全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2007 

Thermal Disruption of Mushroom Body Development and Odor Learning in Drosophila

DOI: 10.1371/journal.pone.0001125

Full-Text   Cite this paper   Add to My Lib

Abstract:

Environmental stress (nutritive, chemical, electromagnetic and thermal) has been shown to disrupt central nervous system (CNS) development in every model system studied to date. However, empirical linkages between stress, specific targets in the brain, and consequences for behavior have rarely been established. The present study experimentally demonstrates one such linkage by examining the effects of ecologically-relevant thermal stress on development of the Drosophila melanogaster mushroom body (MB), a conserved sensory integration and associative center in the insect brain. We show that a daily hyperthermic episode throughout larval and pupal development (1) severely disrupts MB anatomy by reducing intrinsic Kenyon cell (KC) neuron numbers but has little effect on other brain structures or general anatomy, and (2) greatly impairs associative odor learning in adults, despite having little effect on memory or sensory acuity. Hence, heat stress of ecologically relevant duration and intensity can impair brain development and learning potential.

References

[1]  Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108: Suppl 3511–533.
[2]  Weinstock M (2001) Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 65: 427–451.
[3]  Welberg LA, Seckl JR (2001) Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol 13: 113–128.
[4]  Mattson SN, Riley EP (1998) A review of the neurobehavioral deficits in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol Clin Exp Res 2: 279–294.
[5]  Roebuck TM, Mattson SN, Riley EP (1998) A review of the neuroanatomical findings in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol Clin Exp Res 2: 339–244.
[6]  Milunsky A, Ulcickas M, Rothman KJ, Willett W, Jick SS, et al. (1992) Maternal heat exposure and neural-tube defects. J Am Med Assoc 268: 882–885.
[7]  Suarez L, Felkner M, Hendricks K (2004) The effect of fever, febrile illnesses, and heat exposures on the risk of neural tube defects in a Texas-Mexico border population. Birth Defects Res A Clin Mol Teratol 70: 815–819.
[8]  Rhees RW, Al-Saleh HN, Kinghorn EW, Fleming DE, Lephart ED (1999) Relationship between sexual behavior and sexually dimorphic structures in the anterior hypothalamus in control and prenatally stressed male rats. Brain Res Bull 50: 193–199.
[9]  Feder ME (1997) Necrotic fruit: A novel model system for thermal ecologists. J Therm Biol 22: 1–9.
[10]  Roberts SP, Feder ME (1999) Natural hyperthermia and expression of the heat shock protein Hsp70 affect developmental abnormalities in Drosophila melanogaster. Oecologia 121: 323–329.
[11]  de Belle JS, Kanzaki R (1999) Protocerebral Olfactory Processing. In: Hansson BS, editor. Insect Olfaction. Stuttgart: Springer. pp. 243–281.
[12]  Zars T (2000) Behavioral functions of the insect mushroom bodies. Curr Opin Neurobiol 10: 790–795.
[13]  Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4: 266–275.
[14]  Tautz J, Maier S, Groh C, R?ssler W, Brockmann A (2003) Behavioral performance in adult honey bees is influenced by the temperature experienced during their pupal development. Proc Natl Acad Sci U S A 100: 7343–7347.
[15]  Groh C, Tautz J, R?ssler W (2004) Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development. Proc Natl Acad Sci U S A 101: 4268–4273.
[16]  Groh C, Ahrens D, R?ssler W (2006) Environment- and age-dependent plasticity of synaptic complexes in the mushroom bodies of honeybee queens. Brain Behav Evol 68: 1–14.
[17]  Technau GM (1984) Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J Neurogenet 1: 113–126.
[18]  Balling A, Technau GM, Heisenberg M (1987) Are the structural changes in adult Drosophila mushroom bodies memory traces? Studies on biochemical learning mutants. J Neurogenet 4: 65–73.
[19]  Heisenberg M, Heusipp M, Wanke C (1995) Structural plasticity in the Drosophila brain. J Neurosci 15: 1951–1960.
[20]  Barth M, Heisenberg M (1997) Vision affects mushroom bodies and central complex in Drosophila melanogaster. Learn Mem 4: 219–229.
[21]  Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol. 12: 633–638.
[22]  Technau GM, Heisenberg M (1982) Neural reorganisation during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 295: 405–407.
[23]  Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto D (1997) The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124: 761–771.
