{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,15]],"date-time":"2026-07-15T00:33:59Z","timestamp":1784075639496,"version":"3.55.0"},"reference-count":47,"publisher":"The Company of Biologists","license":[{"start":{"date-parts":[[2019,1,1]],"date-time":"2019-01-01T00:00:00Z","timestamp":1546300800000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/www.biologists.com\/user-licence-1-1\/"}],"funder":[{"DOI":"10.13039\/501100001691","name":"Japan Society for the Promotion of Science","doi-asserted-by":"publisher","award":["16K07443"],"award-info":[{"award-number":["16K07443"]}],"id":[{"id":"10.13039\/501100001691","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>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 non-ocular photosensory systems play remain elusive. We found that the terrestrial slug Limax valentianus avoids light and escape into dark areas even if it is blinded by the removal of the bilateral superior tentacle. The escape behaviour was more evident for the short-wavelength light. Illumination with blue but not red light, to the head 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 that of rhodopsin to a lesser extent, were expressed in the brain according to RT-PCR. Light-evoked neural responses were recorded from the left cerebro-pleuro connective of the isolated suboesophageal ganglia of the brain, revealing that the brain is sensitive to short wavelengths of light (400 \u2013 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 Limax valentianus detect and avoid light by using their brain as a light sensing organ in the absence of eyes.<\/jats:p>","DOI":"10.1242\/jeb.208595","type":"journal-article","created":{"date-parts":[[2019,7,2]],"date-time":"2019-07-02T19:54:09Z","timestamp":1562097249000},"source":"Crossref","is-referenced-by-count":12,"title":["Light avoidance by non-ocular photosensing system in the terrestrial slug<i>Limax valentianus<\/i>"],"prefix":"10.1242","author":[{"given":"Haruka","family":"Nishiyama","sequence":"first","affiliation":[{"name":"Department of Environmental Sciences, International College of Arts and Sciences, Fukuoka Women's University, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Akane","family":"Nagata","sequence":"additional","affiliation":[{"name":"Department of Environmental Sciences, International College of Arts and Sciences, Fukuoka Women's University, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuko","family":"Matsuo","sequence":"additional","affiliation":[{"name":"Department of Environmental Sciences, International College of Arts and Sciences, Fukuoka Women's University, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3144-4275","authenticated-orcid":false,"given":"Ryota","family":"Matsuo","sequence":"additional","affiliation":[{"name":"Department of Environmental Sciences, International College of Arts and Sciences, Fukuoka Women's University, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","published-online":{"date-parts":[[2019,1,1]]},"reference":[{"key":"2021042513381495600_JEB208595C1","doi-asserted-by":"publisher","first-page":"258","DOI":"10.1006\/nlme.1999.3933","article-title":"Appetitive learning using visual conditioned stimuli in the pond snail, Lymnaea","volume":"73","author":"Andrew","year":"2000","journal-title":"Neurobiol. Learn. Mem."},{"key":"2021042513381495600_JEB208595C2","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1002\/jez.1402160104","article-title":"Extraocular photoentrainment of the circadian locomotor rhythm of the garden slug Limax","volume":"216","author":"Beiswanger","year":"1981","journal-title":"J. Exp. Zool."},{"key":"2021042513381495600_JEB208595C3","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1007\/BF00696349","article-title":"Extraocular photoreceptors and oscillators can control the circadian rhythm of behavioral activity in Aplysia","volume":"84","author":"Block","year":"1973","journal-title":"J. Com. Physiol. A."},{"key":"2021042513381495600_JEB208595C4","doi-asserted-by":"publisher","first-page":"158","DOI":"10.1111\/j.1744-7410.2003.tb00081.x","article-title":"Description of intracerebral ocelli in two species of North American crayfish: Orconectes limosus (Cambaridae) and Pacifastacus leniusculus (Astacidae)","volume":"122","author":"Bobkova","year":"2003","journal-title":"Invertebr. Biol."},{"key":"2021042513381495600_JEB208595C5","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1085\/jgp.62.3.239","article-title":"Light response of a giant Aplysia neuron","volume":"62","author":"Brown","year":"1973","journal-title":"J. Gen. Physiol."