From embryo to adult: Persistent neurogenesis and apoptotic cell death shape the lobster deutocerebrum

Journal of Neuroscience

Volumn 19, Issue 9, 1999, Pages 3472-3485

  Harzsch, Steffen ^a   Miller, Julie ^b   Benton, Jeannie ^b   Beltz, Barbara ^b  

^a BIELEFELD UNIVERSITY   (Germany)

^b WELLESLEY COLLEGE   (United States)

Author keywords

Apoptosis; BrdU; Crustacea; Deutocerebrum; Homarus americanus; Neurogenesis; Phosphorylated histone H3; Plasticity; Synapsin; TUNEL

Indexed keywords

ADULTHOOD; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN; CELL PROLIFERATION; CELL SHAPE; EMBRYO DEVELOPMENT; FEMALE; IMMUNOHISTOCHEMISTRY; INTERNEURON; LOBSTER; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROPIL; NONHUMAN; OLFACTORY NERVE; PRIORITY JOURNAL; SMELLING; SYNAPTOGENESIS;

EID: 0033135538     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-09-03472.1999     Document Type: Article

References (104)

1. Ajiro K, Yoda K, Utsumi K, Nishikawa Y (1996) Alteration of cell cycle-dependent histone phosphorylation by okadaic acid. J Biol Chem 271:13197-13201.
2. Alvarez-Buylla A, Kirn JR (1997) Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J Neurobiol 33:585-601.
3. Alvarez-Buylla A, Temple S (1998) Stem cells in the developing and adult nervous system. J Neurobiol 36:105-110.
4. Beltz BS (1999) The distribution and functional anatomy of amine-containing neurons in decapod crustaceans. Microsc Res Tech 44:105-120.
5. Beltz BS, Helluy S, Ruchhoeft ML, Gammil LS (1992) Aspects of the embryology and neural development of the American lobster. J Exp Zool 261:288-297.
6. Ben-Sasson SA, Sherman Y, Gavrieli Y (1995) Identification of dying cells-in situ staining. In: Methods in cell biology: cell death, Vol 46 (Schwartz LM, Osborne BA, eds), pp 29-40. New York: Academic.
7. Benton J, Huber R, Ruchhoeft M, Helluy S, Beltz B (1997) Serotonin depletion by 5,7-dihydroxytryptamine alters deutocerebral development in the lobster, Homarus americanus. J Neurobiol 33:357-373.
8. Bieber M, Fuldner D (1979) Brain growth during the adult stage of a holometabolous insect. Naturwissenschaften 66:426.
9. Blaustein DN, Derby CD, Simmons RB, Beall AC (1988) Structure of the brain and medulla terminalis of the spiny lobster Panulirus argus and the crayfish Procambarus clarkii with an emphasis on olfactory centers. J Crustac Biol 8:493-519.
10. Boeckh J, Tolbert LP (1993) Synaptic organization and development of the antennal lobe in insects. Microsc Res Tech 24:260-280.
11. Bulloch AGM, Jones PG (1988) Modulation of neurite outgrowth by intact and axotomized neurons of Helisoma. Am Zool 28:1123-1134.
12. Bulloch AGM, Ridgway RL (1989) Neuronal plasticity in the adult invertebrate nervous system. J Neurobiol 20:295-311.
13. Burrows M (1996) The neurobiology of an insect brain. New York: Oxford UP.
14. Calof AL, Mumm JS, Rim PC, Shou J (1998) The neuronal stem cell of the olfactory epithelium. J Neurobiol 36:190-205.
15. Cameron HA, McKay R (1998) Stem cells and neurogenesis in the adult brain. Curr Opin Neurobiol 8:677-680.
16. Campos-Ortega JA (1993) Early neurogenesis in Drosophila melanogaster. In: The development of Drosophila melanogaster (Bate M, Martinez-Arias A, eds), pp 1091-1130. Plainview, NY: Cold Spring Harbor Laboratory.
17. Cayre M, Strambi C, Strambi A (1994) Neurogenesis in an adult insect brain and its hormonal control. Nature 368:57-59.
18. Cayre M, Strambi C, Charpin P, Augier R, Meyer MR, Edwards JS, Strambi A (1996) Neurogenesis in adult insect mushroom bodies. J Comp Neurol 371:300-310.
