From Photons to Behaviors: Neural Implementations of Visual Behaviors in Drosophila

Ryu, Leesun; Kim, Sung Yong; Kim, Anmo J.

doi:10.3389/fnins.2022.883640

Cited by 12 publications

(6 citation statements)

References 163 publications

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“…Thus, these neurons share physiological properties with lobula plate tangential cells in flies. Lobula plate tangential cells have central brain ramifications in the PS and PLP but not in the VLP (Ito et al., 2014; Namiki, Wada, et al., 2018; Ryu et al., 2022). As shown here, this also holds for the investigated widefield sensitive cells in the mantis (TADpro, TApro dist 1, and TAcen).…”

Section: Discussionmentioning

confidence: 99%

“…In the mantis, a subdivision, like in the cockroach, dung beetles, and locust (Althaus et al., 2022; Immonen et al., 2017; von Hadeln et al., 2018), was not obvious. The PS is a major target of motion‐sensitive projection neurons from the ME and LOX signaling ego motion (Namiki, Dickinson, et al., 2018; Paulk et al., 2008, 2009; Ryu et al., 2022; Strausfeld, 1976; Strausfeld & Bassemir, 1985a, 1985b; Suver et al., 2016) and is innervated by numerous descending and ascending neurons (Okada et al., 2003; Ryu et al., 2022; Staudacher, 1998; Staudacher et al., 2023; Strausfeld, 1976). In addition, the PS receives input from numerous brain areas including the LAL, as reported in the silk moth ( Bombyx mori ), where these neurons seem to be involved in motor control for pheromone processing (Namiki, Wada, et al., 2018).…”

Section: Discussionmentioning

confidence: 99%

“…The fly LOX comprises two nested neuropils, the lobula plate and the lobula. Widefield motion is processed in a directionally selective manner in the lobula plate, while in the lobula, several types of projection neurons respond to motion of small, dark targets (Klapoetke et al, 2022;Ryu et al, 2022). In the mantis, widefield motion is processed in a directionally selective manner by neurons ramifying in distal layers of the ALO (TADpro, TApro dist 1, and TAcen in Rosner et al [2019Rosner et al [ , 2020; TAproM1 and TAproM2 in Yamawaki [2019]) and, additionally, by neurons with input exclusively in the dorsal lobe of the LOX (Yamawaki, 2019).…”

Section: Insights From Ramification Sites Of Optic Lobe Neuronsmentioning

confidence: 99%

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Anatomical organization of the cerebrum of the praying mantis Hierodula membranacea

Althaus,

Exner,

von Hadeln

et al. 2024

J of Comparative Neurology

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Many predatory animals, such as the praying mantis, use vision for prey detection and capture. Mantises are known in particular for their capability to estimate distances to prey by stereoscopic vision. While the initial visual processing centers have been extensively documented, we lack knowledge on the architecture of central brain regions, pivotal for sensory motor transformation and higher brain functions. To close this gap, we provide a three‐dimensional (3D) reconstruction of the central brain of the Asian mantis, Hierodula membranacea. The atlas facilitates in‐depth analysis of neuron ramification regions and aides in elucidating potential neuronal pathways. We integrated seven 3D‐reconstructed visual interneurons into the atlas. In total, 42 distinct neuropils of the cerebrum were reconstructed based on synapsin‐immunolabeled whole‐mount brains. Backfills from the antenna and maxillary palps, as well as immunolabeling of γ‐aminobutyric acid (GABA) and tyrosine hydroxylase (TH), further substantiate the identification and boundaries of brain areas. The composition and internal organization of the neuropils were compared to the anatomical organization of the brain of the fruit fly (Drosophila melanogaster) and the two available brain atlases of Polyneoptera—the desert locust (Schistocerca gregaria) and the Madeira cockroach (Rhyparobia maderae). This study paves the way for detailed analyses of neuronal circuitry and promotes cross‐species brain comparisons. We discuss differences in brain organization between holometabolous and polyneopteran insects. Identification of ramification sites of the visual neurons integrated into the atlas supports previous claims about homologous structures in the optic lobes of flies and mantises.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Insights From Ramification Sites Of Optic Lobe Neuronsmentioning

confidence: 99%

See 1 more Smart Citation

Anatomical organization of the cerebrum of the praying mantis Hierodula membranacea