},{"key":"2021042513381495600_JEB208595C6","doi-asserted-by":"publisher","first-page":"156","DOI":"10.1016\/0003-2697(87)90021-2","article-title":"Single-step method for RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction","volume":"162","author":"Chomczynski","year":"1987","journal-title":"Anal. Biochem."},{"key":"2021042513381495600_JEB208595C7","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/S0006-8993(02)03143-8","article-title":"Non-ocular dermal photoreception in the pond snail Lymnaea stagnalis","volume":"951","author":"Chono","year":"2002","journal-title":"Brain Res."},{"key":"2021042513381495600_JEB208595C8","doi-asserted-by":"publisher","first-page":"669","DOI":"10.1085\/jgp.12.5.669","article-title":"The phototrophic excitation of Limax","volume":"12","author":"Crozier","year":"1929","journal-title":"J. Gen. Physiol."},{"key":"2021042513381495600_JEB208595C9","doi-asserted-by":"publisher","first-page":"6053","DOI":"10.1073\/pnas.1515516113","article-title":"Deep-brain photoreception links luminance detection to motor output in Xenopus frog tadpoles","volume":"113","author":"Currie","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042513381495600_JEB208595C10","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1007\/s00114-007-0315-2","article-title":"Clockwork blue: on evolution of non-image-forming retinal photoreceptors in marine and terrestrial vertebrates","volume":"95","author":"Erren","year":"2008","journal-title":"Naturwissenschaften"},{"key":"2021042513381495600_JEB208595C11","doi-asserted-by":"publisher","first-page":"2042","DOI":"10.1016\/j.cub.2012.08.016","article-title":"Deep brain photoreceptors control light-seeking behavior in zebrafish larvae","volume":"22","author":"Fernandes","year":"2012","journal-title":"Curr. Biol."},{"key":"2021042513381495600_JEB208595C12","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1111\/j.1744-7410.2002.tb00131.x","article-title":"Intracerebral ocelli in an amphipod: external photoreceptors of the sandhopper Talitrus saltator (Crustacea, Amphipoda)","volume":"121","author":"Frelon-Raimond","year":"2005","journal-title":"Invert. Biol."},{"key":"2021042513381495600_JEB208595C13","doi-asserted-by":"publisher","first-page":"532","DOI":"10.2108\/zs170071","article-title":"Context-dependent passive avoidance learning in the terrestrial slug Limax","volume":"34","author":"Fujisaki","year":"2017","journal-title":"Zool. Sci."},{"key":"2021042513381495600_JEB208595C14","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1002\/neu.20210","article-title":"Novel kruppel-like factor is induced by neuronal activity and sensory input in the central nervous system of the terrestrial slug Limax valentianus","volume":"66","author":"Fukunaga","year":"2006","journal-title":"J. Neurobiol."},{"key":"2021042513381495600_JEB208595C15","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1016\/j.yfrne.2014.11.001","article-title":"The hypothalamic photoreceptors regulating seasonal reproduction in birds: a prime role for VA opsin","volume":"37","author":"Garc\u00eda-Fern\u00e1ndez","year":"2015","journal-title":"Front. Neuroendocrinol."},{"key":"2021042513381495600_JEB208595C16","doi-asserted-by":"publisher","first-page":"S286","DOI":"10.1007\/s00239-003-0038-8","article-title":"The coevolution of blue-light photoreception and circadian rhythms","volume":"57","author":"Gehring","year":"2003","journal-title":"J. Mol. Evol."},{"key":"2021042513381495600_JEB208595C17","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1007\/BF00618180","article-title":"Morphology and function of the photoexcitable neurones in the central ganglia of Onchidium verruculatum","volume":"99","author":"Gotow","year":"1975","journal-title":"J. Comp. Physiol."},{"key":"2021042513381495600_JEB208595C18","doi-asserted-by":"publisher","first-page":"18","DOI":"10.3389\/neuro.03.018.2009","article-title":"A new photosensory function for simple photoreceptors, the intrinsically photoresponsive neurons of the sea slug Onchidium","volume":"3","author":"Gotow","year":"2009","journal-title":"Front. Cell. Neurosci."},{"key":"2021042513381495600_JEB208595C19","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1007\/s001140050732","article-title":"The brain as a photoreceptor: intracerebral ocelli in the firefly","volume":"87","author":"Hariyama","year":"2000","journal-title":"Naturwissenschaften"},{"key":"2021042513381495600_JEB208595C20","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1242\/jeb.57.3.651","article-title":"Photosensitive neurones in the marine pulmonate mollusk Onchidium verruculatum","volume":"57","author":"Hisano","year":"1972","journal-title":"J. Exp. Biol."