Two Visual Processing Pathways Are Targeted by Gonadotropin-Releasing Hormone in the Retina

In fish the terminal nerve is comprised of a group of cells with somata adjacent to the olfactory bulb and processes that extend both anteriorly to the olfactory mucosa and posteriorly to the telencephalon. In teleost fish an additional group of axons extends along the optic tract and delivers putative neuromodulators to the retina. One peptide – gonadotropin-releasing hormone (GnRH) – has been implicated as a prime candidate neuromodulator based on electrophysiological evidence that exogenous application influences neural activity. Here we describe the expression patterns of two GnRH receptor subtypes in the retina of a teleost fish, Astatotilapia (Haplochromis) burtoni. The type 1 GnRH receptor (GnRH-R1) was expressed in cells of the amacrine cell layer – where lateral inputs affect the flow of visual information from photoreceptors to the brain – and in a distribution and location pattern similar to dopaminergic interplexiform cells. Immunohistochemical labeling of GnRH fibers revealed varicosities along terminal nerve axons near the amacrine cell layer and near cells immunoreactive for tyrosine hydroxylase, a dopaminergic cell marker. This finding supports an existing model that the terminal nerve forms synapses with dopaminergic interplexiform cells. Surprisingly, the type 2 GnRH receptor (GnRH-R2) was abundantly expressed in ganglion cells, which lie along the direct pathway of visual information to the brain. These data suggest that GnRH from the TN could broadly influence processing of retinal signals both in lateral processing circuits through GnRH-R1 and in the vertical throughput pathway through GnRH-R2.

[1]  H. Wagner,et al.  Localization and function of dopamine in the adult vertebrate retina , 1992, Neurochemistry International.

[2]  R. Delay,et al.  Neuromodulatory Effects of Gonadotropin Releasing Hormone on Olfactory Receptor Neurons , 2000, The Journal of Neuroscience.

[3]  M. A. Zandbergen,et al.  Evolutionary development of three gonadotropin-releasing hormone (GnRH) systems in vertebrates , 2002, Brain Research Bulletin.

[4]  S. White,et al.  Social regulation of gonadotropin-releasing hormone. , 2002, The Journal of experimental biology.

[5]  J. Dunn,et al.  The effect of surgical isolation or ablation of the medial basal hypothalamus on serum prolactin levels in male rats. , 1976, Neuroendocrinology.

[6]  Nasotemporal asymmetry during teleost retinal growth: preserving an area of specialization. , 1999, Journal of neurobiology.

[7]  N. Illing,et al.  Gonadotropin-releasing hormone receptor in the teleost Haplochromis burtoni: structure, location, and function. , 2001, Endocrinology.

[8]  Neville N. Osborne,et al.  Neurobiology of the Inner Retina , 1989, NATO ASI Series.

[9]  D. L. Meyer,et al.  Centrifugal Phe-Met-Arg-Phe-NH2-like immunoreactive innervation of the retina in a non-teleost bony fish, Lepisosteus osseus , 1999, Neuroscience Letters.

[10]  O. Umino,et al.  Dopamine release from interplexiform cells in the retina: effects of GnRH, FMRFamide, bicuculline, and enkephalin on horizontal cell activity , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  R. Northcutt,et al.  Silver lampreys (Ichthyomyzon unicuspis) lack a gonadotropin‐releasing hormone‐ and FMRFamide‐immunoreactive terminal nerve , 1996, The Journal of comparative neurology.

[12]  S. Basinger,et al.  FMRFamide-immunoreactive retinopetal fibers in the frog, Rana pipiens: demonstration by lesion and immunocytochemical techniques , 1988, Brain Research.

[13]  B. Claas,et al.  Centrifugal innervation of the retina by luteinizing hormone releasing hormone (LHRH)-immunoreactive telencephalic neurons in teleostean fishes , 2004, Cell and Tissue Research.

[14]  W. Stell,et al.  The goldfish nervus terminalis: a luteinizing hormone-releasing hormone and molluscan cardioexcitatory peptide immunoreactive olfactoretinal pathway. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[15]  O. Kah,et al.  Evolutionary aspects of GnRHs, GnRH neuronal systems and GnRH receptors in teleost fish. , 2004, General and comparative endocrinology.

[16]  J. Dowling,et al.  Dopamine modulates the kinetics of ion channels gated by excitatory amino acids in retinal horizontal cells. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[17]  W. Stell,et al.  Efferent Projections to the Goldfish Retina , 1989 .

[18]  W. Stell,et al.  Choline acetyltransferase immunoreactivity suggests that ganglion cells in the goldfish retina are not cholinergic , 1986, The Journal of comparative neurology.

[19]  O. Kah,et al.  Cloning, Tissue Distribution, and Central Expression of the Gonadotropin-Releasing Hormone Receptor in the Rainbow Trout (Oncorhynchus mykiss)1 , 2000, Biology of reproduction.

[20]  W. Stell,et al.  Gonadotropin-releasing hormone (GnRF), Molluscan cardioexcitatory peptide (FMRFamide), enkephalin and related neuropeptides affect goldfish retinal ganglion cell activity , 1986, Brain Research.

[21]  Y. Oka Gonadotropin-releasing hormone (GnRH) cells of the terminal nerve as a model neuromodulator system , 1992, Neuroscience Letters.

[22]  W. Stell,et al.  Electron microscopic study of immunocytochemically labeled centrifugal fibers in the goldfish retina , 1990, The Journal of comparative neurology.

[23]  Y. Jan,et al.  Peptidergic transmitters in synaptic boutons of sympathetic ganglia , 1980, Nature.

[24]  Dopamine D2 receptor‐mediated modulation of rod‐cone coupling in the Xenopus retina , 1996, The Journal of comparative neurology.

[25]  B Ehinger,et al.  The interplexiform cell system - I. Synapses of the dopaminergic neurons of the goldfish retina , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[26]  R. Fernald,et al.  Gonadotropin-Releasing Hormone Genes: Phylogeny, Structure, and Functions , 1999, Frontiers in Neuroendocrinology.

[27]  S. White,et al.  Three gonadotropin-releasing hormone genes in one organism suggest novel roles for an ancient peptide. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[28]  John E. Dowling,et al.  Centrifugal fibres synapse on dopaminergic interplexiform cells in the teleost retina , 1987, Nature.

[29]  L. S. Demski,et al.  Terminal nerve complex. , 1993, Acta anatomica.

[30]  P. Iuvone,et al.  NEUROTRANSMITTERS AND NEUROMODULATORS IN THE RETINA: REGULATION, INTERACTIONS, AND CELLULAR EFFECTS , 1986 .

[31]  L. S. Demski The Evolution of Neuroanatomical Substrates of Reproductive Behavior: Sex Steroid and LHRH-Specific Pathways Including the Terminal Nerve , 1984 .

[32]  R. Marc Spatial organization of neurochemically classified interneurons of the goldfish retina—I. Local patterns , 1982, Vision Research.