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Motion Vision Processing in Fly Lobula Plate Tangential Cells
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Physiology.
2014 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Flies are highly visually guided animals. In this thesis, I have used hoverflies as a model for studying motion vision. Flies process motion vision in three visual ganglia: the lamina, the medulla, and the lobula complex. In the posterior part of lobula complex, there are around 60 lobula plate tangential cells (LPTCs). Most of LPTCs have large receptive fields where the local direction sensitivity suggests that they function as matched filters to specific types of optic flow. LPTCs connect to descending or neck motor neurons that control wing and head movements, respectively. Therefore, in this thesis I have focused on the electrophysiological responses of LPTCs to gain understanding of visual behaviors in flies.

The elementary motion detector (EMD) is a model that can explain the formation of local motion sensitivity. However, responses to higher order motion, where the direction of luminance change is uncorrelated with the direction of movement, cannot be predicted by classic EMDs. Nevertheless, behavior shows that flies can see and track bars with higher order motion cues. I showed (Paper I) that several LPTCs also respond to higher order motion.

Many insects, including flies, release octopamine during flight. Therefore, adding octopamine receptor agonists can mimic physical activity. Our study (Paper II) investigated the effect of octopamine on three adaptation components. We found that the contrast gain reduction showed a frequency dependent increase after octopamine stimulation. Since the contrast gain is non-directional, it is likely presynaptic to the LPTC. We therefore believe that octopamine acts on the delay filter in the EMD.

In the third paper we describe a novel LPTC. The centrifugal stationary inhibited flicker excited (cSIFE) is excited by flicker and inhibited by stationary patterns. Neither of these responses can be predicted by EMD models. Therefore, we provide a new type of motion detector that can explain cSIFE’s responses (Paper III).

During bar tracking, self-generated optic flow may counteract the steering effect by inducing a contradictory optomotor response. Behavior shows that during bar fixation, flies ignore background optic flow. Our study (Paper IV) focus on the different receptive fields of two LPTCs, and relate these to the bar fixation behavior. In the neuron with a small and fronto-dorsal receptive field, we find a higher correlation with bar motion than with background motion. In contrast, the neuron with a larger receptive field shows a higher correlation with background motion.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2014. , 47 p.
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 984
Keyword [en]
hoverflies, EMD, higher order motion, octopamine, cSIFE, figure-ground discrimination, motion vision, lobula plate tangential cells
National Category
Biological Sciences
URN: urn:nbn:se:uu:diva-220915ISBN: 978-91-554-8908-3OAI: oai:DiVA.org:uu-220915DiVA: diva2:707300
Public defence
2014-05-09, Museum Gustavianum, Uppsala, 13:15 (English)
Available from: 2014-04-17 Created: 2014-03-24 Last updated: 2014-04-29
List of papers
1. Higher-order motion sensitivity in fly visual circuits
Open this publication in new window or tab >>Higher-order motion sensitivity in fly visual circuits
2012 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 109, no 22, 8758-8763 p.Article in journal (Refereed) Published
Abstract [en]

In higher-order motion stimuli, the direction of object motion does not follow the direction of luminance change. Such stimuli could be generated by the wing movements of a flying butterfly and further complicated by its motion in and out of shadows. Human subjects readily perceive the direction of higher-order motion, although this stands in stark contrast to prevailing motion vision models. Flies and humans compute motion in similar ways, and because flies behaviorally track bars containing higher-order motion cues, they become an attractive model system for investigating the neurophysiology underlying higher-order motion sensitivity. We here use intracellular electrophysiology of motion-vision-sensitive neurons in the hoverfly lobula plate to quantify responses to stimuli containing higher-order motion. We show that motion sensitivity can be broken down into two separate streams, directionally coding for elementary motion and figure motion, respectively, and that responses to Fourier and theta motion can be predicted from these. The sensitivity is affected both by the stimulus' time course and by the neuron's underlying receptive field. Responses to preferred-direction theta motion are sexually dimorphic and particularly robust along the visual midline.

elementary motion detector, neural delays, sexual dimorphism, bar motion
National Category
Medical and Health Sciences
urn:nbn:se:uu:diva-176824 (URN)10.1073/pnas.1203081109 (DOI)000304881700079 ()
Available from: 2012-06-27 Created: 2012-06-26 Last updated: 2014-04-29Bibliographically approved
2. Octopaminergic modulation of contrast sensitivity
Open this publication in new window or tab >>Octopaminergic modulation of contrast sensitivity
2012 (English)In: Frontiers in Integrative Neuroscience, ISSN 1662-5145, Vol. 6, no Article 55Article in journal (Refereed) Published
Abstract [en]