},{"key":"2021042513381495600_JEB208595C21","doi-asserted-by":"publisher","first-page":"483","DOI":"10.1016\/S1095-6433(02)00351-3","article-title":"Photosensitive neurons in mollusks","volume":"134","author":"Kartelija","year":"2003","journal-title":"Comp. Biochem. Physiol. A."},{"key":"2021042513381495600_JEB208595C22","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1016\/0042-6989(75)90284-9","article-title":"Fine structure of the retina of a slug, Limax flavus L","volume":"15","author":"Kataoka","year":"1975","journal-title":"Vision Res."},{"key":"2021042513381495600_JEB208595C23","doi-asserted-by":"publisher","first-page":"106","DOI":"10.3389\/fevo.2016.00106","article-title":"The biological mechanisms and behavioral functions of opsin-based light detection by the skin","volume":"4","author":"Kelley","year":"2016","journal-title":"Front. Ecol. Evol."},{"key":"2021042513381495600_JEB208595C24","doi-asserted-by":"publisher","first-page":"1137","DOI":"10.1007\/s00359-015-1043-2","article-title":"Short- and long-wavelength-sensitive opsins are involved in photoreception both in the retina and throughout the central nervous system of crayfish","volume":"201","author":"Kingston","year":"2015","journal-title":"J. Comp. Physiol. A"},{"key":"2021042513381495600_JEB208595C25","doi-asserted-by":"publisher","first-page":"3834","DOI":"10.1523\/JNEUROSCI.3689-12.2013","article-title":"Identification of nonvisual photomotor response cells in the vertebrate hindbrain","volume":"33","author":"Kokel","year":"2013","journal-title":"J. Neurosci."},{"key":"2021042513381495600_JEB208595C26","doi-asserted-by":"crossref","DOI":"10.1093\/acprof:oso\/9780199581139.001.0001","volume-title":"Animal Eyes","author":"Land","year":"2012","edition":"2nd edn"},{"key":"2021042513381495600_JEB208595C27","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1007\/BF00696348","article-title":"Extraocular photoreceptors can entrain the circadian rhythm in the abdominal ganglion of Aplysia","volume":"84","author":"Lickey","year":"1973","journal-title":"J. Comp. Physiol. A."},{"key":"2021042513381495600_JEB208595C28","doi-asserted-by":"publisher","first-page":"2239","DOI":"10.1046\/j.1471-4159.2000.0742239.x","article-title":"Identification and cataloging of genes induced by long-lasting long-term potentiation in awake rats","volume":"74","author":"Matsuo","year":"2000","journal-title":"J. Neurochem."},{"key":"2021042513381495600_JEB208595C29","doi-asserted-by":"publisher","first-page":"1023","DOI":"10.1007\/s00359-014-0954-7","article-title":"Photo-tropotaxis based on projection through the cerebral commissure in the terrestrial slug Limax","volume":"200","author":"Matsuo","year":"2014","journal-title":"J. Comp. Physiol. A"},{"key":"2021042513381495600_JEB208595C30","doi-asserted-by":"publisher","first-page":"3301","DOI":"10.1242\/jeb.162701","article-title":"Expression and light-dependent translocation of \u03b2-arrestin in the visual system of the terrestrial slug Limax valentianus","volume":"220","author":"Matsuo","year":"2017","journal-title":"J. Exp. Biol."},{"key":"2021042513381495600_JEB208595C31","article-title":"Co-expression of opsins in the eye photoreceptors of the terrestrial slug Limax valentianus","author":"Matsuo","year":"2019","journal-title":"J. Comp Neurol"},{"key":"2021042513381495600_JEB208595C32","doi-asserted-by":"publisher","first-page":"320","DOI":"10.1073\/pnas.67.1.320","article-title":"External light perception in the sparrow, III: the eyes do not participate in photoperiodic photoreception","volume":"67","author":"Menaker","year":"1970","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042513381495600_JEB208595C33","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1002\/jemt.1070","article-title":"Photoreception and circadian clock system of the chicken pineal gland","volume":"53","author":"Okano","year":"2001","journal-title":"Microsc. Res. Tech."},{"key":"2021042513381495600_JEB208595C34","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/S0006-3495(83)84285-4","article-title":"Squid retinochrome. Configurational changes of the retinal chromophore","volume":"44","author":"Ozaki","year":"1983","journal-title":"Biophys. J."},{"key":"2021042513381495600_JEB208595C35","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1016\/0300-9629(77)90019-6","article-title":"Effects of light on identified Helix pomatia neurons","volume":"58A","author":"Pa\u0161i\u0107","year":"1977","journal-title":"Comp. Biochem. Physiol."},{"key":"2021042513381495600_JEB208595C36","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1017\/S0952523811000150","article-title":"Understanding the dermal light sense in the context of integrative photoreceptor cell biology","volume":"28","author":"Ramirez","year":"2011","journal-title":"Vis. Neurosci."