Kato, Masaru

Oishi, Tadashi

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RIGHT:URL:CITATION:AUTHOR(S):ISSUE DATE:TITLE:Pineal Organ as a PossiblePhotoreceptor in PhotoperiodicTesticular Response in JapaneseQuailOishi, Tadashi; Kato, MasaruOishi, Tadashi ...[et al]. Pineal Organ as a Possible Photoreceptor in PhotoperiodicTesticular Response in Japanese Quail. Memoirs of the Faculty of Science, KyotoUniversity. Series of biology. New series 1968, 2(1): 12-181968-09-30http://hdl.handle.net/2433/258781      Nl glEMOIRS OF THE F'ACULTY OF SCIENCE, KYOTO UNIVERSITY, SERIES OF BIOLOGY                       VoL ll.,No. I, pp. 1.?.-18, Sept. 1968      Pineal Organ as a Possible Photoreceptor in            Photoperiodic Testicular Response in                           Japanese Quail                      Tadashi OisHi and Masaru KATo        Department of Zoology, Faculty of Science, Kyoto University,                               Kyoto, Jcftpan      ABS7'RACT In male Japanese quail illumination of the pineal organ with     luminous paint emitting orange light causes maintenance of testicular size     for two weeks after transfer from continuous light (LL) to 8-hour daily     photoperiods (8L16D). Non-treated coiitrols and subjects treated with lurni-     not'ts paint emitting green light, subrnitted to the same change in day length,     underwent extensive testicular regression. Although pinealectomy did not     affect testicular size in birds subjected to LL, pinealectomized birds treated     with luminous paint underwent testicular regressio'n when changed to 8L16D.     This suggests that the pineal organ may serve as a receptor for long wave     lengths in the photoperiodic testicutlar response in this species.                               Introduction    There have been very few investigations of the photoreception naeclaanism inphotoperiodical]y induced testicular clevelopment in birds (Farner, 1959) sinceBenoit and his colleagues suggested that liglat could stimulate the hypothalamusdirectly through the orbit in the duck (Benoit and Assenmacher, 1959). Inrecent studies, eviclence was obtained that suggests the existence of photorecep-tors ka the brain of the Japanese quail (Oishi el al., 1966), Although Oksclaeand Vaupel-von Harnack (1965) found no typical photoreceptor st'ructure in thebircls stuclied by them, Bischoff and Richter (1966) tiouncl that the pineal cellsot" the quail hacl numerous ixticro-vil]i ancl ixtembranous ]amellar complexessuggestive ot' a photoreceptor function. Quay and Renzoni (19. 63) also suggestedmicroscopically the presence of sensory cells in the pineal organ of birds, Shouldthis be the case, there is the possibility of the phylogenetic persistence of aphotoreceptor now involved in testicular development, since the pineal is thoughtto have a ftmction as a photoreceptor of reptiles and amphibians (Bagnara, 1965;Clausen and Poris, 1937; van de Kamer, 1965), Also possibly pertinent is thereport that the mairtmalian pineal, which has no clirect role ot'- photoreceptor,                       Pineal asaPossible Photoreceptor 13secretes melatonin that inhibits Iight-induced gonadal growth (Wurtmcftn andAxelrod, 1965). For these reasons, experiments were carried out to confirm thepreliminary stuclies (Kato et al., 1967) that have shown an effect of local illumi-nation of pineal organ on testicular activity.                          Materials aRd Method$    Experiments were carried out with mature male :Japanese quail of 11 weeksof age, which had been reared under continuous light from hatching. Day-lightfluorescent tubes were used as the light source. Light intensity at the floor ofaviary was 100-1000 lux during light t-raction and less than O.Ol lux in darkfx'action of the 24-hour cycle. Room temperature was held at 25.5Å} O.2eC throllg-hout the experiments. Cominercially prepared t'ood and water were provided adlibitu7n.    To illuminate tlie pineal organ, radioluminous pigments were painted locallyon the adjacent region of the skull. Two kinds of radioltmiinous pigments (LC-R!A and LC-GIH) made by Dai Nippon Sinleuch Co., Ltd. were used. LC-RIAenaits orange light (maximum 600 mpt) and LC-GIH emits green light (maximum520 mpt). The characteznistic of these paints have been described previously (Katoel al., 1967).    Pinealectomy was eÅ}-fected as follows. The skin on the midline of theoccipital region of the head xvas cut open with a surgical scissors and a smallrectangular flap of the skull (about 15 mm2) was cut out with a hancl drill.The pineal organ was carefully reinoved through an opening in the meninges,As soon as the pineal organ was taken out, a gelform sponge was placed on thewound for hemostasis. The survival rate in the operation was about 80-0o!; ananatomical examination of the pinealectomy was niade each individual at antopsy.In the shamoperated controls all procedures xvere tlie same as for the pinealecto-mized birds except for the actual removal of the pineal organ. These operationswere made four clays before the beginning of the experiments.    