Circadian rhythms in the morphology of neurons in Drosophila

Neurons have an enormous capacity to adapt to changing conditions through the regulation of gene expression, morphology, and physiology. In the fruit fly Drosophila melanogaster, this plasticity includes recurrent changes taking place within intervals of a few hours during the day. The rhythmic alterations in the morphology of neurons described so far include changes in axonal diameter, branching complexity, synapse numbers, and the number of synaptic vesicles. The cycles of these changes have larger amplitude when the fly is exposed to light, but they persist in constant darkness and require the expression of the clock genes period and timeless, leading to the concept of circadian plasticity. The molecular mechanisms driving these cycles appear to require the expression of these genes either inside the neurons themselves or in other peripheral pacemaker cells. Loss-of-function mutations in period and timeless not only abolish the morphological rhythms, but also often cause abnormal axonal branching suggesting that circadian plasticity is relevant for the maintenance of normal morphology. Research into whether (1) circadian plasticity is a common feature of neurons in all animals and (2) our own neurons change shape between day and night will be of interest.

[1]  G. Marqués,et al.  Morphogens and synaptogenesis in Drosophila. , 2005, Journal of neurobiology.

[2]  I. Meinertzhagen,et al.  Daily and circadian rhythms of synaptic frequency in the first visual neuropile of the housefly’s (Musca domestica L.) optic lobe , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[3]  I. Meinertzhagen,et al.  Monopolar cell axons in the first optic neuropil of the housefly, Musca domestica L., undergo daily fluctuations in diameter that have a circadian basis , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  C. Consoulas Remodeling of the leg sensory system during metamorphosis of the hawkmoth, Manduca sexta , 2000, The Journal of comparative neurology.

[5]  T. Dickmeis,et al.  Start the clock! Circadian rhythms and development , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[6]  Satchidananda Panda,et al.  Circadian rhythms from flies to human , 2002, Nature.

[7]  G. Tononi,et al.  Is Sleep Essential? , 2008, PLoS biology.

[8]  H. Keshishian,et al.  Neuromuscular development in Drosophila: insights from embryos and pupae , 1995, Current Opinion in Neurobiology.

[9]  M. F. Ceriani,et al.  Circadian Remodeling of Neuronal Circuits Involved in Rhythmic Behavior , 2008, PLoS biology.

[10]  C. Reggiani,et al.  Neuromuscular junction in abdominal muscles of Drosophila melanogaster during adulthood and aging , 2007, The Journal of comparative neurology.

[11]  C. Kyriacou,et al.  Circadian changes in Drosophila motor terminals , 2007, Developmental neurobiology.

[12]  H. Keshishian,et al.  Stereotypic morphology of glutamatergic synapses on identified muscle cells of Drosophila larvae , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  J. Aschoff,et al.  Circadian Timing a , 1984, Annals of the New York Academy of Sciences.

[14]  A. Sehgal,et al.  Loss of circadian behavioral rhythms and per RNA oscillations in the Drosophila mutant timeless. , 1994, Science.

[15]  V. Auld,et al.  Roles of glia in the Drosophila nervous system. , 2006, Seminars in cell & developmental biology.

[16]  K. Ikeda,et al.  Organization of identified axons innervating the dorsal longitudinal flight muscle ofDrosophila melanogaster , 1980, Journal of neurocytology.

[17]  G. Robinson,et al.  Behavioral development in the honey bee: toward the study of learning under natural conditions. , 1995, Learning & memory.

[18]  E. Pyza,et al.  Circadian rhythms in behaviour and in the visual system of the blow fly, Calliphora vicina , 2001 .

[19]  E. Pyza,et al.  Circadian Control of Dendrite Morphology in the Visual System of Drosophila melanogaster , 2009, PloS one.

[20]  R. Barlow Circadian and efferent modulation of visual sensitivity. , 2001, Progress in brain research.

[21]  C. Helfrich-Förster,et al.  Synergic Entrainment of Drosophila’s Circadian Clock by Light and Temperature , 2009, Journal of biological rhythms.

[22]  Richard D Fetter,et al.  Dynactin Is Necessary for Synapse Stabilization , 2002, Neuron.

