Motion generation by Drosophila mechanosensory neurons

In Drosophila melanogaster, hearing is supported by mechanosensory neurons transducing sound-induced vibrations of the antenna. It is shown here that these neurons additionally generate motions that mechanically drive the antenna and tune it to relevant sounds. Motion generation in the Drosophila auditory system is betrayed by the auditory mechanics; the antenna of the fly nonlinearly alters its tuning as stimulus intensity declines and oscillates spontaneously in the absence of sound. The susceptibility of auditory motion generation to mechanosensory mutations shows that motion is generated by mechanosensory neurons. Motion generation depends on molecular components of the mechanosensory transduction machinery (NompA, NompC, Btv, and TilB), apparently involving mechanical activity of ciliated dendrites and microtubule-dependent motors. Hence, in analogy to vertebrate hair cells, the mechanosensory neurons of the fly serve dual, transducing, and actuating roles, documenting a striking functional parallel between the vertebrate cochlea and the ears of Drosophila.

[1]  Maurice J. Kernan,et al.  Genetically Similar Transduction Mechanisms for Touch and Hearing in Drosophila , 2000, The Journal of Neuroscience.

[2]  Otoacoustic Emissions from a Nonvertebrate Ear , 1998, Naturwissenschaften.

[3]  Peter G. Gillespie,et al.  Molecular basis of mechanosensory transduction , 2001, Nature.

[4]  D. Eberl,et al.  Feeling the vibes: chordotonal mechanisms in insect hearing , 1999, Current Opinion in Neurobiology.

[5]  R. Blandau,et al.  Observations on the solitary cilium of rabbit oviductal epithelium: its motility and ultrastructure. , 1985, The American journal of anatomy.

[6]  M. Göpfert,et al.  Biomechanics: Turning the key on Drosophila audition , 2001, Nature.

[7]  C. Zuker,et al.  Genetic dissection of mechanosensory transduction: Mechanoreception-defective mutations of drosophila , 1994, Neuron.

[8]  T. Matheson,et al.  Chordotonal Organs of Insects , 1998 .

[9]  N. Perrimon,et al.  A genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Andrew P Jarman,et al.  Studies of mechanosensation using the fly. , 2002, Human molecular genetics.

[11]  P. Dallos.  The active cochlea , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  H. C. BENNET-CLARK,et al.  Acoustics of Insect Song , 1971, Nature.

[13]  A. Hudspeth,et al.  Putting ion channels to work: mechanoelectrical transduction, adaptation, and amplification by hair cells. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[14]  A J Hudspeth,et al.  Negative hair-bundle stiffness betrays a mechanism for mechanical amplification by the hair cell. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[15]  A. J. Hudspeth,et al.  How the ear's works work , 1989, Nature.

[16]  Jason C. Caldwell,et al.  Towards a molecular understanding of Drosophila hearing. , 2002, Journal of neurobiology.

[17]  R. Greenspan,et al.  Courtship in Drosophila. , 2003, Annual review of genetics.

[18]  L. Robles,et al.  Mechanics of the mammalian cochlea. , 2001, Physiological reviews.

[19]  C. Zuker,et al.  A Drosophila mechanosensory transduction channel. , 2000, Science.

[20]  Daniel Robert,et al.  Active auditory mechanics in mosquitoes , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[21]  A J Hudspeth,et al.  Active hair-bundle movements can amplify a hair cell's response to oscillatory mechanical stimuli. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Jingchun Zhu,et al.  nompA Encodes a PNS-Specific, ZP Domain Protein Required to Connect Mechanosensory Dendrites to Sensory Structures , 2001, Neuron.

[23]  C. Zuker,et al.  Genetic approaches to mechanosensory transduction , 1995, Current Opinion in Neurobiology.

[24]  F. Varela,et al.  Evidence for active role of cilia in sensory transduction. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[25]  New Aspects of Cochlear Mechanics and Inner Ear Pathophysiology , 1990 .

[26]  New aspects of cochlear mechanics and inner ear pathophysiology , 1990 .

[27]  Renato Nobili,et al.  How well do we understand the cochlea? , 1998, Trends in Neurosciences.

[28]  M. Sato,et al.  THE EFFECT OF DIMETHYL SULFOXIDE ON THE NEURONAL EXCITABILITY AND CHOLINERGIC TRANSMISSION IN APLYSIA GANGLION CELLS * , 1975, Annals of the New York Academy of Sciences.

[29]  A. Hudspeth,et al.  Mechanical amplification of stimuli by hair cells , 1997, Current Opinion in Neurobiology.

[30]  M. Göpfert,et al.  The mechanical basis of Drosophila audition. , 2002, The Journal of experimental biology.

[31]  G. Theophilidis,et al.  Dimethylsulfoxide (DMSO) eliminates the response of the sensory neurones of an insect mechanoreceptor, the femoral chordotonal organ of Locusta migratoria, but blocks conduction of their sensory axons at much higher concentrations: A possible mechanism of analgesia , 1994, Neuroscience Letters.

[32]  G. Manley,et al.  Evidence for an active process and a cochlear amplifier in nonmammals. , 2001, Journal of neurophysiology.

[33]  J. C. Hall.  The mating of a fly. , 1994, Science.