Body weights and testicular weights vLiere recorded at the beginning ancl theend of the experiments respectively. Brains and testes were fixed in Bouin'sfluid for histological observatlon, The details of the experimental lightingregimens were shown in Fig.-1. Experiinental conditions were maintained fortwo weeks in all cases.    As controls, normal animals (A) were divided into two groups at the age of11 weeks and were maintained under continuous Iight (LL) and 8 hours light 16hours darl<ness (8L 16D), respectively. At the beginning of the experimentalillumination, sham-operated birds (B) were divided to four groups. One groupwas maintained tmder ILL, the other three groups were placed on under 8L 16D;the first and seconcl groups were without radioluminous paint, whereas the birdsin the thircl group were painted with the LC-RIA on a sniall surface area (about15 inni2) above the pineal organ; the t'ourth gi'oup was treatecl siinilarly "iiththe LC-GIH. The pinealectomized birds (C) were also divided in four groups14A:BNorrnGlihsadaTsamnaOib"Hi and Masaru KAToSham-operated animals                  TC : Pinealectomized animals                           T       (hatching)           k--- l1 weeks -* 4d.           Fig. 1. : Experimental           white line : continuous           black line : 8-hours daily             t: sham operation             :•, : pinealectomy           LC--RIA : treatment with           LC-GIH : trcatment witheach treated identically with its                           Results    The results obtained aretwo weeks after change from LL toXVhereas norrnal controls heldcular weight ot' 1,' ,328 Å} 144 mg.    For the sham-operated birds onÅ} 31 mg whereas it was 421 Å} 159rence is significant (p<O.05). Thisthat the shani operation has notestes of the birds treated withstate (1,O05 Å} 58 mg) for at leastwith LC-GIE[ (green ligh't) regressedbetween these values wasLC-RIALC-GIHLC -- RIALC-GIH        -)i(--- 2 weeks -       scliedule       Iight (LL)         photoperiods (8L 16D)         a radiolGininous paint (orange iight)         a radioluminous paint (green light)      corresponding control group.          and Discussion  summarized in Table I. Ixllormal anima}s (group A),         8L 16D had a mean weight of 152 Å} 45 mg.   continuously on LL to this time had a irtean testi-      The difi'erence ie highly significant (p<O.Ol).         LL the mean testicular weight was 1, 352         mg for those changed to 8L 16D; the diffe-          difference between LL and 8L l6D indicates      infltience on tlae testiculai" development.• The     LC-RIA (orange light) maintained their developed         two weel<s on 8L16D whereas those treated         consiclerably (/1-75 Å} 97 mg). The clifferencestatistically significant (p<O.05).Pineal as a Possible Photoreceptor 15Table 1. Experimental ResulicsABCExperiment IiTiordsof Body wllgeahnt i- \eslielsweighwwtwwun'   ........... .............. . .. .... .. .......-.. ...g.gg})........,,,.,... ......gg.}.g.)... ; Normal animals  Sta rt 5 le4. 8.", -.. 3.8 1, 396 .ti: 112  LL 5 93 7i. 3.2 1, 328 .i.um 144  8L 16D 10 104. 7f.: le.4 152 r}: 45: Sham-operated animals  Start 5 88.4:i: 4.6 1,490.-." 83  LL 5 99.8rt 2.4 1,352ri.:- 31  8L16D 5 92•O.",L". 6+3 421.",'a'..159  8L16D (LC-RIA) 6 99.7-4.-.. 2.6 1,e05,f,,- 58  8L!6D (LC-GIH) 6 99.5.k 2.3 475th.- 97: Pinealectomizedanimals  Start 5 85.6:i: 4.4 1,45{ .".: 66  LL 8 101.0.-,i-,. 3. 9. 1, 670.-i.: 87  8L16D 6 102.0ti: 3.1 273Å}194  8L16D (LC-RIA) 6 91.6ra: 3.5 438.-,L.162•  8L16D (LC--GII{[) 10 103.6.j,-,wr 1.4 441.Å}139.              Start : at the be•ginning of the experiments Cll weeks of age)              LL : continuous Hght              8L16D : 8 hours light : l6 hours darkness              LC-RIA ; radioluminous paint (orange light)              LC-GII-I : radioluminous paint (green light)   Important in Gr'oup B is not that a sliglit di'fference occured between thesham-operated birds on LL and LC-RIA-treated group but that gonadal develop-ment was maintained on the local illuiinination wlth LC-RIA, It suggests stronglythat the pineal organ has soirte photoreceptive function, It is also clear that tliemaintenance of maturity was not due to the contamination of tritium radiationfroni the radioluminous paint, because the two substances (IC-RIA and LC-GIE[)caused different testicular responses (see Table I). These results also suggestthat the pineal organ is involved in reception of long wave' Iengths sttcli as or-ange but not with short wave lengths like green.   