[23]  I. Meinertzhagen,et al.  The Effects of Light Reversals on Photoreceptor Synaptogenesis in the Fly Musca domestica , 1997, The European journal of neuroscience.

[24]  Bing Zhang,et al.  Age‐related changes in climbing behavior and neural circuit physiology in Drosophila , 2007, Developmental neurobiology.

[25]  M Heisenberg,et al.  Structural plasticity in the Drosophila brain , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  I. Kurnaz,et al.  Signaling by Neuronal Tyrosine Kinase Receptors: Relevance for Development and Regeneration , 2009, Anatomical record.

[27]  R. Cantera,et al.  Synaptic vesicles in motor synapses change size and distribution during the day , 2010, Synapse.

[28]  N. Strausfeld,et al.  Vision in insects: pathways possibly underlying neural adaptation and lateral inhibition. , 1977, Science.

[29]  Stephan J. Sigrist,et al.  Rapid Activity-Dependent Modifications in Synaptic Structure and Function Require Bidirectional Wnt Signaling , 2008, Neuron.

[30]  Richard D. Fetter,et al.  Watching a Synapse Grow Noninvasive Confocal Imaging of Synaptic Growth in Drosophila , 1999, Neuron.

[31]  A. Simoni,et al.  Temperature Entrainment of Drosophila's Circadian Clock Involves the Gene nocte and Signaling from Peripheral Sensory Tissues to the Brain , 2009, Neuron.

[32]  R. Levine,et al.  Dendritic Remodeling and Growth of Motoneurons during Metamorphosis of Drosophila melanogaster , 2002, The Journal of Neuroscience.

[33]  Structural daily rhythms in GFP-labelled neurons in the visual system of Drosophila melanogaster. , 2005, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[34]  B. Matthews,et al.  Molecules and mechanisms of dendrite development in Drosophila , 2009, Development.

[35]  Allan I Pack,et al.  Rest in Drosophila Is a Sleep-like State , 2000, Neuron.

[36]  T. Holmes,et al.  Circadian- and light-dependent regulation of resting membrane potential and spontaneous action potential firing of Drosophila circadian pacemaker neurons. , 2008, Journal of neurophysiology.

[37]  K. Ikeda,et al.  Morphological identification of the motor neurons innervating the dorsal longitudinal flight muscle of Drosophila melanogaster , 1988, The Journal of comparative neurology.

[38]  I A Meinertzhagen,et al.  Experience-Dependent Developmental Plasticity in the Optic Lobe of Drosophila melanogaster , 1997, The Journal of Neuroscience.

[39]  Giorgio F. Gilestro,et al.  Widespread Changes in Synaptic Markers as a Function of Sleep and Wakefulness in Drosophila , 2009, Science.

[40]  P. Rivlin,et al.  Morphology and molecular organization of the adult neuromuscular junction of Drosophila , 2004, The Journal of comparative neurology.

[41]  Vivian Budnik,et al.  Introduction on the use of the Drosophila embryonic/larval neuromuscular junction as a model system to study synapse development and function, and a brief summary of pathfinding and target recognition. , 2006, International review of neurobiology.

[42]  M. Landgraf,et al.  Development of Drosophila motoneurons: specification and morphology. , 2006, Seminars in cell & developmental biology.

[43]  P. Hardin,et al.  The Circadian Timekeeping System of Drosophila , 2005, Current Biology.

[44]  H. Keshishian,et al.  Neuromuscular development in drosophila: insights from single neurons and single genes , 1993, Trends in Neurosciences.

[45]  J. Hirsh Decapitated Drosophila: a novel system for the study of biogenic amines. , 1998, Advances in pharmacology.

[46]  S. Oliet,et al.  Neuronal, glial and synaptic remodeling in the adult hypothalamus: functional consequences and role of cell surface and extracellular matrix adhesion molecules , 2004, Neurochemistry International.

[47]  I. Meinertzhagen,et al.  Neurotransmitters alter the numbers of synapses and organelles in photoreceptor terminals in the lamina of the housefly, Musca domestica , 1998, Journal of Comparative Physiology A.

