Abstract
The evolutionary origin of novelties is a central problem in biology. At a cellular level this requires, for example, molecularly resolving how brainstem motor neurons change their innervation target from muscle fibers (branchial motor neurons) to neural crest-derived ganglia (visceral motor neurons) or ear-derived hair cells (inner ear and lateral line efferent neurons). Transplantation of various tissues into the path of motor neuron axons could determine the ability of any motor neuron to innervate a novel target. Several tissues that receive direct, indirect, or no motor innervation were transplanted into the path of different motor neuron populations in Xenopus laevis embryos. Ears, somites, hearts, and lungs were transplanted to the orbit, replacing the eye. Jaw and eye muscle were transplanted to the trunk, replacing a somite. Applications of lipophilic dyes and immunohistochemistry to reveal motor neuron axon terminals were used. The ear, but not somite-derived muscle, heart, or liver, received motor neuron axons via the oculomotor or trochlear nerves. Somite-derived muscle tissue was innervated, likely by the hypoglossal nerve, when replacing the ear. In contrast to our previous report on ear innervation by spinal motor neurons, none of the tissues (eye or jaw muscle) was innervated when transplanted to the trunk. Taken together, these results suggest that there is some plasticity inherent to motor innervation, but not every motor neuron can become an efferent to any target that normally receives motor input. The only tissue among our samples that can be innervated by all motor neurons tested is the ear. We suggest some possible, testable molecular suggestions for this apparent uniqueness.
Highlights
Synaptic contacts likely originated in evolution as connections between sensory-motor neurons and muscle tissue in diploblastic animals, such as jellyfish, [1] forming a monosynaptic reflex network from sensory cell directly to effector cell
Vertebrate motor neurons have evolved to form synapses on a variety of targets originating from developmentally different sources including mesoderm-derived muscle fibers, epithelial placode-derived neurosensory cells and neurons, and neural crest-derived autonomic ganglia [9,10,11,12]
We were able to demonstrate the ability of the oculomotor nerve, and in one case the trochlear nerve, to extend motor neuron axons to hair cells of an ear transplanted to the orbit to replace the eye
Summary
Synaptic contacts likely originated in evolution as connections between sensory-motor neurons and muscle tissue in diploblastic animals, such as jellyfish, [1] forming a monosynaptic reflex network from sensory cell directly to effector cell. Vertebrate motor (efferent) neurons have evolved to form synapses on a variety of targets originating from developmentally different sources including mesoderm-derived muscle fibers, epithelial placode-derived neurosensory cells and neurons (i.e. inner ear hair cells and neurons), and neural crest-derived autonomic ganglia [9,10,11,12]. Among all cranial motor neurons, motor neurons of the facial nerve are unique in that they innervate targets from three different developmental origins: branchial arch-derived muscle by branchial motor neurons, neural crest-derived ganglia by visceral motor neurons, and placodally-derived inner ear hair cells by inner ear efferents [4]. Given the ability of some motor neurons to innervate targets from a variety of origins, the possibility exists that there is conservation of the core molecular machinery that allows for recognition of a particular target by multiple motor neuron types
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