Althaus,

Exner,

von Hadeln

et al. 2024

J of Comparative Neurology

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“…These circuit differences reflect different sensory ecologies between insect species. It also emphasizes the general importance of comparative studies on multimodal information processing (Thiagarajan and Sachse 2022 ) and the role of differences in visual pathways on visual behaviors (Ryu et al 2022 ).…”

Section: Connections Between the Mb And CX Pathwaysmentioning

confidence: 99%

The role of learning-walk related multisensory experience in rewiring visual circuits in the desert ant brain

2022

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Efficient spatial orientation in the natural environment is crucial for the survival of most animal species. Cataglyphis desert ants possess excellent navigational skills. After far-ranging foraging excursions, the ants return to their inconspicuous nest entrance using celestial and panoramic cues. This review focuses on the question about how naïve ants acquire the necessary spatial information and adjust their visual compass systems. Naïve ants perform structured learning walks during their transition from the dark nest interior to foraging under bright sunlight. During initial learning walks, the ants perform rotational movements with nest-directed views using the earth’s magnetic field as an earthbound compass reference. Experimental manipulations demonstrate that specific sky compass cues trigger structural neuronal plasticity in visual circuits to integration centers in the central complex and mushroom bodies. During learning walks, rotation of the sky-polarization pattern is required for an increase in volume and synaptic complexes in both integration centers. In contrast, passive light exposure triggers light-spectrum (especially UV light) dependent changes in synaptic complexes upstream of the central complex. We discuss a multisensory circuit model in the ant brain for pathways mediating structural neuroplasticity at different levels following passive light exposure and multisensory experience during the performance of learning walks.

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“…Fruit flies demonstrate impressive agility in flight (Card and Dickinson, 2008 ;Fry et al, 2005 ;Liu et al, 2019 ;Muijres et al, 2014 ), and vision plays a pivotal role in the flight control, often translating directly into precise flight maneuvers. Neural circuit mechanisms underlying many of these visuomotor behaviors have been studied intensively in recent years, both structurally and functionally (Fenk et al, 2022 ;Joesch, 2009 ;Joesch et al, 2010 ;Takemura et al, 2013 ;Wu et al, 2016 ) (see (Currier et al, 2023 ;Ryu et al, 2022 ) for reviews). While we have gained a qualitative grasp of the neural substrates underlying various visual behaviors, a quantitative understanding remains less explored (Ache et al, 2019 ;Maisak et al, 2013 ;Mauss et al, 2015 ;Städele et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

A visual efference copy-based navigation algorithm in Drosophila for complex visual environments

Canelo,

Kim,

Park

et al. 2024

Preprint

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Drosophila visuomotor processing has been intensively studied in recent years, leading to a qualitative understanding of individual neural circuits. However, the collective operation of these circuits during naturalistic behaviors, in which flies encounter a mixture of complex visual stimuli—including those caused by their own actions—remains unexplored. In this study, we developed an integrative model of Drosophila visuomotor processing, wherein multiple visuomotor circuits interconnect through an efference copy (EC) mechanism. To derive the model experimentally, we analyzed the wingbeat responses of flying Drosophila to individual, rotating visual patterns. We then combined these models to build an integrative model for superposed visual patterns, using three different strategies: the addition-only, the graded EC, and the all-or-none EC models. We compared orientation behaviors of these models with those of flying Drosophila that rotates their body freely in response to complex visual patterns. Results of these experiments support the all-or-none EC model, in which the amplitude of the flight turn is unimpeded by the background scene, irrespective of the visual environment. Together, our “virtual fly” model provides a formal description of vision-based navigation strategies of Drosophila in complex visual environments and offers a novel framework for assessing the role of constituent visuomotor neural circuits in real-world contexts.

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From Photons to Behaviors: Neural Implementations of Visual Behaviors in Drosophila

Cited by 12 publications

References 163 publications

Anatomical organization of the cerebrum of the praying mantis Hierodula membranacea

Anatomical organization of the cerebrum of the praying mantis Hierodula membranacea

The role of learning-walk related multisensory experience in rewiring visual circuits in the desert ant brain

A visual efference copy-based navigation algorithm in Drosophila for complex visual environments

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