19. Charmantier G, Charmantier M, Aiken DE (1991) Metamorphosis of the lobster Homarus (Decapoda): a review. J Crustac Biol 11:481-495.
20. Davis RL, Han KA (1996) Mushrooming mushroom bodies. Curr Biol 6:146-148.
21. Derby CD, Blaustein DN (1988) Morphological and physiological characterization of individual olfactory interneurons connecting the brain and eyestalk ganglia of the crayfish. J Comp Physiol [A] 163:777-794.
22. Doe CQ, Skeath JB (1996) Neurogenesis in the insect central nervous system. Curr Opin Neurobiol 6:18-24.
23. Dohle W (1976) Die Bildung und Differenzierung des postnauplialen Keimstreifs von Diastylis rathkei (Crustacea, Cumacea). II. Die Differenzierung und Musterbildung des Ektoderms. Zoomorphologie 84:235-277.
24. Dohle W (1997) Myriapod-insect relationships as opposed to an insect-crustacean sister group relationship. In: Arthropod relationships (Fortey RA, Thomas RH, eds), pp 305-315. London: Chapman and Hall.
25. Dohle W, Scholtz G (1997) How far does cell lineage influence cell fate specification in crustacean embryos? Semin Cell Dev Biol 8:379-390.
26. Dolbeare F (1996) Bromodeoxyuridine: a diagnostic tool in biology and medicine. III. Proliferation in normal, injured and diseased tissue, growth factors, differentiation, DNA replication sites and in situ hybridization. Histochem J 28:531-575.
27. Eriksson PS, Perfilieva E, Björk-Eriksson, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult hippocampus. Nat Med 4:1313-1317.
28. Fahrbach SE, Giray T, Robinson GE (1995a) Volume changes in the mushroom bodies of adult honey bee queens. Neurobiol Learn Mem 63:181-191.
29. Fahrbach SE, Strande JL, Robinson GE (1995b) Neurogenesis is absent in the brains of adult honey bees and does not explain behavioral neuroplasticity. Neurosci Lett 197:145-148.
30. French KA, Kristan Jr WB (1994) Cell-cell interactions that modulate neuronal development in the leech. J Neurobiol 25:640-651.
31. Gage FH, Kempermann G, Palmer TD, Peterson DA, Ray J (1998) Multipotent progenitor cells in the adult dentate gyrus. J Neurobiol 36:249-266.
32. García-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A (1998) Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol 36:234-248.
33. Gerberding M (1997) Germ band formation and early neurogenesis of Leptodora kindti (Cladocera): first evidence for neuroblasts in the entomostracan crustaceans. Invertebr Reprod Dev 32:93-73.
34. Goldman SA (1997) Comparative strategies of subependymal neurogenesis in the adult forebrain. In: Isolation, characterization and utilization of CNS stem cells (Gage FH, Christen Y, eds), pp 43-66. Berlin: Springer.
35. Goldman SA (1998) Adult neurogenesis: from canaries to the clinic. J Neurobiol 36:267-286.
36. Goodman CS, Doe CQ (1993) Embryonic development of the Drosophila central nervous system. In: The development of Drosophila melanogaster (Bate M, Martinez-Arias A, eds), pp 1131-1207. Plainview, NY: Cold Spring Harbor Laboratory.
37. Gronenberg W, Heeren S, Hölldobler B (1996) Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J Exp Biol 199:2011-2019.
38. Gurley LR, D'Anna JA, Barham SS, Deaven LL, Tobey RA (1978) Histone phosphorylation and chromatin structure during mitosis in Chinese hamster cells. Eur J Biochem 84:1-15.
39. Hammer M, Menzel R (1995) Learning and memory in the honeybee. J Neurosci 15:1617-1630.
40. Harzsch S, Dawirs R (1993) On the morphology of the central nervous system in larval stages of Carcinus maenas L. (Decapoda, Brachyura). Helgol Meeresunters 47:61-79.
