Fine structure of synaptic sites and circuits in mushroom bodies of insect brains

Abel, 2001, Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera, J. Comp. Neurol., 437, 363, 10.1002/cne.1289 Aganati, 2006, Volume transmission and wiring transmission from cellular to molecular networks: history and perspectives, Acta Physiol. Oxf., 187, 329, 10.1111/j.1748-1716.2006.01579.x Akert, 1967, Über Glomeruli im Zentralnervensystem von Vertebraten und Invertebraten, Schweiz Arch. Neurol. Psychiatr., 100, 321 Aronstein, 1995, Immunocytochemistry of a novel GABA receptor subunit Rdl in Drosophila melanogaster, Invertebr. Neurosci., 1, 25, 10.1007/BF02331829 Aso, 2009, The mushroom body of adult Drosophila characterized by GAL4 drivers, J. Neurogen., 23, 156, 10.1080/01677060802471718 Aso, 2014, Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila, eLife, 10.7554/eLife.04580 Aso, 2014, The neuronal architecture of the mushroom body provides a logic for associative learning, Elife, 3, e04577, 10.7554/eLife.04577 Bellonci, 1883, Sur la structure et les rapports des lobes olfactives dans les arthropodes supérieures et les vertébrés, Arch. Ital. Biol., 3, 191 Berry, 2008, Olfactory memory traces in Drosophila, Prog. Brain Res., 169, 293, 10.1016/S0079-6123(07)00018-0 Bicker, 1999, Histochemistry of classical transmitters in antennal lobes and mushroom bodies of the honeybee, Microsc. Res. Tech., 145, 174, 10.1002/(SICI)1097-0029(19990501)45:3<174::AID-JEMT5>3.0.CO;2-U Bicker, 1999, Biogenic amines in the brain of the honeybee: cellular distribution, development and behavioural functions, Microsc. Res. Tech., 145, 106 Bicker, 1985, Mushroom body feedback interneurons in the honeybee show GABA-like immunoreactivity, Brain Res., 360, 394, 10.1016/0006-8993(85)91262-4 Binzer, 2014, Neuropeptidome of Tribolium castaneum antennal lobes and mushroom bodies, J. Comp. Neurol., 522, 337, 10.1002/cne.23399 Blenau, 2011, Distribution of serotonin (5HT) and its receptors in the insect brain with focus on the mushroom bodies. Lessons from Drosophila melanogaster and Apis mellifera, Arthropod Struct. Dev., 40, 381, 10.1016/j.asd.2011.01.004 Blenau, 1999, Neurons with dopamine-like immunoreactivity target mushroom body Kenyon cell somata in the brain of some hymenopteran insects, J. Ins. Morphol. Embryol., 28, 203, 10.1016/S0020-7322(99)00025-2 Boeckh, 1970, Sensorische Eingänge und synaptische Verbindungen im Zentralnervensystem von Insekten. Experimentelle Degeneration in der antennalen Sinnesbahn im Oberschlundganglion von Fliegen und Schaben, Z. Zellforsch., 103, 429, 10.1007/BF00335285 Breer, 1987, Neurochemical aspects of cholinergic synapses in the insect brain, 415 Brotz, 1997, Gamma-aminobutyric acid receptor distribution in the mushroom bodies of a fly (Callipora erythrocephala): a functional subdivision of Kenyon cells, J. Comp. Neurol., 383, 42, 10.1002/(SICI)1096-9861(19970623)383:1<42::AID-CNE3>3.0.CO;2-L Brown, 2002, Stereological analysis reveals striking differences in the structural plasticity of two readily identifiable glomeruli in the antennal lobes of the adult worker honeybee, J. Neurosci., 22, 8514, 10.1523/JNEUROSCI.22-19-08514.2002 Brown, 2004, Foraging experience, glomerulus volume, and synapse number: a stereological study of the honey bee antennal lobe, Dev. Neurobiol., 60, 40, 10.1002/neu.20002 Brown, 2012, Fine structural organization of the hemiellipsoid body of the land hermit crab, Coenobita clypeatus, J. Comp. Neurol., 520, 2847, 10.1002/cne.23058 Bruns, 1995, Real-time measurement of transmitter release from single synaptic vesicles, Nature, 377, 62, 10.1038/377062a0 Burette, 2012, Electron tomographic analysis of synaptic ultrastructure, J. Comp. Neurol., 520, 2697, 10.1002/cne.23067 Burrows, 1996 Bush, 2010, A map of octopaminergic neurons in the Drosophila brain, J. Comp. Neurol., 513, 643, 10.1002/cne.21966 Butcher, 2012, Different classes of input and output neurons reveal new features in microglomeruli of thr adult Drosophila mushroom body