hawkmoths to track flowers in hovering flight at different light levels, and showed that a subset of the observed behavioural phenomena could be explained by temporal processing in the nervous system (Paper IV). Taken together, this work has provided detailed insight into how neural processing can increase visual reliability in dim light. The results presented are not only relevant to hawkmoths, since neural summation is also expected to increase visual sensitivity in other species of nocturnal insects, and can be compared to similar mechanisms in vertebrates. Furthermore, this work is instructive for the development of artificial visual systems, for which insect brains have proven to be a successful biomimetic model. (Less)
Abstract (Swedish)
Alla djur uppfattar världen med sina sinnen, vilka ger information till beslut och rörelser. Tyvärr har sinnena begränsningar och när de upphör att ge pålitlig information kommer djurets överlevnad att hotas. Synsinnet till exempel utmanas dagligen, eftersom dess signalstyrka minskar när mörkret faller och ökar igen när solen går upp. I denna avhandling undersökte jag synsystemets anpassningar hos svärmare, en grupp insekter som klarar av mycket låga ljusintensiteter under natten. Jag fokuserade mina studier på neurala anpassningar som yttrar sig i informationsbearbetning hos synneuroner, i motsats till anatomiska anpassningar, såsom modifikationer i ögat. Jag kunde visa att neurala anpassningar förekommer i synsystemet hos svärmare i form... (More)
Alla djur uppfattar världen med sina sinnen, vilka ger information till beslut och rörelser. Tyvärr har sinnena begränsningar och när de upphör att ge pålitlig information kommer djurets överlevnad att hotas. Synsinnet till exempel utmanas dagligen, eftersom dess signalstyrka minskar när mörkret faller och ökar igen när solen går upp. I denna avhandling undersökte jag synsystemets anpassningar hos svärmare, en grupp insekter som klarar av mycket låga ljusintensiteter under natten. Jag fokuserade mina studier på neurala anpassningar som yttrar sig i informationsbearbetning hos synneuroner, i motsats till anatomiska anpassningar, såsom modifikationer i ögat. Jag kunde visa att neurala anpassningar förekommer i synsystemet hos svärmare i form av integrering av visuell information i tid och rum. Dessutom visade jag att en kombination av spatial och temporal summering ökar ljuskänsligheten och informationsinnehållet på ett supralinjärt sätt (Publikation I). Mängden spatial och temporal summering matchade de ekologiska behov som olika arter av svärmare har, samt deras anatomiska anpassningar för synkänslighet (Publikation II). Jag identifierade också nervceller som utför spatial och temporal summering i hjärnan hos svärmare (Publikation III). Slutligen kvantifierade jag effekterna som temporal summering har på svärmares förmåga att spåra blommor i rörelse och visade att en del av det observerade beteendet kan förklaras med temporal bearbetning i nervsystemet (Publikation IV). Sammanfattningsvis ger detta arbete en detaljerad inblick i hur neural summering kan öka ljuskänsligheten i svagt ljus. Dessa resultat är inte bara relevanta för svärmare, utan även för andra insekter och djurgrupper. Dessutom är detta arbete lärorikt för utvecklingen av artificiella synsystem, som insekters syn visat sig vara en framgångsrik biomimetisk modell för. (Less)
Please use this url to cite or link to this publication:
author
supervisor
opponent
  • Professor Laughlin, Simon, University of Cambridge, United Kingdom
organization
publishing date
type
Thesis
publication status
published
subject
keywords
vision, insect, hawkmoth, motion vision, spatial and temporal summation, dim light, neural processing
pages
94 pages
publisher
Lund University, Faculty of Science, Department of Biology
defense location
The Ecology building, lecture hall “Blå Hallen”, Sölvegatan 37, Lund
defense date
2016-12-02 10:00:00
ISBN
978-91-7753-065-7
978-91-7753-064-0
language
English
LU publication?
yes
id
5ab665dc-7981-4db5-8a51-f0dbcebc6352
date added to LUP
2016-11-07 18:21:34
date last changed
2020-10-13 13:46:54
@phdthesis{5ab665dc-7981-4db5-8a51-f0dbcebc6352,
  abstract     = {{All animals perceive the world through their senses, which form the basis for their decisions and motor actions. However, when these all-important senses reach their limit and cease to provide reliable information, the animal’s survival is threatened. Among the senses, vision is brought to its limits on a daily basis, because its signal strength is diminished as night falls, and increases again as the sun rises. In this thesis, I investigated adaptations that enable the visual system of hawkmoths, a group of insects, to cope with the low light intensities they face at night. I have focused on neural adaptations, manifested in the processing of visual neurons, in contrast to anatomical adaptations, such as modifications of the eye. I showed that neural adaptations exist in the motion vision system of hawkmoths, in the form of integration of visual information in space and time. Furthermore, I demonstrated that a combination of such spatial and temporal summation increased sensitivity and information content in dim light (Paper I). The amount of spatial and temporal summation matched the ecological needs of different hawkmoth species, as well as their anatomical adaptations for visual sensitivity: night active species, and species with less sensitive eyes had more extensive spatial and temporal summation than day-active species and species with very sensitive optics (Paper II). Furthermore, I identified and characterised candidate neurons that carry out spatial and temporal summation in the brain of hawkmoths (Paper III). Finally, I quantified the effects of temporal summation on the ability of hawkmoths to track flowers in hovering flight at different light levels, and showed that a subset of the observed behavioural phenomena could be explained by temporal processing in the nervous system (Paper IV). Taken together, this work has provided detailed insight into how neural processing can increase visual reliability in dim light. The results presented are not only relevant to hawkmoths, since neural summation is also expected to increase visual sensitivity in other species of nocturnal insects, and can be compared to similar mechanisms in vertebrates. Furthermore, this work is instructive for the development of artificial visual systems, for which insect brains have proven to be a successful biomimetic model.}},
  author       = {{Stöckl, Anna}},
  isbn         = {{978-91-7753-065-7}},
  keywords     = {{vision; insect; hawkmoth; motion vision; spatial and temporal summation; dim light; neural processing}},
  language     = {{eng}},
  publisher    = {{Lund University, Faculty of Science, Department of Biology}},
  school       = {{Lund University}},
  title        = {{Neurons against Noise : Neural adaptations for dim light vision in hawkmoths}},
  url          = {{https://lup.lub.lu.se/search/files/16645681/FinalThesis_AnnaStoeckl_kappa.pdf}},
  year         = {{2016}},
}