[48]  M. M. L. Vail Survival of some photoreceptor cells in albino rats following long-term exposure to continuous light. , 1976 .

[49]  I A Meinertzhagen,et al.  An analysis of the number and composition of the synaptic populations formed by photoreceptors of the fly , 1982, The Journal of comparative neurology.

[50]  M. W. Young,et al.  In situ localization of the per clock protein during development of Drosophila melanogaster , 1988, Molecular and cellular biology.

[51]  J. Dunlap Molecular Bases for Circadian Clocks , 1999, Cell.

[52]  U. Wolfrum,et al.  Active zone proteins are dynamically associated with synaptic ribbons in rat pinealocytes , 2008, Cell and Tissue Research.

[53]  G. Cao,et al.  Circadian Control of Membrane Excitability in Drosophila melanogaster Lateral Ventral Clock Neurons , 2008, The Journal of Neuroscience.

[54]  R J Konopka,et al.  Clock mutants of Drosophila melanogaster. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Paul J Shaw,et al.  Waking Experience Affects Sleep Need in Drosophila , 2006, Science.

[56]  G. Technau Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. , 1984, Journal of neurogenetics.

[57]  I. Meinertzhagen,et al.  Daily rhythmic changes of cell size and shape in the first optic neuropil in Drosophila melanogaster. , 1999, Journal of neurobiology.

[58]  D. V. van Meyel,et al.  Longitudinal glia in the fly CNS: pushing the envelope on glial diversity and neuron-glial interactions. , 2007, Neuron glia biology.

[59]  L. Vollrath,et al.  Plasticity of retinal ribbon synapses , 1996, Microscopy research and technique.

[60]  E. Pyza,et al.  Involvement of glial cells in rhythmic size changes in neurons of the housefly's visual system. , 2004, Journal of neurobiology.

[61]  Hongjun Song,et al.  Adult neurogenesis in the mammalian central nervous system. , 2005, Annual review of neuroscience.

[62]  Kerstin I. Mehnert,et al.  A peripheral pacemaker drives the circadian rhythm of synaptic boutons in Drosophila independently of synaptic activity , 2008, Cell and Tissue Research.

[63]  C. Helfrich-Förster The locomotor activity rhythm of Drosophila melanogaster is controlled by a dual oscillator system , 2001 .

[64]  S. Kay,et al.  Independent photoreceptive circadian clocks throughout Drosophila. , 1997, Science.

[65]  Paul J Shaw,et al.  Use-Dependent Plasticity in Clock Neurons Regulates Sleep Need in Drosophila , 2009, Science.

[66]  C. Helfrich-Förster The circadian system of Drosophila melanogaster and its light input pathways. , 2002, Zoology.

[67]  J. Aschoff,et al.  Circadian rhythms: influences of internal and external factors on the period measured in constant conditions. , 2010 .

[68]  Eric R Kandel,et al.  Synaptic remodeling, synaptic growth and the storage of long-term memory in Aplysia. , 2008, Progress in brain research.

[69]  O. Bosler,et al.  Daily changes in synaptic innervation of VIP neurons in the rat suprachiasmatic nucleus: contribution of glutamatergic afferents , 2010, The European journal of neuroscience.

[70]  Hans-Joachim Wagner,et al.  Adaptation-dependent changes of bipolar cell terminals in fish retina: Effects on overall morphology and spinule formation in Ma and Mb cells , 1996, Vision Research.

[71]  F. Jackson Glial cell modulation of circadian rhythms , 2011, Glia.

[72]  J. C. Hall,et al.  Spatial and temporal expression of the period gene in Drosophila melanogaster. , 1988, Genes & development.

[73]  A Borst,et al.  Drosophila mushroom body mutants are deficient in olfactory learning. , 1985, Journal of neurogenetics.

[74]  E. Pyza,et al.  External and internal inputs affecting plasticity of dendrites and axons of the fly's neurons. , 2008, Acta neurobiologiae experimentalis.

[75]  F. Jackson,et al.  Drosophila Ebony Activity Is Required in Glia for the Circadian Regulation of Locomotor Activity , 2007, Neuron.