In the pinealectomized birds on LL, testicular weight was maintained (l, 670Å} 87 mg), Whereas there vtTas signi'ficant re.crression (273 Å} 194 mg; p<O.Ol)in these changed to 8L16D. These testicular responses were the same as those'of normal animals. However the testiculaz- weight of the birds treated with LC-RIA and IC-GIH were lower than those of birds held on LL (p<O. 05) ancl showedno signi'ficant dif'ference from those changed to 8L16D.    Despite a shorFday treatment gonadal activity was maintained in the intactbirds painted with LC-RIA (B-fourth group), but not in the pinealectomized bircls(C-fourth group). rl]lais suggests that the latter had lost a part of the photo- 16 Tadashi OisHi ancl Masaru l<A'roreceptor system in the pinealec'tomy. However in pinealectomizecl birds (C-secondgroup), the testicular responses were pert'ectly the same as that of normal. It isthought that the systein that induces gonadcal activity can also be activatedthrough a retinal pathway alone,    The pineal organ has not been reported pi-eviotts]y to have a photorecep'torfunction in bird,s. It was siiggested by pre3i,minary study (Kato et al., 1967) andnow confirmeci in the experiment reported here, The results coincide well theobservation that the orange-red !ight had a tenclency to be inost oflective for'the clevelopment ot" gonads in normal birds (Konishi and Kato, unpublished;Benoit ancl Ott, 1938). The scftme tendency can also be observed in enuclea'tedqtiail (Oishi and Kato, unpub]isheCi). It is also significant that a substantlalamollnt of light can reach the pineal through the skull. Ganong et al. (1963)have reportecl tlaat light penetrates into the brain in maiuma•ls. Similarly wealso observecl in quail ehat a consiclerable amount of light penetrated throvighthe skull into the brain,    In our preliminary vvork, it w.fts 't'ouii!d that the testes could consequentlyrespond photoperioclically to the local illumination of eyes; the retina ftu?ctlonsas one ot- the photoreceptors ii:i the photoperiodic testicular responses (Oishi andKato, unpublished). Thus, it 'is sugg'ested that quail has, at least, two sets ofphotoreceptor elements for photoperiodic testicular response, one in eye and theother pineal organ X]Ve must also consider the report that ]ight stiniulates thehypothalanuis directly thereby causes gonadal growth (Benoit, 1959, in dllcks;and Lisk and Kannwisher, 1964, in rats). Thus, it is clear that non-retina}pliotoreceptor in the photoperiodic responses still requh-e further stucly. Recen-tly, pineal organ has been shown to be one of the endocrine glands invo]ved inthe control of gonadal function in naamirLals (Thieblot, l965). In hamstei-s itwas found that pinealectoiny prevents the atrophy of gonad in short day (Hoff-man, 1965); aclministi+ation of pineal extracts produces gonadal ati'ophy, in rats(Ifft, 1962; Kitay, 1954), Similar' results had alreaCly been seen i'n whiteieghorn chickens as that mammals (Shellabarger, 1953). In more recent experi-ments pinealectoiny seems to give no effect on the photoperioclically inducedtesticular developiictent not only in young quail (Hoirtrna et al., 1967, Sayler andXiVo!fson, 1967) bnt also in adu!ts (present work). On the other hand, it hasbeen reported that melatonin synthesis in the hen pineal and serotonin content ofpigeon pineal are controlled by light (Axelrod et al., 1964; Quay, 1966). Con-sequently it is conceivable that the p'ineal organ of birds utilizes environmentallight energy, particulariy for testicular development in male quail. In this con-junction it is important to note again that the quail pineal has a possible photo-receptable fine structure that suggests a photoreceptor function. This mayrepresent a new phylogenetic aspect of pineal functions in consideration of itsrole in reptiles and amphibians.                       Pineal asa Possible Photoreceptor 17                            Acknowledgements    We are indebted to Dr. }I. Kobayashi for his guidance on the technique ofpinealectonay and to Dr. T. Konishi for his 1<ind advices. Thanks also toProfessor D. S, Farner for reading this manuscript and for his 1<ind advice.                                 Referenees AXELROD, J., WVRTMAN, R. J., and WINGET, C.M. (1964).     Melatonin synthesis in the hen pineal gland and its control by light. Natttre 201,     1134. BAGNARA, J. T. (1965). Pineal regulation of body blanching in amphibian larvae.     Prog-ress in Bi-ain Res. 10, 489-504. BEATOIT, J., and ASSENMACHER, I. (1959). 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Pineal Organ as a Possible Photoreceptor in Photoperiodic Testicular Response in Japanese Quail

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Pineal Organ as a Possible Photoreceptor in Photoperiodic Testicular Response in Japanese Quail

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