Seeing the light: photobehavior in fruit fly larvae

Understanding how sensory stimuli drive behavior requires a detailed understanding of the molecular and neural nature through which the stimuli are received and processed. The visual system of the fruit fly Drosophila melanogaster shares marked similarities to that of mammals. Although much focus has been given to the fly visual system, an even further simplified eye and brain makes the visual system of Drosophila larvae an excellent model for dissecting sensory processing and behavioral responses to light. Recent work has identified sensory and central brain neurons required for larval visual behaviors, including circadian rhythms. Here, we review the genes and neurons regulating visual processing in Drosophila larvae and discuss the implications of this work for furthering understanding of more complex visual systems.

[1]  Ralph J Greenspan,et al.  Serotonin and neuropeptide F have opposite modulatory effects on fly aggression , 2007, Nature Genetics.

[2]  G. Nagel,et al.  Light-Induced Activation of Distinct Modulatory Neurons Triggers Appetitive or Aversive Learning in Drosophila Larvae , 2006, Current Biology.

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

[4]  Benjamin Richier,et al.  PDF-modulated visual inputs and cryptochrome define diurnal behavior in Drosophila , 2009, Nature Neuroscience.

[5]  A. Borst.  Drosophila's View on Insect Vision , 2009, Current Biology.

[6]  P. Nawathean,et al.  The doubletime and CKII kinases collaborate to potentiate Drosophila PER transcriptional repressor activity. , 2004, Molecular cell.

[7]  Naryttza N. Diaz,et al.  Photoreceptors: Unconventional Ways of Seeing , 2011, Current Biology.

[8]  Ana Regina Campos,et al.  Photic input pathways that mediate the Drosophila larval response to light and circadian rhythmicity are developmentally related but functionally distinct , 2005, The Journal of comparative neurology.

[9]  A. Chess,et al.  Function of Rhodopsin in Temperature Discrimination in Drosophila , 2011, Science.

[10]  Randolf Menzel,et al.  Insect visual perception: complex abilities of simple nervous systems , 1997, Current Opinion in Neurobiology.

[11]  Zhefeng Gong,et al.  Two Pairs of Neurons in the Central Brain Control Drosophila Innate Light Preference , 2010, Science.

[12]  John B. Thomas,et al.  A sensory feedback circuit coordinates muscle activity in Drosophila , 2007, Molecular and Cellular Neuroscience.

[13]  Andrey Rzhetsky,et al.  A Chemosensory Gene Family Encoding Candidate Gustatory and Olfactory Receptors in Drosophila , 2001, Cell.

[14]  L. Gilbert,et al.  Prothoracicotropic hormone regulates developmental timing and body size in Drosophila. , 2007, Developmental cell.

[15]  I. Meinertzhagen,et al.  The Extraretinal Eyelet of Drosophila: Development, Ultrastructure, and Putative Circadian Function , 2002, The Journal of Neuroscience.

[16]  Aravinthan D. T. Samuel,et al.  Navigational Decision Making in Drosophila Thermotaxis , 2010, The Journal of Neuroscience.

[17]  A. Borst,et al.  Fly motion vision. , 2010, Annual review of neuroscience.

[18]  R. Allada,et al.  The CRYPTOCHROME Photoreceptor Gates PDF Neuropeptide Signaling to Set Circadian Network Hierarchy in Drosophila , 2009, Current Biology.

[19]  E. Meyer-Bernstein,et al.  Photic Signaling by Cryptochrome in the DrosophilaCircadian System , 2001, Molecular and Cellular Biology.

[20]  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.

[21]  C. Helfrich-Förster,et al.  Ectopic Expression of the Neuropeptide Pigment-Dispersing Factor Alters Behavioral Rhythms in Drosophila melanogaster , 2000, The Journal of Neuroscience.

[22]  Gilles Laurent,et al.  painless, a Drosophila Gene Essential for Nociception , 2003, Cell.

