Co‐expression of opsins in the eye photoreceptor cells of the terrestrial slug <i>Limax valentianus</i>

Matsuo, Ryota; Koyanagi, Mitsumasa; Nagata, Akane; Matsuo, Yuko

doi:10.1002/cne.24732

Cited by 16 publications

(28 citation statements)

References 51 publications

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“…We detected all five mRNA species in the ST and three mRNA species in the brain (Opn5A, retinochrome and xenopsin; Fig. 4A), replicating previous findings (Matsuo et al, 2019). The expression of xenopsin mRNA was also detected in the BW and the PS, whereas retinochrome was barely detected in the BW and was not found in the PS (Fig.…”

Section: Expression Of Opsin Mrnasupporting

confidence: 90%

“…However, a larger percentage of animals was expected to avoid short-wavelength light if monochromatic light with an equivalent photon flux density was used instead. We and other groups also demonstrated that the eye of Limax is more responsive to short-wavelength blue light, especially when the eye is light adapted (Suzuki et al, 1979;Matsuo et al, 2017Matsuo et al, , 2019. The preferential use of short-wavelength light is thought to be a widely conserved phenomenon in the animal kingdom (Gehring and Rosbash, 2003;Erren et al, 2008), and the slugs also appear to have inherited this trait.…”

Section: ) Andsupporting

confidence: 54%

“…2A), but they escaped only from short wavelength light if the irradiance was low (10 μW cm −2 ; Fig. 2B), consistent with the higher sensitivity of the slugs' eyes to short-wavelength light (Suzuki et al, 1979;Matsuo et al, 2017Matsuo et al, , 2019. We judged the avoidance behaviour based on whether more than half of the slug's body was within the dark compartment (criterion number 1).…”

Section: Wavelength Dependency Of Avoidance Behavioursupporting

confidence: 54%

“…We recently found that several opsin species are expressed not only in the photoreceptors of the eye but also in the brain of Limax (Matsuo et al, 2019;see Fig. 4).…”

Section: Discussionmentioning

confidence: 99%

“…We next analysed the expression of opsins, the well-studied photopigment genes in the animal kingdom, in different parts of the body by RT-PCR. As we recently found that five mRNA species belonging to the opsin family genes exist in L. valentianus (Matsuo et al, 2019), the expression of these mRNAs in the brain, the ST (including the eyes), the PS and the dorsal surface of the body (body wall, BW) was examined. We chose the PS because its light detection capability has been suggested in the pond snail Lymnaea stagnalis (Sunada et al, 2010).…”

Section: Expression Of Opsin Mrnamentioning

confidence: 99%

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Light avoidance by non-ocular photosensing system in the terrestrial slugLimax valentianus

Nishiyama

Nagata

Matsuo

et al. 2019

Journal of Experimental Biology

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Although the eye is the best-studied photoreceptive organ in animals, the presence of non-ocular photosensing systems has been reported in numerous animal species. However, most of the roles that nonocular photosensory systems play remain elusive. We found that the terrestrial slug Limax valentianus avoids light and escapes into dark areas even if it is blinded by the removal of the bilateral superior tentacle. The escape behaviour was more evident for short-wavelength light. Illumination to the head with blue but not red light elicited avoidance behaviour in the blinded slugs. Illumination to the tail was ineffective. The light-avoidance behaviour of the blinded slugs was not affected by the removal of the penis, which lies on the brain in the head, suggesting that the penis is dispensable for sensing light in the blinded slug. mRNA of Opn5A, xenopsin, retinochrome and, to a lesser extent, rhodopsin was expressed in the brain according to RT-PCR. Lightevoked neural responses were recorded from the left cerebro-pleural connective of the isolated suboesophageal ganglia of the brain, revealing that the brain is sensitive to short wavelengths of light (400-480 nm). This result is largely consistent with the wavelength dependency of the light-avoidance behaviour of the blinded slugs that we observed in the present study. Our results strongly support that the terrestrial slug L. valentianus detects and avoids light by using its brain as a light-sensing organ in the absence of eyes.

