Abstract
The auditory system of the cricket shows a remarkable level of anatomical plasticity in response to injury. Removal of the auditory organ deafferents several types of auditory neurons of the central nervous system. These neurons respond to the loss of input by sending dendrites across the midline, a boundary they typically respect, and forming synapses with the auditory afferents of the contralateral ear. This compensatory growth and synapse formation reinstates neuron-specific frequency tuning curves. Growth and branching after deafferentation are sexually dimorphic, with male growth rates being linear and female growth rates being nonlinear. Female dendrites stop growing and branching after only a few days, while male dendrites continue to grow steadily, becoming twice as long as females by 20 days after deafferentation. Exploration of the molecular basis of this compensatory plasticity has revealed a number of possible candidates, including semaphorins and a VAMP family member, neuronal synaptobrevin.
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Bingol B, Schuman EM (2005) Synaptic protein degradation by the ubiquitin proteasome system. Curr Opin Neurobiol 15:536–541
Born D, Rubel E (1985) Afferent influences on brain stem auditory nuclei of the chicken: neuron number and size following cochlea removal. J Comp Neurol 231:435–445
Bowen MF, Bollenbacher WE, Gilbert LI (1984) In vitro studies on the role of the brain and prothoracic glands in the pupal diapause of Manduca Sexta. J Exp Biol 108:9–24
Brodfuehrer PD, Hoy RR (1988) Effect of auditory deafferentation on the synaptic connectivity of a pair of identified interneurons in adult field crickets. J Neurobiol 19:17–38
Buschges A, Ramirez JM, Pearson KG (1992) Reorganization of sensory regulation of locust flight after partial deafferentation. J Neurobiol 23:31–43
Campbell D, Holt C (2001) Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis. Neuron 32:1013–1026
Cayre M, Strambi C, Strambi A, Charpin P, Ternaux JP (2000) Dual effect of ecdysone on adult cricket mushroom bodies. Eur J Neurosci 12:633–642
Cooke BM, Woolley CS (2005) Gonadal hormone modulation of dendrites in the mammalian CNS. J Neurobiol 64:34–46
De Winter F, Oudega M, Lankhorst A, Hamers F, Blits B, Ruitenberg M, Pasterkamp R, Gispen W, Verhaagen J (2002) Injury-induced class 3 semaphorin expression in the rat spinal cord. Exp Neurol 175:61–75
DeVoogd T, Nottebohm F (1981) Gonadal hormones induce dendritic growth in the adult avian brain. Science 214:202–204
Devor M (1975) Neuroplasticity in the rearrangement of olfactory tract fibers after neonatal transection in hamster. J Comp Neurol 166:49–72
Diatchenko L, Lau Y, Campbell A, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov E, Siebert P (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci U S A 93:6025–6030
Easter S, Purves D, Rakic P, Spitzer N (1985) The changing view of neural specificity. Science 230:507–511
Emoto K, He Y, Ye B, Grueber WB, Adler PN, Jan LY, Jan YN (2004) Control of dendritic branching and tiling by the Tricornered-kinase/Furry signaling pathway in Drosophila sensory neurons. Cell 119:245–256
Fenstermaker V, Chen Y, Ghosh A, Yuste R (2004) Regulation of dendritic length and branching by semaphorin 3A. J Neurobiol 58:403–412
Ferguson K, Long H, Cameron S, Chang W-T, Rao Y (2009) The conserved Ig superfamily member Turtle mediates axonal tiling in Drosophila. J Neurosci 29:14151–14159
Genikhovich G, Kurn U, Hemmrich G, Bosch T (2006) Discovery of genes expressed in Hydra embryogenesis. Dev Biol 289:466–481
Gontheir B, Koncina E, Satkauskas S, Perraut M, Roussel G, Aunis D, Kapfhammer J, Bagnard D (2009) A PKC-dependent recruitment of MMP-2 controls semaphorin-3A growth-promoting effect in cortical dendrites. PLoS ONE 4, e5099
Groh C, Meinertzhagen IA (2010) Brain plasticity in Diptera and Hymenoptera. Front Biosci (Scholar Ed) 2:268
Grueber WB, Graubard K, Truman JW (2001) Tiling of the body wall by multidendritic sensory neurons in Manduca sexta. J Comp Neurol 440:271–283
Grueber WB, Jan LY, Jan YN (2002) Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129:2867–2878
Hall GF, Cohen MJ (1988) The pattern of dendritic sprouting and retraction induced by axotomy of lamprey central neurons. J Neurosci 8:3584–3597
Harel NY, Strittmatter SM (2006) Can regenerating axons recapitulate developmental guidance during recovery from spinal cord injury? Nat Rev Neurosci 7:603–616