[23]  J. Truman,et al.  Sequential Nuclear Accumulation of the Clock Proteins Period and Timeless in the Pacemaker Neurons of Drosophila melanogaster , 2002, The Journal of Neuroscience.

[24]  Bertram Gerber,et al.  Olfactory learning and behaviour are ‘insulated’ against visual processing in larval Drosophila , 2006, Journal of Comparative Physiology A.

[25]  Jeffrey C. Hall,et al.  The cryb Mutation Identifies Cryptochrome as a Circadian Photoreceptor in Drosophila , 1998, Cell.

[26]  Jeffrey C. Hall,et al.  CYCLE Is a Second bHLH-PAS Clock Protein Essential for Circadian Rhythmicity and Transcription of Drosophila period and timeless , 1998, Cell.

[27]  M. W. Young,et al.  PER-TIM Interactions in Living Drosophila Cells: An Interval Timer for the Circadian Clock , 2006, Science.

[28]  Xiangzhong Zheng,et al.  Serotonin Modulates Circadian Entrainment in Drosophila , 2005, Neuron.

[29]  L. Looger,et al.  Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall , 2010, Nature.

[30]  P. Garrity,et al.  The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. , 2005, Genes & development.

[31]  S. Benzer,et al.  Glia in the chiasms and medulla of the Drosophila melanogaster optic lobes , 1997, Cell and Tissue Research.

[32]  B. Iyengar,et al.  Genetic Dissection of Behavior: Modulation of Locomotion by Light in the Drosophila melanogaster Larva Requires Genetically Distinct Visual System Functions , 1999, The Journal of Neuroscience.

[33]  B. Iyengar,et al.  Behavioral Characterization and Genetic Analysis of the Drosophila melanogaster Larval Response to Light as Revealed by a Novel Individual Assay , 2000, Behavior genetics.

[34]  Ana Regina Campos,et al.  Genetic dissection of trophic interactions in the larval optic neuropil of Drosophila melanogaster. , 2005, Developmental biology.

[35]  Ana Regina Campos,et al.  Kinematic Analysis of Drosophila Larval Locomotion in Response to Intermittent Light Pulses , 2007, Behavior genetics.

[36]  Esteban O. Mazzoni,et al.  Circadian Pacemaker Neurons Transmit and Modulate Visual Information to Control a Rapid Behavioral Response , 2005, Neuron.

[37]  Albert Cardona,et al.  The Drosophila larval visual system: high-resolution analysis of a simple visual neuropil. , 2011, Developmental biology.

[38]  Margaret I. Hall,et al.  The Nocturnal Bottleneck and the Evolution of Mammalian Vision , 2010, Brain, Behavior and Evolution.

[39]  Simon G Sprecher,et al.  Distinct Visual Pathways Mediate Drosophila Larval Light Avoidance and Circadian Clock Entrainment , 2011, The Journal of Neuroscience.

[40]  H. Wijnen,et al.  Integration of Light and Temperature in the Regulation of Circadian Gene Expression in Drosophila , 2007, PLoS genetics.

[41]  Andreas S. Thum,et al.  Capacity of visual classical conditioning in Drosophila larvae. , 2011, Behavioral neuroscience.

[42]  G. Stormo,et al.  The Neuropeptide Pigment-Dispersing Factor Coordinates Pacemaker Interactions in the Drosophila Circadian System , 2004, The Journal of Neuroscience.

[43]  S. Kay,et al.  Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. , 1998, Science.

[44]  A. Klarsfeld,et al.  A Role for Blind DN2 Clock Neurons in Temperature Entrainment of the Drosophila Larval Brain , 2009, The Journal of Neuroscience.

[45]  L. Vosshall,et al.  Bilateral olfactory sensory input enhances chemotaxis behavior , 2008, Nature Neuroscience.

[46]  Feng Zhang,et al.  Nociceptive Neurons Protect Drosophila Larvae from Parasitoid Wasps , 2007, Current Biology.

[47]  P. Shen,et al.  Regulation of aversion to noxious food by Drosophila neuropeptide Y– and insulin-like systems , 2005, Nature Neuroscience.