calyx, J. Comp. Neurol., 520, 2185, 10.1002/cne.23037 Cajal, 1915, 1168 Capani, 2001, Selective localization of high concentrations of F-actin in subpopulations of dendritic spines in rat central nervous system: a three-dimensional electron microscopic study, J. Comp. Neurol., 435, 156, 10.1002/cne.1199 Carlsson, 2010, Multiple neuropeptides in the Drosophila antennal lobe suggest complex modulatory circuits, J. Comp. Neurol., 518, 3359, 10.1002/cne.22405 Cayre, 2002, The common properties of neurogenesis in the adult brain: from invertebrates to vertebrates, Comp. Biochem. Physiol. B, 132, 1, 10.1016/S1096-4959(01)00525-5 Coss, 1980, Changes of morphology of dendritic spines of calycal honeybee interneurons associated with cumulative nursing and foraging experience, Brain Res., 192, 49, 10.1016/0006-8993(80)91007-0 Christiansen, 2011, Presynapses in Kenyon cell dendrites in the mushroom body calyx of Drosophila, J. Neurosci., 31, 9696, 10.1523/JNEUROSCI.6542-10.2011 Daniels, 2008, Visualising glutamatergic cell bodies and synapses in Drosophila larval and adult CNS, J. Comp. Neurol., 508, 131, 10.1002/cne.21670 Davis, 2005, Olfactory memory formation in Drosophila: from molecular to systems neuroscience, Annu. Rev. Neurosci., 28, 275, 10.1146/annurev.neuro.28.061604.135651 De Camilli, 2001, The structure of synapses, 89 De Robertis, 1955, Some features of the submicroscopic morphology of synapses in frog and earthworm, J. Biophys. Biochem. Cytol., 1, 47, 10.1083/jcb.1.1.47 Devaud, 2001, Odor exposure causes central adaptation and morphological changes in selected olfactory glomeruli in Drosophila, J. Comp. Neurol., 21, 6274 Devaud, 2003, Structural and functional changes in the olfactory pathway of adult Drosophila take place at a critical age, Dev. Neurobiol., 56, 13, 10.1002/neu.10215 Dobrin, 2011, Muscarinic regulation of Kenyon cell dendritic arborizations in adult worker honeybees, Arthropod Struct. Dev., 40, 409, 10.1016/j.asd.2011.01.003 Durst, 1994, Development and experience lead to increased volume of subcompartments of the honeybee mushroom body, Behav. Neurol. Biol., 62, 259, 10.1016/S0163-1047(05)80025-1 Ehmer, 2002, Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera), J. Comp. Neurol., 451, 362, 10.1002/cne.10355 Eickhoff, 2012, Developmental expression of cell recognition molecules in the mushroom body and antennal lobe of the locust Locusta migratoria, J. Comp. Neurol., 520, 2021, 10.1002/cne.23026 Enell, 2007, γ-Aminobutyric acid (GABA) signaling components in Drosophila: immunocytochemical localization of GABAB receptors in relation to the GABAA receptor subunit RDL and a vesicular GABA transporter, J. Comp. Neurol., 505, 18, 10.1002/cne.21472 Erber, 1987, Functional roles of the mushroom bodies in insects, 485 Fahrbach, 2006, Structure of the mushroom bodies of the insect brain, Annu. Rev. Entomol., 51, 209, 10.1146/annurev.ento.51.110104.150954 Farris, 2011, Are mushroom bodies cerebellum-like structures?, Arthropod Struct. Dev., 40, 368, 10.1016/j.asd.2011.02.004 Farris, 2003, Development and evolution of the insect mushroom bodies: towards the understanding of conserved developmental mechanisms in a higher brain center, Arthropod Struct. Dev., 32, 79, 10.1016/S1467-8039(03)00009-4 Farris, 2001, Experience and age-related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee, J. Neurosci., 21, 6395, 10.1523/JNEUROSCI.21-16-06395.2001 Fiala, 2002, Genetically expressed Camaeleon in Drosophila melanogaster is used to visualise olfactory information in projection neurons, Curr. Biol., 12, 1877, 10.1016/S0960-9822(02)01239-3 Fouquet, 2009, Maturation of active zone assembly by Drosphila Bruchpilot, J. Cell Biol., 186, 129, 10.1083/jcb.200812150 Frambach, 2004 Frambach, 2004, Separate distribution of deutocerebral projection neurons in the mushroom bodies of the cricket brain, Acta Biol. Hung, 55, 21, 10.1556/ABiol.55.2004.1-4.4 Frambach, 2004, F-actin at identified synapses in the mushroom body neuropil of the insect brain, J. Comp. Neurol., 475, 303, 