Abstract
Antibodies directed against different visual pigment opsins, and an antibody raised against the C terminal of the α-subunit of retinal G protein (transducin) labelled cerebrospinal fluid-contacting cells located within the hypothalamus (postoptic commissural nucleus and ventral hypothalamic nucleus) of ammocoete lampreys (Petromyzon marinus). These antibodies also labelled photoreceptor cells within the retina and the pineal and parapineal organs, but no other areas of the brain. Despite considerable behavioural and physiological evidence for the existence of deep brain photoreceptors, numerous studies have failed to identify photoreceptor proteins within the basal brain. The results presented in this paper support our recent results in the lizard Anolis carolinensis, suggesting that a group of cerebrospinal fluid-contacting neurons within the vertebrate brain have a photosensory capacity. We speculate that these cells mediate extraocular and extrapineal photoreception in nonmammalian vertebrates.
Similar content being viewed by others
References
Benoit J (1935a) Le role des yeux dans l'action stimulante de la lumière sur le developpement testiculaire chez le canard. C R Soc Biol (Paris) 118:669–671
Benoit J (1935b) Stimulation par la lumière artificielle du developpement testiculaire chez des canards aveugles par section du nerf optique. C R Soc Biol (Paris) 120:133–136
Benoit J (1964) The role of the eyes and of the hypothalamus in the photostimulation of gonads in the duck. Ann N Y Acad Sci 117:204–215
Foster R G, Follett B K (1985) The involvement of a rhodopsin-like photopigment in the photoperiodic response of the Japanese quail. J Comp Physiol 157:519–528
Foster R G, Korf H-W, Schalken J J (1987) Immunocytochemical markers revealing retinal and pineal but not hypothalamic photoreceptor systems in the Japanese quail. Cell Tissue Res 248:161–167
Foster R G, Garcia-Fernandez J M, Provencio I, DeGrip W J (1993) Opsin localization and chromophore retinoids identified within the basal brain of the lizard Anolis carolinensis. J Comp Physiol 172:33–45
Frisch K von (1911) Beiträge zur Physiologie der Pigmentzellen in der Fischhaut. Pflugers Arch 138:319–387
Groos G (1982) The comparative physiologyof extraocular photoreception. Experientia 38:989–1128
Hardisty M W, Potter I C (1971) The behavior, ecology and growth of larval lampreys. In: The biology of lampreys. Hardisty M W, Potter I C (eds) Academic Press, London, pp 85–125
Hartwig H G (1982) Comparative aspects of retinal and extraretinal photosensory input channels of entraining endogenous rhythms. In: Aschoff J, Daan S, Groos G (eds) Vertebrate circadian systems. Springer, Berlin Heidelberg New York, pp 25–30
Kavaliers M (1980) Retinal and extraretinal entrainment action spectra for the activity rhythm of the lake chub Conessius plumbeus. Behav Neural Biol 30:56–67
Margry R J C F, Jacobs C W M, DeGrip W J, Daemen F J M (1983) Detergent-induced specificity of an anti-rhodopsin serum for opsin. Micro complement-fixation studies. Biochim Biophys Acta 742:463–470
Menaker M (1968) Extraretinal light perception in the sparrow. I. Entrainment of the biological clock. Proc Natl Acad Sci USA 59:414–421
Menaker M (1972) Nonvisual light reception. Sci Am 226:22–29
Menaker M, Keatts H (1968) Extraretinal light perception in the sparrow. II. Photoperiodic stimulation of testis growth. Proc Natl Acad Sci USA 60:146–151
Menaker M, Roberts R, Elliott J, Underwood H (1970) Extraretinal light perception in the sparrow. III. The eyes do not participate in photoperiodic photoreception. Proc Natl Acad Sci USA 67:320–325
Oksche A, Hartwig H G (1975) Photoneuroendocrine systems and the third ventricle. In: Knigge K M, Scott D E, Kobayashi H, Ishii S (eds) Brain-endocrine interactions II. Karger, Basel, pp 118–131