},{"key":"2021042513381495600_JEB208595C37","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1016\/j.cbpa.2010.01.026","article-title":"A new role for photoresponsive neurons called simple photoreceptors in the sea slug Onchidium verruculatum: potentiation of synaptic transmission and motor response","volume":"156","author":"Shimotsu","year":"2010","journal-title":"Comp. Biochem. Physiol. A."},{"key":"2021042513381495600_JEB208595C38","doi-asserted-by":"publisher","first-page":"745","DOI":"10.1007\/BF00187319","article-title":"Light-evoked walking in crayfish: behavioral and neuronal responses triggered by the caudal photoreceptor","volume":"166","author":"Simon","year":"1990","journal-title":"J. Comp. Physiol. A."},{"key":"2021042513381495600_JEB208595C39","first-page":"342","article-title":"Sensory systems involved in the shadow response of Lymnaea stagnalis (L.) as studied with use of habituation phenomena","volume":"75","author":"Stoll","year":"1972","journal-title":"Proc. K. Ned. Akad. Wet. C."},{"key":"2021042513381495600_JEB208595C40","doi-asserted-by":"publisher","first-page":"3409","DOI":"10.1242\/jeb.043521","article-title":"The shadow-induced withdrawal response, dermal photoreceptors, and their input to the higher-oder interneuron RPeD11 in the pond snail Lymnaea stagnalis","volume":"213","author":"Sunada","year":"2010","journal-title":"J. Exp. Biol."},{"key":"2021042513381495600_JEB208595C41","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1007\/BF00657527","article-title":"Duplex system in the simple retina of a gastropod mollusk, Limax flavus L","volume":"133","author":"Suzuki","year":"1979","journal-title":"J. Comp. Physiol."},{"key":"2021042513381495600_JEB208595C42","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1007\/BF00619152","article-title":"Non-ocular photoreceptors and photo-orientation in the pond snail Lymnaea stagnalis (L.)","volume":"149","author":"van Duivenboden","year":"1982","journal-title":"J. Comp. Physiol."},{"key":"2021042513381495600_JEB208595C43","doi-asserted-by":"publisher","first-page":"R685","DOI":"10.1016\/j.cub.2009.07.036","article-title":"Seasonal biology: avian photoreception goes deep","volume":"19","author":"Wyse","year":"2009","journal-title":"Curr. Biol."},{"key":"2021042513381495600_JEB208595C44","doi-asserted-by":"publisher","first-page":"921","DOI":"10.1038\/nature09576","article-title":"Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall","volume":"468","author":"Xiang","year":"2010","journal-title":"Nature."},{"key":"2021042513381495600_JEB208595C45","doi-asserted-by":"publisher","first-page":"1841","DOI":"10.1242\/jeb.018028","article-title":"Redundancy of olfactory sensory pathways for odor-aversion memory in the terrestrial slug Limax valentianus","volume":"211","author":"Yamagishi","year":"2008","journal-title":"J. Exp. Biol"},{"key":"2021042513381495600_JEB208595C46","first-page":"581","article-title":"Extraocular photoreception","volume-title":"Handbook of Sensory Physiology","author":"Yoshida","year":"1979"},{"key":"2021042513381495600_JEB208595C47","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1111\/j.1463-6395.2008.00369.x","article-title":"Eyes and vision in Arion rufus and Deroceras agreste (Mollusca; Gastropoda; Pulmonata): what role does photoreception play in the orientation of these terrestrial slugs?","volume":"90","author":"Zieger","year":"2009","journal-title":"Acta Zool."}],"container-title":["Journal of Experimental Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/syndication.highwire.org\/content\/doi\/10.1242\/jeb.208595","content-type":"unspecified","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.208595\/1909494\/jeb208595.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.208595\/2066224\/jeb_208595v1.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.208595\/2066224\/jeb_208595v1.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,22]],"date-time":"2022-09-22T19:47:45Z","timestamp":1663876065000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/jeb\/article\/doi\/10.1242\/jeb.208595\/258873\/Light-avoidance-by-non-ocular-photosensing-system"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,1,1]]},"references-count":47,"URL":"https:\/\/doi.org\/10.1242\/jeb.208595","relation":{},"ISSN":["1477-9145","0022-0949"],"issn-type":[{"value":"1477-9145","type":"electronic"},{"value":"0022-0949","type":"print"}],"subject":[],"published":{"date-parts":[[2019,1,1]]},"article-number":"jeb.208595"}}