Morphological and physiological changes in central auditory neurons following unilateral foreleg amputation in larval crickets

Summary1.In view of the surprising recent demonstration that developmentally one-eared female crickets can track sound sources (Huber et al. 1984), we have looked for correlates in the morphological and physiological properties of auditory interneurons of these animals. One foreleg was amputated in the 3rd/4th or penultimate (8/9th) larval instar; in both cases the leg regenerated without developing a functional ear. In the adult stage, these animals were studied first for their phonotactic behavior and then by intracellular recording and staining; three types of auditory interneurons in the prothoracic ganglion were identified: the omega neuron ON1, and the ascending neurons AN1 and AN2.2.Of these three neuron types, those that normally receive excitatory input from the side now deafferented send dendrites across the midline of the ganglion, along specific pathways, to end in the auditory neuropil of the intact side (Figs. 1–4).3.The new connections are functional, as shown by the responses of the neurons to synthesized calling songs presented to the remaining ear. With respect to the copying of chirp structure, threshold curves and intensity characteristics, these neurons respond like cells in intact animals that are presented with the same stimulus on the side ipsilateral to the main input region of the neurons (Figs. 2–4). The implication is that in animals with one ear missing, functional pathways within the central nervous system are reorganized, resulting in better orientation of one-eared animals.

[1]  John Thorson,et al.  Auditory behavior of the cricket , 2004, Journal of Comparative Physiology A.

[2]  Dendritic sprouting and compensatory synaptogenesis in an identified interneuron follow auditory deprivation in a cricket. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[3]  E. Holst Die Arbeitsweise des Statolithen-apparates Bei Fischen , 2004, Zeitschrift für vergleichende Physiologie.

[4]  Franz Huber,et al.  Intracellular recording and staining of cricket auditory interneurons (Gryllus campestris L.,Gryllus bimaculatus DeGeer) , 1978, Journal of comparative physiology.

[5]  R. Sperry CHEMOAFFINITY IN THE ORDERLY GROWTH OF NERVE FIBER PATTERNS AND CONNECTIONS. , 1963, Proceedings of the National Academy of Sciences of the United States of America.

[6]  A. Moiseff,et al.  Sensitivity to ultrasound in an identified auditory interneuron in the cricket: a possible neural link to phonotactic behavior , 1983, Journal of comparative physiology.

[7]  Axon growth from limb motoneurons in the locust embryo: the effect of target limb removal on the path taken out of the central nervous system. , 1982, Developmental biology.

[8]  John T. Schmidt The formation of retinotectal projections , 1982, Trends in Neurosciences.

[9]  R. J. Biggin Pattern re-establishment--transplantation and regeneration of the leg in the cricket Teleogryllus commodus (Walker). , 1981, Journal of embryology and experimental morphology.

[10]  R. Hoy,et al.  Auditory interneurons in the cricketTeleogryllus oceanicus: Physiological and anatomical properties , 2004, Journal of comparative physiology.

[11]  Franz Huber,et al.  Processing of sound signals by six types of neurons in the prothoracic ganglion of the cricket,Gryllus campestris L. , 1982, Journal of comparative physiology.

[12]  T. Page Regeneration of the optic tracts and circadian pacemaker activity in the cockroachLeucophaea maderae , 1983, Journal of comparative physiology.

[13]  A. Selverston,et al.  Synaptic connectivity between cricket auditory interneurons as studied by selective photoinactivation , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Competition controls the growth of an identified axonal arborization. , 1984, Science.

[15]  J. Camhi,et al.  Responses to wind recorded from the cercal nerve of the cockroachPeriplaneta americana , 1979, Journal of comparative physiology.

[16]  R. Levine,et al.  Mechanisms responsible for changes observed in response properties of partially deafferented insect interneurons. , 1980, Journal of neurophysiology.

[17]  J. Thorson,et al.  Auditory behavior of the cricket , 2004, Journal of Comparative Physiology A.

[18]  J. Denburg Elimination of inappropriate axonal branches of regenerating cockroach motor neurons as detected by the retrograde transport of horseradish peroxidase conjugated wheat germ agglutinin , 1982, Brain Research.

[19]  E. Ball,et al.  Structure and development of the auditory system in the prothoracic leg of the cricket Teleogryllus commodus (walker) , 1974, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[20]  W. Precht Neuronal Operations in the Vestibular System , 1978, Studies of Brain Function.

[21]  K. Schildberger,et al.  Temporal selectivity of identified auditory neurons in the cricket brain , 2004, Journal of Comparative Physiology A.

[22]  R. Murphey,et al.  Recovery from deafferentation by cricket interneurons after reinnervation by their peripheral field , 1976, The Journal of comparative neurology.

[23]  Barbara Schmitz Phonotaxis inGryllus campestris L. (Orthoptera, Gryllidae) , 1985, Journal of Comparative Physiology A.

[24]  Topographical organization of the auditory pathway within the prothoracic ganglion of the cricket Gryllus campestris L. , 1985, Cell and Tissue Research.

[25]  R. D. Clark Structural and functional changes in an identified cricket neuron after separation from the soma. I. Structural changes , 1976, The Journal of comparative neurology.

[26]  R. Murphey,et al.  The effects of transplantation and regeneration of sensory neurons on a somatotopic map in the cricket central nervous system. , 1981, Developmental biology.

[27]  J. Palka,et al.  Deafferentation slows the growth of specific dendrites of identified giant interneurons , 1975, The Journal of comparative neurology.

[28]  A. V. Popov,et al.  Auditory interneurons in the prothoracic ganglion of the cricket, gryllus bimaculatus deGeer , 2004, Journal of comparative physiology.

[29]  A. V. Popov,et al.  Auditory interneurones in the prothoracic ganglion of the cricket,Gryllus bimaculatus , 1982, Journal of comparative physiology.

[30]  K. G. Hill,et al.  Functional development of the auditory system of the cricket,Teleogryllus commodus , 1978, Journal of comparative physiology.

[31]  Roger W. Sperry,et al.  OPTIC NERVE REGENERATION WITH RETURN OF VISION IN ANURANS , 1944 .

[32]  Analysis of the cricket auditory system by acoustic stimulation using a closed sound field , 1981, Journal of comparative physiology.

[33]  J. Palka,et al.  The cerci and abdominal giant fibres of the house cricket, Acheta domesticus. II. Regeneration and effects of chronic deprivation , 1974, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[34]  N. Vardi,et al.  Functional recovery from lesions in the escape system of the cockroach , 2004, Journal of comparative physiology.

[35]  G. Boyan,et al.  Auditory neurones in the brain of the cricket Gryllus bimaculatus (De Geer): Ascending interneurones , 1982 .

[36]  J. Westin Responses to wind recorded from the cercal nerve of the cockroachPeriplaneta americana , 1979, Journal of comparative physiology.