Co-expression of VAL- and TMT-opsins uncovers ancient photosensory interneurons and motorneurons in the vertebrate brain

PLoS Biol. 2013;11(6):e1001585. doi: 10.1371/journal.pbio.1001585. Epub 2013 Jun 11.

Abstract

The functional principle of the vertebrate brain is often paralleled to a computer: information collected by dedicated devices is processed and integrated by interneuron circuits and leads to output. However, inter- and motorneurons present in today's vertebrate brains are thought to derive from neurons that combined sensory, integration, and motor function. Consistently, sensory inter-motorneurons have been found in the simple nerve nets of cnidarians, animals at the base of the evolutionary lineage. We show that light-sensory motorneurons and light-sensory interneurons are also present in the brains of vertebrates, challenging the paradigm that information processing and output circuitry in the central brain is shielded from direct environmental influences. We investigated two groups of nonvisual photopigments, VAL- and TMT-Opsins, in zebrafish and medaka fish; two teleost species from distinct habitats separated by over 300 million years of evolution. TMT-Opsin subclasses are specifically expressed not only in hypothalamic and thalamic deep brain photoreceptors, but also in interneurons and motorneurons with no known photoreceptive function, such as the typeXIV interneurons of the fish optic tectum. We further show that TMT-Opsins and Encephalopsin render neuronal cells light-sensitive. TMT-Opsins preferentially respond to blue light relative to rhodopsin, with subclass-specific response kinetics. We discovered that tmt-opsins co-express with val-opsins, known green light receptors, in distinct inter- and motorneurons. Finally, we show by electrophysiological recordings on isolated adult tectal slices that interneurons in the position of typeXIV neurons respond to light. Our work supports "sensory-inter-motorneurons" as ancient units for brain evolution. It also reveals that vertebrate inter- and motorneurons are endowed with an evolutionarily ancient, complex light-sensory ability that could be used to detect changes in ambient light spectra, possibly providing the endogenous equivalent to an optogenetic machinery.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aging / metabolism
  • Amino Acid Sequence
  • Animals
  • Brain / cytology*
  • Brain / metabolism*
  • Brain / radiation effects
  • Cell Line
  • Cell Nucleus / metabolism
  • Cell Nucleus / radiation effects
  • Choline O-Acetyltransferase / metabolism
  • Conserved Sequence
  • Humans
  • Interneurons / cytology
  • Interneurons / metabolism*
  • Interneurons / radiation effects
  • Larva / metabolism
  • Light
  • Mice
  • Molecular Sequence Data
  • Motor Neurons / cytology
  • Motor Neurons / metabolism*
  • Motor Neurons / radiation effects
  • Opsins / chemistry
  • Opsins / genetics
  • Opsins / metabolism*
  • Oryzias / metabolism
  • Photoreceptor Cells, Vertebrate / cytology
  • Photoreceptor Cells, Vertebrate / metabolism*
  • Photoreceptor Cells, Vertebrate / radiation effects
  • Phylogeny
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Sequence Analysis, Protein
  • Vertebrates / metabolism*
  • Zebrafish / metabolism

Substances

  • Opsins
  • RNA, Messenger
  • Choline O-Acetyltransferase

Grant support

PhD fellowship of the Boehringer Ingelheim Foundation (http://www.bifonds.de/fellowships-grants/phd-fellowships.html) to RMF; funds of the Max F. Perutz Laboratories/University of Vienna, the research platform “Marine Rhythms of Life” of the University of Vienna (http://www.univie.ac.at/en/) to KTR; a FWF (www.fwf.ac.at) START award (#AY0041321) to KTR and a HFSP (www.hfsp.org) research grant (#RGY0082/2010) to KTR. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.