[24]  Armstrong JD, de Belle JS, Wang Z, Kaiser K (1998) Metamorphosis of the mushroom bodies; large-scale rearrangements of the neural substrates for associative learning and memory in Drosophila. Learn Mem 5: 102–114.
[25]  Lee T, Lee A, Luo L (1999) Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126: 4065–4076.
[26]  Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415.
[27]  Yang MY, Armstrong JD, Vilinsky I, Strausfeld NJ, Kaiser K (1995) Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15: 45–54.
[28]  Zars T, Fischer M, Schulz R, Heisenberg M (2000) Localization of a short-term memory in Drosophila. Science 288: 672–675.
[29]  Ito K, Sass H, Urban J, Hofbauer A, Schneuwly S (1997) GAL4-responsive UAS-tau as a tool for studying the anatomy and development of the Drosophila central nervous system. Cell Tissue Res 290: 1–10.
[30]  Mader MT (2004) Analyse von Expressionsmustern in den Pilsk?rpern von Drosophila melanogaster. Würzburg, Germany: Universit?t Würzburg. Diplom thesis,.
[31]  Akalal D-BG, Wilson CF, Zong L, Tanaka NK, Ito K, et al. (2006) Roles for Drosophila mushroom body neurons in olfactory learning and memory. Learn Mem 13: 659–668.
[32]  Ahmad K, Henikoff S (2001) Modulation of a transcription factor counteracts heterochromatic gene silencing in Drosophila. Cell 104: 839–847.
[33]  Robertson K, Mergliano J, Minden JS (2003) Dissecting Drosophila embryonic brain development using photoactivated gene expression. Dev Biol 260: 124–137.
[34]  Schulz RA, Chromey C, Lu MF, Zhao B, Olson EN (1996) Expression of the D-MEF2 transcription in the Drosophila brain suggests a role in neuronal cell differentiation. Oncogene 12: 1827–1831.
[35]  Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol [A] 157: 263–277.
[36]  de Belle JS, Heisenberg M (1994) Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263: 692–695.
[37]  de Belle JS, Heisenberg M (1996) Expression of Drosophila mushroom body mutations in alternative genetic backgrounds: a case study of the mushroom body miniature gene (mbm). Proc Natl Acad Sci U S A 93: 9875–9880.
[38]  Margulies C, Tully T, Dubnau J (2005) Deconstructing memory in Drosophila. Curr Biol 17: R700–713.
[39]  McGuire SE, Deshazer M, Davis RL (2005) Thirty years of olfactory learning and memory research in Drosophila melanogaster. Prog Neurobiol 5: 328–347.
[40]  Pinto S, Quintana DG, Smith P, Mihalek RM, Hou ZH, et al. (1999) latheo encodes a subunit of the origin recognition complex and disrupts neuronal proliferation and adult olfactory memory when mutant. Neuron 23: 45–54.
[41]  Yu D, Ponomarev A, Davis RL (2004) Altered representation of the spatial code for odors after olfactory classical conditioning; memory trace formation by synaptic recruitment. Neuron 42: 437–449.
[42]  Urbach R, Schnabel R, Technau GM (2003) The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development 130: 3589–3606.
[43]  Campos-Ortega JA (1993) Early neurogenesis in Drosophila melanogaster. In: Bate M, Martinez-Arias A, editors. Development of Drosophila melanogaster. Cold Spring Harbor: Cold Spring Harbor Laboratory Press. pp. 1091–1130.
[44]  Ito K, Hotta Y (1992) Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev Biol 149: 134–148.
[45]  Stocker RF, Heimbeck G, Gendre N, de Belle JS (1997) Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of antennal target interneurons. J. Neurobiol. 32: 443–456.
[46]  Gerber B, Tanimoto H, Heisenberg M (2004) An engram found? Evaluating the evidence from fruit flies. Curr Opin Neurobiol 14: 737–744.
[47]  Dubnau J, Grady L, Kitamoto T, Tully T (2001) Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 411: 476–480.
[48]  McGuire SE, Le PT, Davis RL (2001) The role of Drosophila mushroom body signaling in olfactory memory. Science 293: 1330–1333.
[49]  Heisenberg M, Borst A, Wagner S, Byers D (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2: 1–30.
[50]  Pascual A, Préat T (2001) Localization of long-term memory within the Drosophila mushroom body. Science 294: 1115–1117.
[51]  Isabel G, Pascual A, Préat T (2004) Exclusive consolidated memory phases in Drosophila. Science 304: 1024–1027.
[52]  Krashes MJ, Keene AC, Leung B, Armstrong JD, Waddell S (2007) Sequential use of mushroom body neuron subsets during drosophila odor memory processing. Neuron 53: 103–115.
[53]  Heisenberg M, B?hl K (1979) Isolation of anatomical brain mutants of Drosophila by histological means. Z Naturforsch C 34: 143–147.
[54]  Abramoff MD, Magelhaes PJ, Ram S (2004) Image processing with ImageJ. Biophotonics International 11: 36–42.
[55]  Zar JH (1996) Biostatistical Analysis, 3rd edition. Englewood Cliffs: Prentice Hall. .

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133