Hegde AN, DiAntonio A (2002) Ubiquitin and the synapse. Nat Rev Neurosci 3:854–861
Hickmott PW, Steen PA (2005) Large-scale changes in dendritic structure during reorganization of adult somatosensory cortex. Nat Neurosci 8:140–142
Horch HW, McCarthy SS, Johansen SL, Harris JM (2009) Differential gene expression during compensatory sprouting of dendrites in the auditory system of the cricket Gryllus bimaculatus. Insect Mol Biol 18:483–496
Horch HW, Sheldon E, Cutting CC, Williams CR, Riker DM, Peckler HR, Sangal RB (2011) Bilateral consequences of chronic unilateral deafferentation in the auditory system of the cricket gryllus bimaculatus. Dev Neurosci 33:21–37
Hoy RR, Nolen TG, Casaday GC (1985) Dendritic sprouting and compensatory synaptogenesis in an identified interneuron following auditory deprivation in a cricket. Proc Natl Acad Sci U S A 82:7772–7776
Ing B, Shteiman-Kotler A, Castelli M, Henry P, Pak Y, Stewart B, Boulianne G, Rotin D (2007) Regulation of commissureless by the ubiquitin ligase DNedd4 is required for neuromuscular synaptogenesis in Drosophila melanogaster. Mol Cell Biol 27:481–496
Jacobsson G, Piehl F, Meister B (1998) VAMP‐1 and VAMP‐2 gene expression in rat spinal motoneurones: differential regulation after neuronal injury. Eur J Neurosci 10:301–316
Jan YN, Jan L (2003) The control of dendrite development. Neuron 40:229–242
Kim S, Chiba A (2004) Dendritic guidance. Trends Neurosci 27:194–202
Kraft R, Levine RB, Restifo LL (1998) The steroid hormone 20-hydroxyecdysone enhances neurite growth of Drosophila mushroom body neurons isolated during metamorphosis. J Neurosci 18:8886–8899
Lakes R, Kalmring K, Engelhard KH (1990) Changes in the auditory system of locusts (Locusta migratoria and Schistocerca gregaria) after deafferentation. J Comp Physiol A 166:553–563
Liang P, Pardee AB (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257:967–971
Lomax M, Huang L, Cho Y, Gong T-W, Altschuler R (2000) Differential display and gene arrays to examine auditory plasticity. Hear Res 147:293–302
Luo L (2000) Rho GTPases in neuronal morphogenesis. Nat Rev Neurosci 1:173–180
Martinez-Arca S, Alberts P, Zahraoui A, Louvard D (2000) Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neurite outgrowth. J Cell Biol 149:889–899
Matheson SF, Levine RB (1999) Steroid hormone enhancement of neurite outgrowth in identified insect motor neurons involves specific effects on growth cone form and function. J Neurobiol 38:27–45
Matsumoto Y (2004) Context-dependent olfactory learning in an insect. Learn Mem 11:288–293
Matsumoto Y, Mizunami M (2000) Olfactory learning in the cricket Gryllus bimaculatus. J Exp Biol 203:2581–2588
Matsumoto Y, Mizunami M (2002) Lifetime olfactory memory in the cricket Gryllus bimaculatus. J Comp Physiol A 188:295–299
Matsumoto Y, Noji S, Mizunami M (2003) Time course of protein synthesis-dependent phase of olfactory memory in the cricket Gryllus bimaculatus. Zool Sci 20:409–416
Matsumoto Y, Unoki S, Aonuma H, Mizunami M (2006) Critical role of nitric oxide-cGMP cascade in the formation of cAMP-dependent long-term memory. Learn Mem 13:35–44
Maynard KR, McCarthy SS, Sheldon E, Horch HW (2007) Developmental and adult expression of semaphorin 2a in the cricket Gryllus bimaculatus. J Comp Neurol 503:169–181
McLean M, Edwards JS (1976) Target discrimination in regenerating insect sensory nerve. J Embryol Exp Morphol:36:19–39
Meinertzhagen IA (2001) Plasticity in the insect nervous system. In: Evans PD (ed) Advances in insect physiology, vol 28. Academic, New York, pp 84–167
Miele G, MacRae L, McBride D, Manson J, Clinton M (1998) Elimination of false positives generated through PCR re-amplification of differential display cDNA. BioTechniques 25:138–144
Morita A (2006) Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling. J Neurosci 26:2971–2980
Murphey RK (1986) The myth of the inflexible invertebrate: competition and synaptic remodelling in the development of invertebrate nervous systems. J Neurobiol 17:585–591
Murphey RK, Mendenhall B, Palka J, Edwards JS (1975) Deafferentation slows the growth of specific dendrites of identified giant interneurons. J Comp Neurol 159:407–418
Murphey RK, Johnson SE, Walthall WW (1981) The effects of transplantation and regeneration of sensory neurons on a somatotopic map in the cricket central nervous system. Dev Biol 88:247–258