41. Harzsch S, Dawirs RR (1994) Neurogenesis in larval stages of the spider crab Hyas araneus (Decapoda, Brachyura): proliferation of neuroblasts in the ventral nerve cord. Roux's Arch Dev Biol 204:93-100.
42. Harzsch S, Dawirs RR (1996) Neurogenesis in the developing crab brain: postembryonic generation of neurons persists beyond metamorphosis. J Neurobiol 29:384-398.
43. Harzsch S, Schmidt M (1996) Brain development in adult crayfish includes the generation of new deutocerebral interneurons. Verh Dtsch Zool Ges 89:50.
44. Harzsch S, Anger K, Dawirs RR (1997) Immunocytochemical detection of acetylated α-tubulin and Drosophila synapsin in the embryonic crustacean nervous system. Int J Dev Biol 41:477-484.
45. Harzsch S, Miller J, Benton J, Dawirs R, Beltz B (1998) Development of the thoracic neuromeres in two crustaceans with different styles of metamorphic development. J Exp Biol 210:2465-2479.
46. Harzsch S, Benton J, Dawirs RR, 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.
47. Heisenberg M (1994) Central brain functions in insects: genetic studies on the mushroom bodies and central complex in Drosophila. Fortschr Zool 39:61-79.
48. Heisenberg M, Heusipp M, Wanke C (1995) Structural plasticity in the Drosophila brain. J Neurosci 15:1951-1960.
49. Helluy SM, Beltz BS (1991) Embryonic development of the American lobster (Homarus americanus): quantitative staging and characterization of an embryonic molt cycle. Biol Bull 180:355-371.
50. Helluy SM, Sandeman R, Beltz B (1993) Comparative brain ontogeny of the crayfish and clawed lobster-implications of direct and larval development. J Comp Neurol 335:343-354.
51. Helluy SM, Ruchhoeft ML, Beltz BS (1995) Development of the olfactory and accessory lobes in the American lobster: an allometric analysis and its implications for the deutocerebral structure of decapods. J Comp Neurol 357:433-445.
52. Helluy SM, Benton JL, Langworthy KA, Ruchhoeft ML, Beltz BS (1996) Glomerular organization in developing olfactory and accessory lobes of American lobsters: stabilization of numbers and increase in size after metamorphosis. J Neurobiol 29:459-472.
53. Hickmott PW, Carew TJ (1991) An autoradiographic analysis of neurogenesis in juvenile Aplysia californica. J Neurobiol 22:313-326.
54. Hildebrand JG (1996) Olfactory control of behavior in moths: central processing of odor information and the functional significance of olfactory glomeruli. J Comp Physiol [A] 178:5-19.
55. Jacobson MD, Weil M, Raff MC (1997) Programmed cell death in animal development. Cell 88:347-354.
56. Kerr JFR, Gobé GC, Winterford CM, Harmon BV (1995) Anatomical methods in cell death. In: Methods in cell biology: cell death, Vol 46 (Schwartz LM, Osborne BA, eds), pp 1-28. New York: Academic.
57. Keshishian H, Broadie K, Chiba A, Bate M (1996) The Drosophila neuromuscular junction: a model system for studying synaptic development and function. Annu Rev Neurosci 19:545-575.
58. Klagges BRE, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E (1996) Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154-3165.
59. Langworthy K, Helluy S, Benton J, Beltz B (1997) Amines and peptides in the brain of the American lobster: immunocytochemical localization patterns and implications for brain function. Cell Tissue Res 288:191-206.
60. Levine RB, Morton DB, Restifo LL (1995) Remodeling of the insect nervous system. Curr Opin Neurobiol 5:28-35.
61. Luskin MB (1998) Neuroblasts of the postnatal mammalian forebrain: their phenotype and fate. J Neurobiol 36:221-233.