[48]  Claude Desplan,et al.  Building a projection map for photoreceptor neurons in the Drosophila optic lobes. , 2004, Seminars in cell & developmental biology.

[49]  C. Helfrich-Förster,et al.  Development of pigment‐dispersing hormone‐immunoreactive neurons in the nervous system of Drosophila melanogaster , 1997, The Journal of comparative neurology.

[50]  Jeffrey C. Hall,et al.  CRY, a Drosophila Clock and Light-Regulated Cryptochrome, Is a Major Contributor to Circadian Rhythm Resetting and Photosensitivity , 1998, Cell.

[51]  M. Mukhopadhyay,et al.  The larval optic nerve is required for the development of an identified serotonergic arborization in Drosophila melanogaster. , 1995, Developmental biology.

[52]  J. C. Hall,et al.  Spatial and Temporal Expression of the period andtimeless Genes in the Developing Nervous System ofDrosophila: Newly Identified Pacemaker Candidates and Novel Features of Clock Gene Product Cycling , 1997, The Journal of Neuroscience.

[53]  Zhefeng Gong,et al.  Behavioral dissection of Drosophila larval phototaxis. , 2009, Biochemical and biophysical research communications.

[54]  W. Gehring.  Historical perspective on the development and evolution of eyes and photoreceptors. , 2004, The International journal of developmental biology.

[55]  A. Sehgal,et al.  Ontogeny of a biological clock in Drosophila melanogaster. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Tao Xu,et al.  C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog , 2010, Nature Neuroscience.

[57]  M. Sokolowski,et al.  Characterization and genetic analysis of Drosophila melanogaster photobehavior during larval development. , 1995, Journal of neurogenetics.

[58]  Jeffrey C. Hall,et al.  A Mutant Drosophila Homolog of Mammalian Clock Disrupts Circadian Rhythms and Transcription of period and timeless , 1998, Cell.

[59]  Franck Pichaud,et al.  Adult and larval photoreceptors use different mechanisms to specify the same Rhodopsin fates. , 2007, Genes & development.

[60]  Ana Regina Campos,et al.  Role of serotonergic neurons in the Drosophila larval response to light , 2009, BMC Neuroscience.

[61]  Aaron DiAntonio,et al.  Visualizing glutamatergic cell bodies and synapses in Drosophila larval and adult CNS , 2008, The Journal of comparative neurology.

[62]  Quan Yuan,et al.  A Sleep-Promoting Role for the Drosophila Serotonin Receptor 1A , 2006, Current Biology.

[63]  Yuh Nung Jan,et al.  Tiling of the Drosophila epidermis by multidendritic sensory neurons. , 2002, Development.

[64]  Roger C. Hardie,et al.  Visual transduction in Drosophila , 2001, Nature.

[65]  Jeffrey C. Hall,et al.  A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. , 2000, Cell.

[66]  S. Collin.  Evolution and Ecology of Retinal Photoreception in Early Vertebrates , 2010, Brain, Behavior and Evolution.

[67]  M. Friedrich.  Continuity versus split and reconstitution: exploring the molecular developmental corollaries of insect eye primordium evolution. , 2006, Developmental biology.

[68]  K. J. Fogle,et al.  CRYPTOCHROME Is a Blue-Light Sensor That Regulates Neuronal Firing Rate , 2011, Science.

[69]  Richard Y. Hwang,et al.  Pickpocket Is a DEG/ENaC Protein Required for Mechanical Nociception in Drosophila Larvae , 2010, Current Biology.

[70]  Simon G. Sprecher,et al.  Switch of rhodopsin expression in terminally differentiated Drosophila sensory neurons , 2008, Nature.

[71]  V. Hartenstein,et al.  The embryonic development of the Drosophila visual system , 1993, Cell and Tissue Research.

[72]  V. Hartenstein,et al.  Early neurogenesis in wild-typeDrosophila melanogaster , 1984, Wilhelm Roux's archives of developmental biology.