Murphey RK, Bacon JP, Sakaguchi DS, Johnson SE (1983a) Transplantation of cricket sensory neurons to ectopic locations: arborizations and synaptic connections. J Neurosci 3:659–672
Murphey RK, Johnson SE, Sakaguchi DS (1983b) Anatomy and physiology of supernumerary cercal afferents in crickets: implications for pattern formation. J Neurosci 3:312–325
Myat A, Henry P, McCabe V, Flintoft L, Rotin D, Tear G (2002) Drosophila Nedd4, a ubiquitin ligase, is recruited by commissureless to control cell surface levels of the roundabout receptor. Neuron 35:447–459
Nakamura F, Ugahin K, Yamashita N, Okada T, Uchida Y, Taniguchi M, Ohshima T, Goshima Y (2009) Increased proximal bifurcation of CA1 pyramidal apical dendrites in sema3A mutant mice. J Comp Neurol 516:360–375
Nordeen KW, Killackey HP, Kitzes LM (1983) Ascending projections to the inferior colliculus following unilateral cochlear ablation in the neonatal gerbil, Meriones unguiculatus. J Comp Neurol 214:144–153
Palka J (1984) Precision and plasticity in the insect nervous system. Trends Neurosci 7:455–456
Palka J, Edwards JS (1974) The cerci and abdominal giant fibres of the house cricket, Acheta domesticus. II. Regeneration and effects of chronic deprivation. Proc R Soc B Biol Sci 185:105–121
Pallas SL, Hoy RR (1986) Regeneration of normal afferent input does not eliminate aberrant synaptic connections of an identified auditory interneuron in the cricket, Teleogryllus oceanicus. J Comp Neurol 248:348–359
Parks T (1979) Afferent influences on the development of the brain stem auditory nuclei of the chicken: otocyst ablation. J Comp Neurol 183:665–678
Pasterkamp RJ, Giger RJ (2009) Semaphorin function in neural plasticity and disease. Curr Opin Neurobiol 19:263–274
Pfister A, Johnson A, Ellers O, Horch HW (2013) Quantification of dendritic and axonal growth after injury to the auditory system of the adult cricket Gryllus bimaculatus. Front Physiol 3:367
Polleux F, Morrow T, Ghosh A (2000) Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404:567–573
Prugh J, Croce Della K, Levine RB (1992) Effects of the steroid hormone, 20-hydroxyecdysone, on the growth of neurites by identified insect motoneurons in vitro. Dev Biol 154:331–347
Purves D (1976) Competitive and non-competitive re-innervation of mammalian sympathetic neurones by native and foreign fibres. J Physiol 261:453–475
Purves D, Hume RI (1981) The relation of postsynaptic geometry to the number of presynaptic axons that innervate autonomic ganglion cells. J Neurosci 1:441–452
Raghuram H, Deb R, Nandi D, Balakrishnan R (2015) Silent katydid females are at higher risk of bat predation than acoustically signalling katydid males. Proc R Soc B Biol Sci 282:20142319
Roederer E, Cohen MJ (1983) Regeneration of an identified central neuron in the cricket. J Neurosci 3:1835–1847
Sanes JR, Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389–442
Schildberger K, Wohlers DW, Schmitz B, Kleindienst HU, Huber F (1986) Morphological and physiological changes in central auditory neurons following unilateral foreleg amputation in larval crickets. J Comp Physiol A 158:291–300
Schmitz B (1989) Neuroplasticity and phonotaxis in monaural adult female crickets (Gryllus bimaculatus de Geer). J Comp Physiol A: Neuroethol 164:343–358
Schmitz B, Kleindienst HU, Schildberger K, Huber F (1988) Acoustic orientation in adult, female crickets (Gryllus- Bimaculatus Degeer) after unilateral foreleg amputation in the larva. J Comp Physiol A-Sens Neural Behav Physiol 162:715–728
Schneider GE (1973) Early lesions of superior colliculus: factors affecting the formation of abnormal retinal projections. Brain Behav Evol 8:73–109
Scotto-Lomassese S, Strambi C, Strambi A, Aouane A, Augier R, Rougon G, Cayre M (2003) Suppression of adult neurogenesis impairs olfactory learning and memory in an adult insect. J Neurosci 23:9289–9296
Selverston AI, Kleindienst HU, Huber F (1985) Synaptic connectivity between cricket auditory interneurons as studied by selective photoinactivation. J Neurosci 5:1283–1292
Shankland M, Bentley D, Goodman CS (1982) Afferent innervation shapes the dendritic branching pattern of the Medial Giant Interneuron in grasshopper embryos raised in culture. Dev Biol 92:507–520
Shirasu M, Kimura K, Kataoka M, Takahashi M, Okajima S, Kawaguchi S, Hirasawa Y, Ide C, Mizoguchi A (2000) VAMP-2 promotes neurite elongation and SNAP-25A increases neurite sprouting in PC12 cells. Neuroscience 37:265–275
