Scientific Understanding of Consciousness
Proprioceptive Neurons in Movement
Science 14 March 2014: Vol. 343 no. 6176 pp. 1256-1259
The stum Gene Is Essential for Mechanical Sensing in Proprioceptive Neurons
Bela S. Desai, Abhishek Chadha, Boaz Cook
Department of Molecular and Cellular Neuroscience, The Scripps Research Institute, La Jolla, CA 92037, USA.
Animal locomotion depends on proprioceptive feedback, which is generated by mechanosensory neurons. We performed a genetic screen for impaired walking in Drosophila and isolated a gene, stumble (stum). The Stum protein has orthologs in animals ranging from nematodes to mammals and is predicted to contain two transmembrane domains. Expression of the mouse orthologs of stum in mutant flies rescued their phenotype, which demonstrates functional conservation. Dendrites of stum-expressing neurons in legs were stretched by both flexion and extension of corresponding joints. Joint angles that induced dendritic stretching also elicited elevation of cellular Ca2+ levels—not seen in stum mutants. Thus, we have identified an evolutionarily conserved gene, stum, which is required for transduction of mechanical stimuli in a specific subpopulation of Drosophila proprioceptive neurons that sense joint angles.
Animal locomotion is achieved by coordination of motor activity according to proprioceptive mechanosensory inputs. In Drosophila, mechanosensation is mediated either by ciliated or multidendritic receptor neurons. Multidendritic neurons can respond to direct application of mechanical force to their membranes. It is less clear, however, how multidendritic mechanosensory neurons can be tuned to one mechanical modality, such as joint angle, and disregard other mechanical stimuli that may originate from external impacts or changes in the shape of muscles during contraction. In order to identify genes involved in proprioceptive sensation, we screened for uncoordination in a collection of ethyl methanesulfonate–mutagenized Drosophila lines.
Taken together, stum expression in mechanosensory neurons, Stum localization to the sensory dendrite, and the abolition of responses to stretching in the stum mutant suggest that stum has an essential role in mediating mechanical sensing in receptor neurons. Because the Stum protein in most species is very small and because Drosophila stum is expressed in limited populations of receptor neurons, we propose that stum is not the mechanically activated channel. Rather, stum may serve as an accessory module that is essential for the proper localization or function of the transduction channels.
The stretch-receptor neurons that express stum present an elegant engineering solution for generating specificity to the modality of mechanical stimulus. The distal part of their dendrite bifurcates into two branches whose tips are anchored to parts of the joint that shift their relative positions. Sensing the stretching only between the two dendritic tips may tune the nerve responses to joint motions and filter out the effect of irrelevant mechanical impacts. This specificity enables the sensory neuron to relay reliable proprioceptive information to the central nervous system.
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