Professor Clare Baker

Neurogenic placodes and the neural crest: development and evolution of the vertebrate peripheral sensory nervous system

Neurogenic placodes and the neural crest are two distinct embryonic cell populations that are crucial for the development of the vertebrate head. Together, they give rise to the whole peripheral nervous system, i.e., all the sensory receptor cells, neurons (nerve cells) and glial cells (nerve-support cells) located outside the brain and spinal cord. Neural crest cells also build much of the craniofacial skeleton.

Neurogenic placodes (paired patches of thickened surface ectoderm in the embryonic head) give rise to the paired peripheral sense organs: the olfactory placodes form the olfactory receptor neurons in the nose that detect smells; the otic placodes form the inner ears, in which fluid movement (due to sound waves or head motion) stimulates mechanosensory hair cells, giving us our senses of hearing and balance; and a series of lateral line placodes forms the lateral line system of fish and aquatic-stage amphibians, in which mechanosensory hair cells (very like those in the inner ear), distributed in lines over the head and flank, detect local water movement for e.g. prey/predator detection and schooling behaviour. Neurogenic placodes also form the hormone-producing cells of the anterior pituitary gland, the eye lenses, and most of the peripheral sensory neurons of the head, collected in discrete cranial sensory ganglia.

Neural crest cells migrate out of the developing brain and spinal cord: they give rise to all the other neurons and all glial cells of the peripheral nervous system, plus a wide variety of other cell types including pigment cells, most of the cartilages and bones of the face and skull, and the dentine-producing cells of teeth.

Development and evolution of electroreceptors

Land vertebrates, as well as frogs and most modern bony fish, have lost one of the most ancient vertebrate senses, the ability to detect weak electric fields in water, used for finding prey and for orientation. Electroreceptors are modified hair cells, distributed in fields of "ampullary organs" on either side of the lateral lines of mechanosensory hair cells. They are found in all major aquatic vertebrate groups, including jawless fish (lampreys), cartilaginous fish (sharks, rays), primitive bony fish (e.g. sturgeon, paddlefish), and even some amphibians (salamanders). Although the ancestors of teleosts (modern bony fish) lost electroreceptors, so that most of these fish cannot detect electric fields, electroreceptors seem to have been independently "re-invented" at least twice in two different groups of teleosts, including catfish and "electric fish". Very little is known about electroreceptor development. We are investigating the embryological origins of electroreceptors, and the genes underlying their formation, in a wide range of vertebrate groups including lamprey, skate, sturgeon and salamander, plus teleost fish lineages in which electroreception evolved independently (catfish and weakly electric teleosts: knifefishes and mormyrids).

Development of olfactory ensheathing glia

Using grafting techniques in chicken embryos and genetic lineage-tracing in mice, we discovered that olfactory ensheathing cells (OECs, which ensheath and protect olfactory nerve fibres) are derived from the neural crest, like all other peripheral glial cells, and not from the olfactory placodes as previously thought (Barraud et al., 2010, PNAS). Excitingly, OECs can promote nerve repair when transplanted into the damaged spinal cord, but it has proved difficult to isolate them in large enough numbers from the nose for effective therapy. Neural crest stem cells persist in adult skin and hair follicles, and it is possible to isolate these stem cells and grow them in the lab. The next step is to work out how to turn these stem cells into OECs: to do this, we need to investigate how this process happens normally in the developing embryo. In recent years we have investigated this question, as well as the role of OECs during the embryonic development of the olfactory system.

Current research team

Martin Minařík (Leverhulme Trust-funded Research Associate)

Surjit Singh Saini (Leverhulme Trust-funded Research Associate)

Szymon Macuda (final-year undergraduate project student)

Collaborators

Marianne Bronner, Caltech, Pasadena, CA, USA
Roman Franěk, University of South Bohemia, Czech Republic
Jason Gallant, Michigan State University, MI, USA
Andrew Gillis, Marine Biological Laboratory, Woods Hole, MA, USA
Henrik Kaessmann, University of Heidelberg, Germany
Frank Kirschbaum, Humboldt University of Berlin, Germany
Raj Ladher, NCBS, Bangalore, India
Michael Markham, University of Oklahoma, OK, USA
David McCauley, University of Oklahoma, OK, USA
Martin Pšenička, University of South Bohemia, Czech Republic
Tatjana Piotrowski, Stowers Institute for Medical Research, MO, USA
Ralph Tiedemann, University of Potsdam, Germany
Harold Zakon, UT Austin, TX, USA