Soba P, Zhu S, Emoto K, Younger S, al E (2007) Drosophila sensory neurons require Dscam for dendritic self-avoidance and proper dendritic field organization. Neuron
Sugimura K, Yamamoto M, Niwa R, Satoh D, Goto S, Taniguchi M, Hayashi S, Uemura T (2003) Distinct developmental modes and lesion-induced reactions of dendrites of two clases of Drosophila sensory neurons. J Neurosci 23:3752–3760
Sutton MA, Schuman EM (2005) Local translational control in dendrites and its role in long-term synaptic plasticity. J Neurobiol 64:116–131
Tailby C, Wright LL, Metha AB, Calford MB (2005) Activity-dependent maintenance and growth of dendrites in adult cortex. Proc Natl Acad Sci U S A 102:4631–4636
Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123–1133
Tran TS, Rubio ME, Clem RL, Johnson D, Case L, Tessier-Lavigne M, Huganir RL, Ginty DD, Kolodkin AL (2009) Secreted semaphorins control spine distribution and morphogenesis in the postnatal CNS. :1–7
Truman JW, Reiss SE (1988) Hormonal regulation of the shape of identified motoneurons in the moth Manduca sexta. J Neurosci 8:765–775
Truman JW, Reiss SE (1995) Neuromuscular metamorphosis in the moth Manduca sexta: hormonal regulation of synapses loss and remodeling. J Neurosci 15:4815–4826
Trune DR (1982a) Influence of neonatal cochlear removal on the development of mouse cochlear nucleus: I. Number, size, and density of its neurons. J Comp Neurol 209:409–424
Trune DR (1982b) Influence of neonatal cochlear removal on the development of mouse cochlear nucleus: II. Dendritic morphometry of its neurons. J Comp Neurol 209:425–434
Vargas ME, Barres BA (2007) Why is Wallerian degeneration in the CNS so slow? Annu Rev Neurosci 30:153–179
Wan JS, Erlander MG (1997) Cloning differentially expressed genes by using differential display and subtractive hybridization. Methods Mol Biol 85:45–68
Weeks JC, Ernst-Utzschneider K (1989) Respecification of larval proleg motoneurons during metamorphosis of the tobacco hornworm, Manduca sexta: segmental dependence and hormonal regulation. J Neurobiol 20:569–592
Williams D (2005) Remodeling dendrites during insect metamorphosis – Williams – 2005 – Journal of Neurobiology – Wiley Online Library. J Neurobiol
Williams DW, Truman JW (2005) Remodeling dendrites during insect metamorphosis. J Neurobiol 64:24–33
Wohlers DW, Huber F (1982) Processing of sound signals by 6 types of neurons in the prothoracic ganglion of the cricket, Gryllus-campestris. J Comp Physiol 146:161–173
Wolf H, Büschges A (1997) Plasticity of synaptic connections in sensory-motor pathways of the adult locust flight system. J Neurophysiol 78:1276–1284
Xu X-ZS, Wes P, Chen H, Li H-S, Yu M, Morgan S, Liu Y, Montell C (1998) Retinal targets for calmodulin include proteins implicated in synaptic transmission. J Biol Chem 47:31297–31307
Yamashita N, Morita A, Uchida Y, Nakamura F, Usui H, Ohshima T, Taniguchi M, Honnorat J, Thomasset N, Takei K, Takahashi T, Kolattukudy P, Goshima Y (2007) Regulation of spine development by semaphorin3A through cyclin-dependent kinase 5 phosphorylation of collapsin response mediator protein 1. J Neurosci 27:12546–12554
Zeng V, Extavour CG (2012) ASGARD: an open-access database of annotated transcriptomes for emerging model arthropod species. Database (Oxford) 2012:bas048
Zeng V, Ewen-Campen B, Horch HW, Roth S, Mito T, Extavour CG (2013) Developmental gene discovery in a hemimetabolous insect: de novo assembly and annotation of a transcriptome for the cricket Gryllus bimaculatus Dearden PK, ed. PLoS ONE 8, e61479
Zera AJ, Zhao Z, Kaliseck K (2007) Hormones in the field: evolutionary endocrinology of Juvenile Hormone and Ecdysteroids in field populations of the wing-dimorphic cricket Gryllus firmus. Physiol Biochem Zool 80:592–606
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This project was supported by a grant from the National Institute of General Medical Sciences (8 P20 GM103423-12) from the National Institutes of Health.
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Horch, H.W., Pfister, A., Ellers, O., Johnson, A.S. (2017). Plasticity in the Cricket Central Nervous System. In: Horch, H., Mito, T., Popadić, A., Ohuchi, H., Noji, S. (eds) The Cricket as a Model Organism. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56478-2_8
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