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Section: Expression Of Opsin Mrnasupporting

confidence: 90%

Section: ) Andsupporting

confidence: 54%

Section: Wavelength Dependency Of Avoidance Behavioursupporting

confidence: 54%

“…We recently found that several opsin species are expressed not only in the photoreceptors of the eye but also in the brain of Limax (Matsuo et al, 2019;see Fig. 4).…”

Section: Discussionmentioning

confidence: 99%

Section: Expression Of Opsin Mrnamentioning

confidence: 99%

See 3 more Smart Citations

Light avoidance by non-ocular photosensing system in the terrestrial slugLimax valentianus

Nishiyama

Nagata

Matsuo

et al. 2019

Journal of Experimental Biology

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Regional expression of neuropeptides in the retina of the terrestrial slug Limax valentianus (Gastropoda, Stylommatophora, Limacidae)

Matsuo

2022

J of Comparative Neurology

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Gastropods use lens‐bearing eyes to detect ambient light. The retina contains photoreceptors that directly project to the brain. Here, we identified the neurotransmitters that the retinal cells use for projection to the brain in the terrestrial slug Limax. We identified 12 genes encoding neuropeptides as well as a novel vesicular glutamate transporter, a marker of glutamatergic neuron, expressed in the retinal cells. Spatial expression profiles of the neuropeptide genes were determined by in situ hybridization. WWamide/MIP1/Pedal peptide2 were coexpressed in the neurons of the accessory retina. In the main retina, prohormone‐4 was expressed in the ventrolateral region. Clionin was expressed in the ventromedial region. Pedal peptide was expressed in the anterior region of the main retina and in the accessory retina. Enterin was expressed in many neurons, including the accessory retina, but not in the dorsal region. FxRIamide1 and 2 were coexpressed in the posterior region. Prohormone‐4 variant was uniformly expressed in many neurons but scarcely in the accessory retina. MIP2 was widely expressed throughout the dorsoventral axis in the posteriolateral region of the main retina. Myo1 was expressed in many neurons of the main retina but predominantly in the dorsal region. These expression patterns were confirmed by immunohistochemistry with specific antibodies against the neuropeptides. Projections of these peptidergic retinal neurons were confirmed by immunostaining of the optic nerve. Our present study revealed regional differentiation of the retina with respect to the neurotransmitters that the retinal cells use.

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Visual afferents from an eye in the terrestrial slug Limax valentianus

Matsuo,

Kawakami,

Matsuo

2024

J of Comparative Neurology

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Terrestrial gastropods have a lens‐bearing eye on the tip of their tentacles. There are two morphologically distinct photoreceptors, called Type‐I and Type‐II photoreceptors, in the retina. Type‐I photoreceptors are equipped with highly developed photoreceptive microvilli in their outer rhabdomeric segment, whereas Type‐II photoreceptors have short and fewer microvilli. Although both types of photoreceptors send afferent projections directly to the brain, their destinations in the brain, called optic neuropiles, have not been sufficiently investigated. Our recent studies revealed that there are commissural fibers in the cerebral ganglia that transmit photic information acquired by bilateral eyes. Moreover, some of the retinal photoreceptors are connected by gap junctions to the photosensitive brain neurons, suggesting the functional interaction of the photic information between the eye and brain photoreceptors, as well as between bilateral eyes. However, it has not been clarified which type of retinal photoreceptors send commissural projections to the contralateral hemiganglion nor interact with the brain photoreceptors. In the present study, we demonstrated by molecular histological analyses and tracer injections that (1) Type‐I and Type‐II photoreceptors send glutamatergic afferent projections to the medial and lateral lobes of the ipsilateral optic neuropile, respectively, (2) direct synaptic interaction between bilateral optic nerves occurs in the medial lobe of the optic neuropile, and (3) brain photosensory neurons form gap junctions with the medial lobe of the contralateral optic neuropile. These results reveal an ordered pattern of afferent projections from the retina and provide insight into the different functional roles of retinal photoreceptors.

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Co‐expression of opsins in the eye photoreceptor cells of the terrestrial slug Limax valentianus

Cited by 16 publications

References 51 publications

Light avoidance by non-ocular photosensing system in the terrestrial slugLimax valentianus

Light avoidance by non-ocular photosensing system in the terrestrial slugLimax valentianus

Regional expression of neuropeptides in the retina of the terrestrial slug Limax valentianus (Gastropoda, Stylommatophora, Limacidae)

Visual afferents from an eye in the terrestrial slug Limax valentianus

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