Neural elements in the pineal complex of the frog, Rana esculenta, II: GABA-immunoreactive neurons and FMRFamide-immunoreactive efferent axons

Abstract The photosensory pineal complex of anurans comprises an extracranial part, the frontal organ, and an intracranial part, the pineal organ proper. Although the pineal organ functions mainly as a luminosity detector, the frontal organ monitor the relative proportions of short and intermediate/long wavelengths in the ambient illumination. The major pathway of information processing in the pineal and frontal organs is the photoreceptor to ganglion cell synapse. It is not known whether interneurons form part of the neural circuitry. In the present study, we demonstrate GABA-immunoreactive (GABA-IR) neurons in the pineal and frontal organs of the frog, Rana esculenta. No GABA-IR axons were observed in the pineal nerve between the frontal and pineal organs, or in the pineal tract that connects the pineal complex with the brain. The GABA-IR neurons differed in morphology from centrally projecting neurons visualized by retrograde labeling with horseradish peroxidase. Thus, we suggest that the GABA-IR neurons in the pineal and frontal organs represent local interneurons. Axons of central origin, immunoreactive with a sensitive antiserum against the tetrapeptide Phe-Met-Phe-Arg-NH2 (FMRFamide), were observed in the intracranial portion of the photosensory pineal organ. The immunoreactive axons enter the caudal pole of the pineal organ via the posterior commissure. The largest density of axons was observed in the caudal part, while fewer axons were detected in the rostral portion. The uneven distribution of the FMRFamide-immunoreactive axons may be related to the distribution of different types of intrapineal neurons. FMRFamide-immunoreactive varicose axons were observed in the extracranial frontal organ. A central innervation of the pineal organ, previously known exclusively from amniotes, is probably not per se linked with the evolutionary transition of the pineal organ from a directly photosensory organ to a neuroendocrine organ. It could rather represent a centrifugal input to a sensory system which has been retained when the directly sensory functions have changed, during phylogency, to neuroendocrine functions.

[1]  H. Meissl,et al.  Neural elements of the pineal complex of the frog, rena esculenta, I: Centrally projecting neurons , 1990, Visual Neuroscience.

[2]  S. Ebbesson,et al.  FMRFamide-like immunoreactive neurons of the nervus terminalis of teleosts innervate both retina and pineal organ , 1988, Brain Research.

[3]  T. van Veen,et al.  Temporal disparity in pineal and retinal ontogeny. , 1988, Brain research.

[4]  H. Meissl,et al.  Intracellular staining of physiologically identified photoreceptor cells and hyperpolarizing interneurons in the teleost pineal organ , 1988, Neuroscience.

[5]  W. Geraerts,et al.  The brain of Lymnaea contains a family of FMRFamide-like peptides , 1987, Peptides.

[6]  J. Wu,et al.  Gamma‐aminobutyric acid‐ and glutamic acid decarboxylase‐immunoreactive neurons in the retina of different vertebrates , 1987, The Journal of comparative neurology.

[7]  B. Vígh,et al.  Three types of photoreceptors in the pineal and frontal organs of frogs: ultrastructure and opsin immunoreactivity. , 1986, Archivum histologicum Japonicum = Nihon soshikigaku kiroku.

[8]  T. Getchell,et al.  Amphibian terminal nerve: distribution revealed by LHRH and AChE markers , 1986, Brain Research.

[9]  P. Emson,et al.  Distribution and origins of substance P (SP)-, calcitonin gene-related peptide (CGRP)-, vasoactive intestinal polypeptide (VIP)- and neuropeptide Y (NPY)-containing nerve fibers in the pineal gland of gerbils , 1986, Neuroscience Letters.

[10]  H. Meissl PHOTONEUROPHYSIOLOGY OF PINEALOCYTES , 1986 .

[11]  S. Yazulla Chapter 1 GABAergic mechanisms in the retina , 1986 .

[12]  F. V. van Leeuwen Pitfalls in immunocytochemistry with special reference to the specificity problems in the localization of neuropeptides. , 1986, American Journal of Anatomy.

[13]  T. Staehelin,et al.  Monoclonal antibodies reveal structural homogeneity of gamma-aminobutyric acid/benzodiazepine receptors in different brain areas. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[14]  G. Engbretson,et al.  Identification of putative neurotransmitters in the lizard parietal eye. , 1985, Investigative ophthalmology & visual science.

[15]  H. Meissl,et al.  Effect of GABA and its antagonists, bicuculline and picrotoxin, on nerve cell discharges of the photosensory pineal organ of the frog, Rana esculenta , 1985, Brain Research.

[16]  G. Lázár,et al.  Cobalt injected into the right and left fasciculi retroflexes clarifies the organization of this pathway , 1985, The Journal of comparative neurology.

[17]  H. Meissl,et al.  Electrophysiological studies on neuronal transmission in the frog's photosensory pineal organ The effect of amino acids and biogenic amines , 1984, Vision Research.

[18]  T. Schwartz,et al.  A cDNA encoding a small common precursor for human pancreatic polypeptide and pancreatic icosapeptide. , 1984, The EMBO journal.

[19]  R. Northcutt,et al.  Nuclear organization of the bullfrog diencephalon , 1983, The Journal of comparative neurology.

[20]  W. Eldred,et al.  Multiple classes of photoreceptors and neurons in the frontal organ of Rana pipiens , 1981, The Journal of comparative neurology.

[21]  W. Eldred,et al.  Pineal photoreceptors: Evidence for a vertebrate visual pigment with two physiologically active states , 1978, Vision Research.

[22]  M. Maxwell Two rapid and simple methods used for the removal of resins from 1.0 μm thick epoxy sections , 1978, Journal of microscopy.

[23]  C. Lent,et al.  Parietal eye of the lizard: neuronal photoresponses and feedback from the pineal gland. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[24]  E. Dodt The Parietal Eye (Pineal and Parietal Organs) of Lower Vertebrates , 1973 .

[25]  D. Klein,et al.  Melatonin metabolism: neural regulation of pineal serotonin: acetyl coenzyme A N-acetyltransferase activity. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[26]  D. Hamasaki Interaction of excitation and inhibition in the stirnorgan of the frog. , 1970, Vision research.

[27]  R. Wurtman,et al.  Melatonin Synthesis in the Pineal Gland: Effect of Light Mediated by the Sympathetic Nervous System , 1964, Science.

[28]  E. Dodt,et al.  PHOTOSENSITIVITY OF A LOCALIZED REGION OF THE FROG DIENCEPHALON. , 1963, Journal of neurophysiology.

[29]  E. Dodt,et al.  Mode of action of pineal nerve fibers in frogs. , 1962, Journal of neurophysiology.