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Open Access Research article

Monoaminergic modulation of photoreception in ascidian: evidence for a proto-hypothalamo-retinal territory

Florian Razy-Krajka17, Euan R Brown28, Takeo Horie3456, Jacques Callebert4, Yasunori Sasakura3, Jean-Stéphane Joly1, Takehiro G Kusakabe5 and Philippe Vernier1*

Author Affiliations

1 Neurobiology and Development, UPR3294, Institut de Neurobiologie Alfred Fessard, Centre National de la Recherche Scientifique, Gif-sur-Yvette, 91190, France

2 Department of Animal Physiology and Evolution, Stazione Zoologica Anton Dohrn, Naples, 80121, Italy

3 Shimoda Marine Research Center, University of Tsukuba, 5-10-1 Shimoda, Shizuoka 415-0025, Japan

4 Laboratoire de biochimie, Hôpital Lariboisière, Paris, 75010, France

5 Department of Biology, Faculty of Science and Engineering, Konan University, Kobe 658-8501, Japan

6 Japan Science and Technology Agency, PREST, 4-1-8 Honcho, Kawaguchi, Saitama 332-0012, Japan

7 New York University Center for Developmental Genetics, Department of Biology, New York University, 1009 Silver Center, 100 Washington Square East, New York, NY 10003-6688, USA

8 Institute of Biological Chemistry, Biophysics and Bioengineering, School of Engineering and Physical Sciences, Heriot-Watt University, Edinburgh EH14 4AS, UK

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BMC Biology 2012, 10:45  doi:10.1186/1741-7007-10-45

Published: 29 May 2012

Abstract

Background

The retina of craniates/vertebrates has been proposed to derive from a photoreceptor prosencephalic territory in ancestral chordates, but the evolutionary origin of the different cell types making the retina is disputed. Except for photoreceptors, the existence of homologs of retinal cells remains uncertain outside vertebrates.

Methods

The expression of genes expressed in the sensory vesicle of the ascidian Ciona intestinalis including those encoding components of the monoaminergic neurotransmission systems, was analyzed by in situ hybridization or in vivo transfection of the corresponding regulatory elements driving fluorescent reporters. Modulation of photic responses by monoamines was studied by electrophysiology combined with pharmacological treatments.

Results

We show that many molecular characteristics of dopamine-synthesizing cells located in the vicinity of photoreceptors in the sensory vesicle of the ascidian Ciona intestinalis are similar to those of amacrine dopamine cells of the vertebrate retina. The ascidian dopamine cells share with vertebrate amacrine cells the expression of the key-transcription factor Ptf1a, as well as that of dopamine-synthesizing enzymes. Surprisingly, the ascidian dopamine cells accumulate serotonin via a functional serotonin transporter, as some amacrine cells also do. Moreover, dopamine cells located in the vicinity of the photoreceptors modulate the light-off induced swimming behavior of ascidian larvae by acting on alpha2-like receptors, instead of dopamine receptors, supporting a role in the modulation of the photic response. These cells are located in a territory of the ascidian sensory vesicle expressing genes found both in the retina and the hypothalamus of vertebrates (six3/6, Rx, meis, pax6, visual cycle proteins).

Conclusion

We propose that the dopamine cells of the ascidian larva derive from an ancestral multifunctional cell population located in the periventricular, photoreceptive field of the anterior neural tube of chordates, which also gives rise to both anterior hypothalamus and the retina in craniates/vertebrates. It also shows that the existence of multiple cell types associated with photic responses predates the formation of the vertebrate retina.