Sensory systems adapt to prolonged stimulation by decreasing their response to continuous stimuli. Whereas visual motion adaptation has traditionally been studied in immobilized animals, recent work indicates that the animal's behavioral state influences the response properties of higher-order motion vision-sensitive neurons. During insect flight octopamine is released, and pharmacological octopaminergic activation can induce a fictive locomotor state. In the insect optic ganglia, lobula plate tangential cells (LPTCs) spatially pool input from local elementary motion detectors (EMDs) that correlate luminosity changes from two spatially discrete inputs after delaying the signal from one. The LPTC velocity optimum thereby depends on the spatial separation of the inputs and on the EMD's delay properties. Recently it was shown that behavioral activity increases the LPTC velocity optimum, with modeling suggesting this to originate in the EMD's temporal delay filters. However, behavior induces an additional post-EMD effect: the LPTC membrane conductance increases in flying flies. To physiologically investigate the degree to which activity causes presynaptic and postsynaptic effects, we conducted intracellular recordings of Eristalis horizontal system (HS) neurons. We constructed contrast response functions before and after adaptation at different temporal frequencies, with and without the octopamine receptor agonist chlordimeform (CDM). We extracted three motion adaptation components, where two are likely to be generated presynaptically of the LPTCs, and one within them. We found that CDM affected the early, EMD-associated contrast gain reduction, temporal frequency dependently. However, a CDM-induced change of the HS membrane conductance disappeared during and after visual stimulation. This suggests that physical activity mainly affects motion adaptation presynaptically of LPTCs, whereas post-EMD effects have a minimal effect.

National Category
Medical and Health Sciences
urn:nbn:se:uu:diva-181382 (URN)10.3389/fnint.2012.00055 (DOI)22876224 (PubMedID)
Available from: 2012-09-25 Created: 2012-09-24 Last updated: 2014-04-29Bibliographically approved
3. Novel Flicker-Sensitive Visual Circuit Neurons Inhibited by Stationary Patterns
Open this publication in new window or tab >>Novel Flicker-Sensitive Visual Circuit Neurons Inhibited by Stationary Patterns
2013 (English)In: Journal of Neuroscience, ISSN 0270-6474, E-ISSN 1529-2401, Vol. 33, no 21, 8980-8989 p.Article in journal (Refereed) Published
Abstract [en]

Many animals use visual motion cues for navigating within their surroundings. Both flies and vertebrates compute local motion by temporal correlation of neighboring photoreceptors, via so-called elementary motion detectors (EMDs). In the fly lobula plate and the vertebrate visual cortex the output from many EMDs is pooled in neurons sensitive to wide-field optic flow. Although the EMD has been the preferred model for more than 50 years, recent work has highlighted its limitations in describing some visual behaviors, such as responses to higher-order motion stimuli. Non-EMD motion processing may therefore serve an important function in vision. Here, we describe a novel neuron class in the fly lobula plate that clearly does not derive its input from classic EMDs. The centrifugal stationary inhibited flicker excited (cSIFE) neuron is strongly excited by flicker, up to very high temporal frequencies. The non-EMD driven flicker sensitivity leads to strong, nondirectional responses to high-speed, wide-field motion. Furthermore, cSIFE is strongly inhibited by stationary patterns, within a narrow wavelength band. cSIFE's outputs overlap with the inputs of well described optic flow-sensitive lobula plate tangential cells (LPTCs). Driving cSIFE affects the active dendrites of LPTCs, and cSIFE may therefore play a large role in motion vision.

National Category
urn:nbn:se:uu:diva-200302 (URN)10.1523/JNEUROSCI.5713-12.2013 (DOI)000319391200007 ()23699509 (PubMedID)
Swedish Research Council
Available from: 2013-05-24 Created: 2013-05-24 Last updated: 2014-04-29Bibliographically approved
4. Enhanced bar detection in hoverfly HSN responses
Open this publication in new window or tab >>Enhanced bar detection in hoverfly HSN responses
(English)Manuscript (preprint) (Other academic)
National Category
Biological Sciences
urn:nbn:se:uu:diva-220912 (URN)
Available from: 2014-03-24 Created: 2014-03-24 Last updated: 2014-04-29

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