A visual pathway for skylight polarization processing in Drosophila

Hardcastle, Ben J.; Omoto, Jaison J.; Kandimalla, Pratyush; Nguyen, Bao; Keleş, Mehmet F.; Boyd, Natalie K.; Hartenstein, Volker; Frye, Mark A.

doi:10.7554/elife.63225

Cited by 80 publications

(155 citation statements)

References 120 publications

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“…The LX consists of two distinct areas, the bulbs (BUs) and the LAL (Ito et al, 2014). The BUs are clusters of microglomerular complexes that relay spatial visual information from the lower unit of the anterior optic tubercle to the CBL (Hardcastle et al, 2021; Held et al, 2016; Mota et al, 2016; Omoto et al, 2017; Seelig & Jayaraman, 2013, 2015; Shiozaki & Kazama, 2017; Träger et al, 2008). The LAL mediates various other sensory input, such as optic flow information toward the noduli (Stone et al, 2017), wind direction signals to the central body (Currier et al, 2020; Okubo et al, 2020), and self‐generated proprioceptive information to the central body (Homberg, 1994; Hulse et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Organization and neural connections of the lateral complex in the brain of the desert locust

Hensgen

Göthe

Jahn

et al. 2021

J of Comparative Neurology

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The lateral complexes (LXs) are bilaterally paired neuropils in the insect brain that mediate communication between the central complex (CX), a brain center controlling spatial orientation, various sensory processing areas, and thoracic motor centers that execute locomotion. The LX of the desert locust consists of the lateral accessory lobe (LAL), and the medial and lateral bulb. We have analyzed the anatomical organization and the neuronal connections of the LX in the locust, to provide a basis for future functional studies. Reanalyzing the morphology of neurons connecting the CX and the LX revealed likely feedback loops in the sky compass network of the CX via connections in the gall of the LAL and a newly identified neuropil termed ovoid body. In addition, we characterized 16 different types of neuron that connect the LAL with other areas in the brain. Eight types of neuron provide information flow between both LALs, five types are LAL input neurons, and three types are LAL output neurons. Among these are neurons providing input from sensory brain areas such as the lobula and antennal neuropils. Brain regions most often targeted by LAL neurons are the posterior slope, the wedge, and the crepine. Two descending neurons with dendrites in the LAL were identified. Our data support and complement existing knowledge about how the LAL is embedded in the neuronal network involved in processing of sensory information and generation of appropriate behavioral output for goal‐directed locomotion.

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Section: Discussionmentioning

confidence: 99%

Organization and neural connections of the lateral complex in the brain of the desert locust

Hensgen

Göthe

Jahn

et al. 2021

J of Comparative Neurology

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“…Within the E-PG network, heading is represented by a single activity bump that changes its position when the insect changes its heading direction 13,16 . The activity bump in E-PG cells results from the integration of visual signals and mechanosensory information 14,[17][18][19] , as well as idiothetic, self-motion signals 13,20,21 .…”

Section: Introductionmentioning

confidence: 99%

Flight-induced compass representation in the monarch butterfly heading network

Beetz

Kraus

Franzke

et al. 2021

Preprint

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Head direction can be represented in a self-centered egocentric or a viewpoint-invariant allocentric reference frame. Using the most efficient representation is especially crucial for migrating animals, like monarch butterflies (Danaus plexippus) that use the sun for orientation. With tetrode recordings from the brain of tethered flying monarch butterflies, we examined the reference frame in which insects encode heading. We show that compass neurons switch their reference frame in a state-dependent manner. In quiescence, they encode sun-bearing angles, allowing the butterfly to map the environment within an egocentric frame. However, during flight, the same neurons encode heading within an allocentric frame. This switch converts the sun from a local to a global cue, an ideal strategy for maintaining a migratory heading over large distance.

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“…In the DRA, the inner photoreceptors express the same UV rhodopsin (Rh3; Fortini and Rubin 1991, 1990) and detect perpendicular angles of polarized UV light (Weir et al 2016). In contrast to the rest of the medulla, R7-DRA and R8-DRA project to the same medulla layer (M6; Chin et al 2014; Pollack and Hofbauer 1991; Fischbach and Dittrich 1989), where their targets include polarization-specific cell types (Sancer et al 2019, 2020; Hardcastle et al 2021). Across insects, a ‘compass pathway’ connects the DRA to the central brain via the anterior optic tubercle (AOTU; Homberg 2015; Hardcastle et al 2021; Pfeiffer and Kinoshita 2012).…”

Section: Introductionmentioning

confidence: 99%

“…In contrast to the rest of the medulla, R7-DRA and R8-DRA project to the same medulla layer (M6; Chin et al 2014; Pollack and Hofbauer 1991; Fischbach and Dittrich 1989), where their targets include polarization-specific cell types (Sancer et al 2019, 2020; Hardcastle et al 2021). Across insects, a ‘compass pathway’ connects the DRA to the central brain via the anterior optic tubercle (AOTU; Homberg 2015; Hardcastle et al 2021; Pfeiffer and Kinoshita 2012). Anatomical and functional data from Drosophila suggests that the central medulla is also connected to the compass pathway (Omoto et al 2017; Hardcastle et al 2021; Otsuna et al 2014), potentially forming parallel pathways for processing different celestial cues (Timaeus et al 2020; Tai et al 2021).…”

Section: Introductionmentioning

confidence: 99%

“…Across insects, a ‘compass pathway’ connects the DRA to the central brain via the anterior optic tubercle (AOTU; Homberg 2015; Hardcastle et al 2021; Pfeiffer and Kinoshita 2012). Anatomical and functional data from Drosophila suggests that the central medulla is also connected to the compass pathway (Omoto et al 2017; Hardcastle et al 2021; Otsuna et al 2014), potentially forming parallel pathways for processing different celestial cues (Timaeus et al 2020; Tai et al 2021).…”

Section: Introductionmentioning

confidence: 99%

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Synaptic targets of photoreceptors specialized to detect color and skylight polarization in Drosophila

Kind

Longden

Nern

et al. 2021

Preprint

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Color and polarization provide complementary information about the world and are detected by specialized photoreceptors. However, the downstream neural circuits that process these distinct modalities are incompletely understood in any animal. We have systematically reconstructed, using light and electron microscopy, the synaptic targets of the photoreceptors specialized to detect color and polarized light in Drosophila. We identified known and novel downstream targets that are selective for different wavelengths as well as for polarized light and followed their projections to other areas in the optic lobes and the central brain. Strikingly, photoreceptors in the polarization-sensitive dorsal rim area target fewer cell types, that lack strong connections to the lobula, a neuropil with a proposed role in color processing. Our reconstruction identifies shared wiring and modality-specific specializations for color and polarization vision, and provides a comprehensive view of the first steps of the pathways processing color and polarized light inputs.

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A visual pathway for skylight polarization processing in Drosophila

Cited by 80 publications

References 120 publications

Organization and neural connections of the lateral complex in the brain of the desert locust

Organization and neural connections of the lateral complex in the brain of the desert locust

Flight-induced compass representation in the monarch butterfly heading network

Synaptic targets of photoreceptors specialized to detect color and skylight polarization in Drosophila

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