Social domination increases neuronal survival in the brain of juvenile crayfish Procambarus clarkii

Journal of Experimental Biology

Volumn 210, Issue 8, 2007, Pages 1311-1324

  Song, Cha Kyong ^a,b   Johnstone, Laurel M ^a,c   Schmidt, Manfred ^a   Derby, Charles D ^a   Edwards, Donald H ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b Ewha Womans University   (South Korea)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

Body growth; Crustacea; Dominance hierarchy; Neurogenesis; Olfaction; Proliferation

Indexed keywords

BROXURIDINE;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; BRAIN; CELL SURVIVAL; COMPARATIVE STUDY; CRAYFISH; CYTOLOGY; IMMUNOHISTOCHEMISTRY; INTERNEURON; MORPHOMETRICS; ODOR; PHYSIOLOGY; SOCIAL DOMINANCE;

ANALYSIS OF VARIANCE; ANIMALS; ASTACOIDEA; BODY WEIGHTS AND MEASURES; BRAIN; BROMODEOXYURIDINE; CELL SURVIVAL; IMMUNOHISTOCHEMISTRY; INTERNEURONS; SMELL; SOCIAL DOMINANCE;

ASTACOIDEA; CRUSTACEA; PROCAMBARUS CLARKII;

EID: 34248592978     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.02758     Document Type: Article

References (65)