Purvis H A (1979) Variations in growth, age at transformation, and sex ratio of sea lampreys reestablished in chemically treated tributaries of the upper Great lakes. Can J Fish Aquat Sci 37:1827–1834
Rubinson K, Cain H (1989) Neural differentiation in the retina of the larval sea lamprey (Petromyzon marinus). Visual Neurosci 3:241–248
Schalken J J, DeGrip W J (1986) Enzyme-linked immunosorbent assay for the quantitative determination of the visual pigment rhodopsin in total eye extracts. Exp Eye Res 43:431–439
Scharrer E (1928) Die Lichtempfindlichkeit blinder Elritzen. I. Untersuchungen über das Zwischenhirn der Fische. Z Vgl Physiol 7:1–38
Scharrer E (1964) Photoneuroendocrine systems: general concepts. Ann NY Acad Sci 117:13–22
Schober W (1964) Vergleichend-anatomische Untersuchungen am Gehirn der Larven und adulten Tiere von Lampetra fluviatilis (Linné, 1758) und Lampetra planeri (Bloch, 1784). J Hirnforsch 7:107–209
Silver R, Witkovsky P, Horvath P, Alones V, Barnstable C J, Lehman M N (1988) Coexpression of opsin-and VIP-like-immunoreactivity in CSF-contacting neurons of the avian brain. Cell Tissue Res 253:189–198
Simonds W F, Goldsmith P K, Codina J, Unson C G, Spiegel A M (1989) Gi2 mediates 326-1 inhibition of adenylyl cyclase in platelet membranes: in situ identification with GαC-terminal antibodies. Proc Natl Acad Sci USA 86:7809–7813
Szél A, Röhlich P (1985) Localization of visual pigment antigen to photoreceptor cells with different oil droplets in the chicken retina. Acta Biol Acad Sci Hung 36:319–324
Szél A, Takács L, Monostori E, Diamantstein T, Vigh-Teichmann I, Röhlich P (1986) Monoclonal antibody recognizing cone visual pigment. Exp Eye Res 43:871–883
Szél A, Diamantstein T, Rohlich P (1988) Identification of the bluesensitive cones in the mammalian retina by anti-visual pigment antibody. J Comp Neurol 273:593–602
Tabata M, Minh-Nyo M, Oguri M (1989) Thresholds of retinal and extraretinal photoreceptors measured by photobehavioral response in catfish, Silurus asotus. J Comp Physiol [A] 164:797–803
Underwood H, Menaker M (1976) Extraretinal photoreception in lizards. J Comp Physiol 83:187–222
Van Veen T, Hartwig H-G, Müller K (1976) Light dependent motor activity and photonegative behavior in the eel (Anguilla anguilla L.). J Comp Physiol 111:209–219
Vigh B, Vigh-Teichmann I (1988) Comparative neurohistology and immunocytochemistry of the pineal complex with special reference to CSF-contacting neuronal structures. Pineal Res Rev 6:1–65
Vigh B, Röhlich P, Vigh-Teichmann I, Aros B (1980) Comparison of the pineal complex, retina and cerebrospinal fluid-contacting neurons by immunocytochemical antirhodopsin reaction. Z Mikrosk Anat Forsch 94:623–640
Vigh B, Vigh-Teichmann I, Röhlich P, Aros B (1982) Immunoreactive opsin in the pineal organ of reptiles and birds. Z Mikrosk Anat Forsch 96:113–129
Vigh B, Vigh-Teichmann I, Röhlich P, Oksche A (1983) Cerebrospinal fluid-contacting neurons, sensory pinealocytes and Landolt's clubs of the retina as revealed by means of electronmicroscopic immunoreaction against opsin. Cell Tissue Res 233:539–548
Yokoyama K, Oksche A, Darden T R, Farner D S (1978) The sites of encephalic photoreception in the photoperiodic induction of growth of the testes in the white-crowned sparrow, Zonotrichia leucophrys gambelii. Cell Tissue Res 189:441–467
Young J Z (1935) The photoreceptors of lampreys. II. The functions of the pineal complex. J Exp Biol 12:254–270
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
García-Fernández, J.M., Foster, R.G. Immunocytochemical identification of photoreceptor proteins in hypothalamic cerebrospinal fluid-contacting neurons of the larval lamprey (Petromyzon marinus). Cell Tissue Res 275, 319–326 (1994). https://doi.org/10.1007/BF00319430
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00319430