62. Macagno ER, Gao WQ, Baptista CA, Passani MB (1990) Competition or inhibition? Developmental strategies in the establishment of peripheral projections by leech neurons. J Neurobiol 21:107-119.
63. Marois R, Carew TJ (1990) The gastropod nervous system in metamorphosis. J Neurobiol 21:1053-1071.
64. Mellon DF, Alones V (1993) Cellular organization and growth-related plasticity of the crayfish olfactory midbrain. Microsc Res Tech 24:231-259.
65. Mellon Jr D, Alones V (1994) Identification of three classes of multiglomerular, broad-spectrum neurons in the crayfish olfactory midbrain by correlated patterns of electrical activity and dendritic arborization. J Comp Physiol 177:55-71.
66. Mellon Jr DF, Alones VE (1997) Response properties of higher level neurons in the central olfactory pathway of the crayfish. J Comp Physiol [A] 181:205-216.
67. Menzel R, Müller U (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu Rev Neurosci 19:379-404.
68. 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.
69. Negoescu A, Lorimier P, Labat-Moleur F, Drouet C, Robert C, Guillermet C, Brambilla C, Brambilla E (1996) In situ apoptotic cell labeling by the TUNEL method: improvement and evaluation on cell preparations. J Histochem Cytochem 44:959-968.
70. Oland LA, Tolbert LP (1996) Multiple factors shape development of olfactory glomeruli: insights from an insect model system. J Neurobiol 30:92-109.
71. Orona E, Ache BW (1992) Physiological and pharmacological evidence for histamine as a neurotransmitter in the olfactory CNS of the spiny lobster. Brain Res 590:136-143.
72. Orona E, Battelle BA, Ache BW (1990) Immunohistochemical and biochemical evidence for the putative inhibitory neurotransmitter histamine and GABA in lobster olfactory lobes. J Comp Neurol 294:633-646.
73. Ray J, Palmer TD, Suhonen J, Takahashi J, Gage F H (1997) Neurogenesis in the adult brain: lessons learned from the studies of progenitor cells from the embryonic and adult nervous system. In: Isolation, characterization and utilization of CNS stem cells. (Gage FH, Christen Y, eds), pp 129-150. Springer: Berlin.
74. Reichert H, Boyan G (1997) Building a brain: developmental insights in insects. Trends Neurosci 20:258-263.
75. Sandeman D, Sandeman R, Derby C, Schmidt M (1992) Morphology of the brain of crayfish, crabs, and spiny lobsters: a common nomenclature for homologous structures. Biol Bull 183:304-326.
76. Sandeman D, Beltz B, Sandeman R (1995a) Crayfish brain interneurons that converge with serotonin giant cells in accessory lobe glomeruli. J Comp Neurol 352:263-279.
77. Sandeman DC, Sandeman RE (1994) Electrical responses and synaptic connections of giant serotonin-immunoreactive neurons in crayfish olfactory and accessory lobes. J Comp Neurol 341:130-144.
78. Sandeman R, Sandeman D (1990) Development and identified neural systems in the crayfish brain. In: Frontiers in crustacean neuroscience (Kennedy K, ed), pp 498-508. Basel: Birkhäuser.
79. Sandeman RE, Sandeman DC (1996) Pre- and postembryonic development, growth and turnover of olfactory receptor neurones in crayfish antennules. J Exp Biol 199:2409-2418.
80. Sandeman RE, Watson AHD, Sandeman DC (1995b) Ultrastructure of the synaptic terminals of the dorsal giant serotonin-IR neuron and deutocerebral commissure interneurons in the accessory and olfactory lobes of the crayfish. J Comp Neurol 361:617-632.
81. Sandeman RE, Clarke D, Sandeman D, Manly M (1998) Growth-related and antennular amputation-induced changes in the olfactory centers of crayfish brain. J Neurosci 18:6195-6209.