1. Altman, J. (1962). Are new neurons formed in the brains of adult mammals? Science 135, 1127-1128.
2. Beltz, B. S. and Sandeman, D. C. (2003). Regulation of life-long neurogenesis in the decapod crustacean brain. Arthropod Struct. Dev. 32, 39-60.
3. Beltz, B. S., Benton, J. L. and Sullivan, J. M. (2001). Transient uptake of serotonin by newborn olfactory projection neurons. Proc. Natl. Acad. Sci. USA 98, 12730-12735.
4. Beltz, B. S., Kordas, K., Lee, M. M., Long, J. B., Benton, J. L. and Sandeman, D. C. (2003). Ecological, evolutionary, and functional correlates of sensilla number and glomerular density in the olfactory system of decapod crustaceans. J. Comp. Neurol. 455, 260-269.
5. Benton, J. L. and Beltz, B. S. (2002). Patterns of neurogenesis in the midbrain of embryonic lobsters differ from proliferation in the insect and the crustacean ventral nerve cord. J. Neurobiol. 53, 57-67.
6. Bovbjerg, R. V. (1953). Dominance order in the crayfish Orconectes virilis (Hagen). Physiol. Zool. 26, 173-178.
7. Breithaupt, T. and Eger, P. (2002). Urine makes the difference: chemical communication in fighting crayfish made visible. J. Exp. Biol. 205, 1221-1231.
8. Brown, J., Cooper-Kuhn, C. M., Kempermann, G., van Praag, H., Winkler, J., Gage, F. H. and Kuhn, H. G. (2003). Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur. J. Neurosci. 17, 2042-2046.
9. Cayre, M., Strambi, C. and Strambi, A. (1994). Neurogenesis in an adult insect brain and its hormonal control. Nature 368, 57-59.
10. Cayre, M., Malaterre, J., Strambi, C., Charpin, P., Ternaux, J. P. and Strambi, A. (2001). Short- and long-chain natural polyamines play specific roles in adult cricket neuroblast proliferation and neuron differentiation in vitro. J. Neurobiol. 48, 315-324.
11. Cayre, M., Malaterre, J., Scotto-Lomassese, S., Strambi, C. and Strambi, A. (2002). The common properties of neurogenesis in the adult brain: from invertebrates to vertebrates. Comp. Biochem. Physiol. 132B, 1-15.
12. Demers, D. M., Metcalf, A. E., Talbot, P. and Hyman, B. C. (1996). Multiple lobster tubulin isoforms are encoded by a simple gene family. Gene 171, 185-191.
13. Derby, C. D. and Steullet, P. (2001). Why do animals have so many receptors? The role of multiple chemosensors in animal perception. Biol. Bull. 200, 211-215.
14. Edwards, D. H., Issa, F. A. and Herberholz, J. (2003). The neural basis of dominance hierarchy formation in crayfish. Microsc. Res. Tech. 60, 369-376.
15. Goergen, E. M., Bagay, L. A., Rehm, K., Benton, J. L. and Beltz, B. S. (2002). Orcadian control of neurogenesis. J. Neurobiol. 53, 90-95.
16. Gould, E., McEwen, B. S., Tanapat, P., Galea, L. A. and Fuchs, E. (1997). Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J. Neurosci. 17, 2492-2498.
17. Gould, E., Tanapat, P., McEwen, B. S., Flugge, G. and Fuchs, E. (1998). Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl. Acad. Sci. USA 95, 3168-3171.
18. Gould, E., Beylin, A., Tanapat, P., Reeves, A. and Shors, T. J. (1999). Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 2, 260-265.
19. Hansen, A. and Schmidt, M. (2001). Neurogenesis in the central olfactory pathway of the adult shore crab Carcinus maenas is controlled by sensory afferents. J. Comp. Neurol. 441, 223-233.
20. Hansen, A. and Schmidt, M. (2004). Influence of season and environment on adult neurogenesis in the central olfactory pathway of the shore crab, Carcinus maenas. Brain Res. 1025, 85-97.
21. Harzsch, S., Benton, J., Dawirs, R. R. and Beltz, B. (1999). A new look at embryonic development of the visual system in decapod crustaceans: neuropil formation, neurogenesis, and apoptotic cell death. J. Neurobiol. 39, 294-306.
22. Hendzel, M. J., Wei, Y., Mancini, M. A., van Hooser, A., Ranalli, T., Brinkley, B. R., Bazett-Jones, D. P. and Allis, C. D. (1997). Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348-360.
23. Herberholz, J., Sen, M. M. and Edwards, D. H. (2003). Parallel changes in agonistic and non-agonistic behaviors during dominance hierarchy formation in crayfish. J. Comp. Physiol. A 189, 321-325.
24. Horner, A. J., Weissburg, M. J. and Derby, C. D. (2004). Dual antennular chemosensory pathways can mediate orientation by Caribbean spiny lobsters in naturalistic flow conditions. J. Exp. Biol. 207, 3785-3796.
25. Issa, F. A., Adamson, D. J. and Edwards, D. H. (1999). Dominance hierarchy formation in juvenile crayfish, Procambarus clarkii. J. Exp. Biol. 202, 3497-3506.
26. Johnson, M. E. and Atema, J. (2005). The olfactory pathway for individual recognition in the American lobster Homarus americanus. J. Exp. Biol. 208, 2865-2872.
27. Karplus, I. and Barki, A. (2004). Social control of growth in the redclaw crayfish, Cherax quadricarinatus: testing the sensory modalities involved. Aquaculture 242, 321-333.
28. Kempermann, G., Brandon, E. P. and Gage, F. H. (1998). Environmental stimulation of 129/SvJ mice causes increased cell proliferation and neurogenesis in the adult dentate gyrus. Curr. Biol. 8, 939-942.
29. Kozorovitskiy, Y. and Gould, E. (2004). Dominance hierarchy influences adult neurogenesis in the dentate gyrus. J. Neurosci. 24, 6755-6759.
30. Lledo, P. M. and Saghatelyan, A. (2005). Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci. 28, 248-254.
31. Linser, P. J., Trapido-Rosenthal, H. G. and Orona, E. (1997). Glutamine synthetase is a glial-specific marker in the olfactory regions of the lobster (Panulirus argus) nervous system. Glia 20, 275-283.
32. Lowe, M. E. (1956). Dominance-subordinance relationships in the crayfish Cambarellus shufeldtii. Tulane Stud. Zool. 4, 139-170.
33. Malatynska, E. and Knapp, R. J. (2005). Dominant-submissive behavior as models of mania and depression. Neurosci. Biobehav. Rev. 29, 715-737.