[76]  Charlotte Helfrich-Förster,et al.  The neuroarchitecture of the circadian clock in the brain of Drosophila melanogaster , 2003, Microscopy research and technique.

[77]  Sarita Hebbar,et al.  Pruning of motor neuron branches establishes the DLM innervation pattern in Drosophila. , 2004, Journal of neurobiology.

[78]  M Heisenberg,et al.  Vision affects mushroom bodies and central complex in Drosophila melanogaster. , 1997, Learning & memory.

[79]  I. Meinertzhagen,et al.  Involvement of V-ATPase in the regulation of cell size in the fly's visual system. , 2004, Journal of insect physiology.

[80]  REGULATION OF CELL SHAPE IN EUGLENA GRACILIS , 2005 .

[81]  Jeffrey C. Hall Trippings along the trail to the molecular mechanisms of biological clocks , 1995, Trends in Neurosciences.

[82]  Michael W. Young,et al.  A TIMELESS-Independent Function for PERIOD Proteins in the Drosophila Clock , 2000, Neuron.

[83]  C. Klämbt,et al.  The eye imaginal disc as a model to study the coordination of neuronal and glial development , 2010, Fly.

[84]  R. Strauss,et al.  Circadian Plasticity in Photoreceptor Cells Controls Visual Coding Efficiency in Drosophila melanogaster , 2010, PloS one.

[85]  D. Saunders Insect circadian rhythms and photoperiodism , 1997, Invertebrate Neuroscience.

[86]  S. Oliet,et al.  Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. , 2008, Physiological reviews.

[87]  W. Engelmann,et al.  Circadian activity rhythm of the house fly continues after optic tract severance and lobectomy. , 1985, Chronobiology international.

[88]  T. Lonergan Regulation of Cell Shape in Euglena gracilis: I. Involvement of the Biological Clock, Respiration, Photosynthesis, and Cytoskeleton. , 1983, Plant physiology.

[89]  O. Trujillo-Cenóz Some aspects of the structural organization of the intermediate retina of dipterans. , 1965, Journal of ultrastructure research.

[90]  N. Klauke,et al.  In vitro effects of putative neurotransmitters on synaptic ribbon numbers and N-acetyltransferase activity in the rat pineal gland , 2005, Journal of Neural Transmission / General Section JNT.

[91]  I. Meinertzhagen,et al.  Brain plasticity in Diptera and Hymenoptera. , 2010, Frontiers in bioscience.

[92]  G. Tononi,et al.  Sleep and synaptic homeostasis: a hypothesis , 2003, Brain Research Bulletin.

[93]  C. Helfrich-Förster Differential Control of Morning and Evening Components in the Activity Rhythm of Drosophila melanogaster—Sex-Specific Differences Suggest a Different Quality of Activity , 2000, Journal of biological rhythms.

[94]  Hölldobler,et al.  Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus , 1996, The Journal of experimental biology.

[95]  Effects of locomotor stimulation and protein synthesis inhibition on circadian rhythms in size changes of L1 and L2 interneurons in the fly's visual system , 2007, Developmental neurobiology.

[96]  J. Takahashi,et al.  The physiology of circadian pacemakers. , 1978, Annual review of physiology.

[97]  R. Levine,et al.  Remodeling of the insect nervous system , 1995, Current Opinion in Neurobiology.

[98]  J. Truman,et al.  Metamorphosis of the central nervous system of Drosophila. , 1990, Journal of neurobiology.

[99]  J. C. Hall,et al.  Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[100]  S. Basinger,et al.  Photoreceptor shedding is initiated by light in the frog retina. , 1976, Science.

[101]  V. Budnik,et al.  Synaptic cytoskeleton at the neuromuscular junction. , 2006, International review of neurobiology.

[102]  Jeffrey C. Hall,et al.  Behavior in Light-Dark Cycles of Drosophila Mutants That Are Arrhythmic, Blind, or Both , 1993, Journal of biological rhythms.

[103]  J. C. Hall,et al.  Rhythmic Expression of a PER-Reporter in the Malpighian Tubules of Decapitated Drosophila: Evidence for a Brain-Independent Circadian Clock , 1997, Journal of biological rhythms.