82. Sanders EJ, Wride MA (1996) Ultrastructural identification of apoptotic nuclei using the TUNEL technique. Histochem J 28:275-281.
83. Schmidt M (1997) Continuous neurogenesis in the olfactory brain of adult shore crabs, Carcinus maenas. Brain Res 762:131-143.
84. Schmidt M, Ache BW (1992) Antennular projections to the midbrain of the spiny lobster. II. Sensory innervation of the olfactory lobe. J Comp Neurol 318:291-303.
85. Schmidt M, Ache BW (1996) Processing of antennular input in the brain of the spiny lobster, Panulirus argus. II. The olfactory pathway. J Comp Physiol [A] 178:605-628.
86. Schmidt M, Ache BW (1997) Immunocytochemical analysis of glomerular regionalization and neuronal diversity in the olfactory deutocerebrum of the spiny lobster. Cell Tissue Res 286:541-563.
87. Schmidt M, Harzsch S (1999) Comparative analysis of neurogenesis in the central olfactory pathway of adult decapod crustaceans by in vivo BrdU-labeling. Biol Bull, in press.
88. Scholtz G (1992) Cell lineage studies in the crayfish Cherax destructor (Crustacea, Decapoda): germ band formation, segmentation and early neurogenesis. Roux's Arch Dev Biol 202:36-48.
89. Scholtz G (1995) Head segmentation in crustacea - an immunocytochemical study. Zoology 98:104-114.
90. Sigg D, Thompson CM, Mercer AR (1997) Activity-dependent changes to the brain and behavior of the honey bee, Apis mellifera (L.). J Neurosci 17:7148-7156.
91. Strausfeld NJ, Buschbeck EK, Gomez RS (1995) The arthropod mushroom body: its functional roles, evolutionary enigmas and mistaken identities. In: The nervous system of invertebrates: an evolutionary and comparative approach (Breidbach O, Kutsch W, eds), pp 349-381. Basel: Birkhäuser.
92. Technau GM (1984) Fiber numbers in the mushroom bodies of adult Drosophila melanogaster depends on age, sex, and experience. J Neurogenet 1:113-126.
93. Technau G, Heisenberg M (1982) Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 295:405-406.
94. Truman JW (1992) Developmental neuroethology of insect metamorphosis. J Neurobiol 23:1404-1422.
95. Wachowiak M, Ache BW (1997) Dual inhibitory pathways mediated by GABA and histaminergic interneurons in the lobster olfactory lobe. J Comp Physiol [A] 180:357-372.
96. Wachowiak M, Diebel CE, Ache BW (1996) Functional organization of olfactory processing in the accessory lobe of the spiny lobster. J Comp Physiol [A] 178:211-226.
97. Wachowiak M, Diebel CE, Ache BW (1997) Local interneurons define functionally distinct regions within lobster olfactory glomeruli. J Exp Biol 200:989-1001.
98. Weeks JC, Wood ER (1996) Short- and long-term modification of reflex function during learning and metamorphosis in Manduca. Biol Bull 191:62-69.
99. White E (1996) Life, death, and the pursuit of apoptosis. Genes Dev 10:1-15.
100. Whitington P (1996) Evolution of neural development in arthropods. Semin Cell Dev Biol 7:605-614.
101. Winnington AP, Napper RM, Mercer AR (1996) Structural plasticity of identified glomeruli in the antennal lobes of adult worker honey bee. J Comp Neurol 365:479-490.
102. Withers GS, Fahrbach SE, Robinson GE (1993) Selective neuroanatomical plasticity and division of labour in the honeybee. Nature 364:238-239.
103. Withers GS, Fahrbach SE, Robinson GE (1995) Effects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees. J Neurobiol 26:130-144.
104. Wolszon L (1995) Cell-cell interactions define the innervation patterns of central leech neurons during development. J Neurobiol 27:335-352.