34. Ming, G. L. and Song, H. (2005). Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 28, 223-250.
35. Mykles, D. L., Haire, M. F. and Skinner, D. M. (2000). Immunocytochemical localization of actin and tubulin in the integument of land crab (Gecarcinus lateralis) and lobster (Homarus americanus). J. Exp. Zool. 286, 329-342.
36. Pham, K., Nacher, J., Hof, P. R. and McEwen, B. S. (2003). Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci. 17, 879-886.
37. Pravosudov, V. V. and Omanska, A. (2005). Dominance-related changes in spatial memory are associated with changes in hippocampal cell proliferation rates in mountain chickadees. J. Neurobiol. 62, 31-41.
38. Rhodes, C. P. and Holdich, D. M. (1979). On size and sexual dimorphism in Australopotamobious pallipes (Lereboullet). Aquaculture 17, 345-358.
39. Rochefort, C., Gheusi, G., Vincent, J. D. and Lledo, P. M. (2002). Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J. Neurosci. 22, 2679-2689.
40. Sandeman, D., Sandeman, R., Derby, C. and Schmidt, M. (1992). Morphology of the brain of crayfish, crabs, and spiny lobsters: A common nomenclature for homologous structures. Biol. Bull. 183, 304-326.
41. Sandeman, R. and Sandeman, D. (2000). 'Impoverished' and 'enriched' living conditions influence the proliferation and survival of neurons in crayfish brain. J. Neurobiol. 45, 215-226.
42. Sandeman, R. and Sandeman, D. (2003). Development, growth, and plasticity in the crayfish olfactory system. Microsc. Res. Tech. 60, 266-277.
43. Sandeman, R., Clarke, D., Sandeman, D. and Manly, M. (1998). Growth-related and antennular amputation-induced changes in the olfactory centers of crayfish brain. J. Neurosci. 18, 6195-6206.
44. Schmidt, M. (1997). Continuous neurogenesis in the olfactory brain of adult shore crabs, Carcinus maenas. Brain Res. 762, 131-143.
45. Schmidt, M. (2001). Neuronal differentiation and long-term survival of newly generated cells in the olfactory midbrain of the adult spiny lobster, Panulirus argus. J. Neurobiol. 48, 181-203.
46. Schmidt, M. (2002). Adult neurogenesis in the central olfactory pathway of decapod crustaceans. In The Crustacean Nervous System (ed. K. Wiese), pp. 433-453. Berlin: Springer Verlag.
47. Schmidt, M. and Demuth, S. (1998). Neurogenesis in the central olfactory pathway of adult decapod crustaceans. Ann. N. Y. Acad. Sci. 855, 277-280.
48. Schmidt, M. and Harzsch, S. (1999). Comparative analysis of neurogenesis in the central olfactory pathway of adult decapod crustaceans by in vivo BrdU labeling. Biol. Bull. 196, 127-136.
49. Scotto-Lomassese, S., Strambi, C., Aouane, A., Strambi, A. and Cayre, M. (2002). Sensory inputs stimulate progenitor cell proliferation in an adult insect brain. Curr. Biol. 12, 1001-1005.
50. Scotto-Lomassese, S., Strambi, C., Strambi, A., Aouane, A., Augier, R., Rougon, G. and Cayre, M. (2003). Suppression of adult neurogenesis impairs olfactory learning and memory in an adult insect. J. Neurosci. 23, 9289-9296.
51. Shors, T. J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T. and Gould, E. (2001). Neurogenesis in the adult is involved in the formation of trace memories. Nature 410, 372-376.
52. Siegel, S. and Castellan, N. J. (1988). Nonparametric Statistics. New York: McGraw-Hill.
53. Song, C.-K., Johnstone, L. M., Schmidt, M., Derby, C. D. and Edwards, D. H. (2005). Social experience changes neurogenesis in the brain of juvenile crayfish Procambarus clarkii. Abstract Viewer and Itinerary Planner. Washington DC: Society for Neuroscience, Program No. 754.12. Online.
54. Song, C.-K., Herberholz, J. and Edwards, D. H. (2006). The effects of social experience on the behavioural response to unexpected touch in crayfish. J. Exp. Biol. 209, 1355-1363.
55. Sullivan, J. M. and Beltz, B. S. (2001). Neural pathways connecting the deutocerebrum and lateral protocerebrum in the brains of decapod crustaceans. J. Comp. Neurol. 441, 9-22.
56. Sullivan, J. M. and Beltz, B. S. (2005a). Integration and segregation of inputs to higher-order neuropils of the crayfish brain. J. Comp. Neurol. 481, 118-126.
57. Sullivan, J. M. and Beltz, B. S. (2005b). Newborn cells in the adult crayfish brain differentiate into distinct neuronal types. J. Neurobiol. 65, 157-170.
58. Sullivan, J. M., Benton, J. L., Sandeman, D. C. and Beltz, B. S. (2006). Adult neurogenesis: a common strategy across diverse species. J. Comp. Neurol. 500, 574-584.
59. van Praag, H., Christie, B. R., Sejnowski, T. J. and Gage, F. H. (1999). Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. USA 96, 13427-13431.
60. Varadaraj, K., Kumari, S. S. and Skinner, D. M. (1997). Molecular characterization of four members of the alpha-tubulin gene family of the Bermuda land crab Gecarcinus lateralis. J. Exp. Zool. 278, 63-77.
61. Warren, R. H. (1984). Axonal microtubules of crayfish and spiny lobster nerve cords are decorated with a heat-stable protein of high molecular weight. J. Cell Sci. 71, 1-15.
62. Warren, R. H. and Rubin, R. W. (1978). Microtubules and actin in giant nerve fibers of the spiny lobster, Panulirus argus. Tissue Cell 10, 687-697.
63. Wei, Y., Mizzen, C. A., Cook, R. G., Gorovsky, M. A. and Allis, C. D. (1998). Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc. Natl. Acad. Sci. USA 95, 7480-7484.
64. Wei, Y., Yu, L., Bowen, J., Gorovsky, M. A. and Allis, C. D. (1999). Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 97, 99-109.
65. Zulandt Schneider, R. A., Schneider, R. W. S. and Moore, P. A. (1999). Recognition of dominance status by chemoreception in the red swamp crayfish, Procambarus clarkii. J. Chem. Ecol. 25, 781-794.