10.1002/cne.20165 Frontali, 1970, Studies on the neuronal organization of cockroach corpora pedunculata, J. Ins. Physiol., 16, 2293, 10.1016/0022-1910(70)90152-6 Galizia, 2000, Odour perception in honeybees: coding information in glomerular patterns, Curr. Opin. Neurobiol., 10, 504, 10.1016/S0959-4388(00)00109-4 Galizia, 2010, Parallel olfactory systems in insects. Anatomy and function, Annu. Rev. Entomol., 55, 399, 10.1146/annurev-ento-112408-085442 Ganeshina, 2010, Stratification and synaptogenesis in the mushroom body of the honeybee, Apis mellifera, J. Morphol., 271, 826 Ganeshina, 2001, GABA-immunoreactive neurons in the mushroom bodies of the honeybee: an electron microscopic study, J. Comp. Neurol., 437, 335, 10.1002/cne.1287 Groh, 2004, Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development, Proc. Nat. Acad. Sci., 101, 4268, 10.1073/pnas.0400773101 Groh, 2006, Environment and age-dependent plasticity of synaptic complexes in the mushroom bodies of honeybee queens, Brain Behav. Evol., 68, 1, 10.1159/000092309 Groh, 2010, Brain plasticity in Diptera and Hymenoptera, Front Biosci., 2, 268 Groh, 2011, Comparison of microglomerular structures in the mushroom body calyx of neopteran insects, Arthropod Struct. Dev., 40, 358, 10.1016/j.asd.2010.12.002 Groh, 2012, Age related plasticity in the synaptic ultrastructure of neurons in the mushroom body calyx of the adult honeybee Apis mellifera, J. Comp. Neurol., 520, 3509, 10.1002/cne.23102 Gronenberg, 2001, Subdivisions of hymenopteran mushroom body calyces by their afferent supply, J. Comp. Neurol., 436, 474, 10.1002/cne.1045 Grünewald, 1999, Morphology of feedback neurons in the mushroom bodies of the honeybee, Apis mellifera, J. Comp. Neurol., 404, 414, 10.1002/(SICI)1096-9861(19990201)404:1<114::AID-CNE9>3.0.CO;2-# Grünewald, 1999, Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee, Apis mellifera, J. Comp. Physiol. A, 185, 565, 10.1007/s003590050417 Hamanaka, 2009, Immunocytochemical localization of synaptic proteins to photoreceptor synapses of Drosophila melanogaster, J. Comp. Neurol., 518, 1133, 10.1002/cne.22268 Hammer, 1993, An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees, Nature, 366, 59, 10.1038/366059a0 Hauser, 2006, A review of neurohormone GPCRs present in the fruit fly Drosophila melanogaster and the honey bee Apis mellifera, Prog. Neurobiol., 80, 1, 10.1016/j.pneurobio.2006.07.005 Heisenberg, 2003, Mushroom body memoir: from maps to models, Nat. Neurosci., 4, 266, 10.1038/nrn1074 Heisenberg, 1998, What do the mushroom bodies do for the insect brain? An introduction, Learn. Mem., 5, 1, 10.1101/lm.5.1.1 Heisenberg, 1995, Structural plasticity in the Drosophila brain, J. Neurosci., 15, 1951, 10.1523/JNEUROSCI.15-03-01951.1995 Herman, 1971, Insect brain as a model for the study of aging. Age related changes in Drosophila melanogaster, Acta Neuropathol., 19, 167183, 10.1007/BF00684595 Hess, 1958, The fine structure of nerve cells and fibres, neuroglia and sheath of the ganglion chain of the cockroach, J. Biophys. Biochem. Cytol., 4, 731, 10.1083/jcb.4.6.731 Heuer, 2012, Neuropeptides in insect mushroom bodies, Arthropod Struct. Dev., 41, 199, 10.1016/j.asd.2012.02.005 Hildebrand, 1997, Mechanisms of olfactory discrimination: converging evidence for common principles across phyla, Annu. Rev. Neurosci., 20, 595, 10.1146/annurev.neuro.20.1.595 Homberg, 1994, Distribution of neurotransmitters in the insect brain, vol. 40, 1 Homberg, 2002, Neurotransmitters and neuropeptides in the brain of the locust, Microsc. Res. Tech., 56, 189, 10.1002/jemt.10024 Honegger, 1975, Cobalt sulphide staining of optic fibres in the brain of the cricket, Gryllus campestris, Cell Tiss. Res., 159, 213, 10.1007/BF00219157 Hourcade, 2010, Long-term memory leads to synaptic reorganization in the mushroom bodies: a memory trace in the insect brain?, J. Neurosci., 30, 6461, 10.1523/JNEUROSCI.0841-10.2010 Howse, 1975, Brain structure and behaviour in insects, Annu. Rev. Entomol., 20, 359, 10.1146/annurev.en.20.010175.002043 Hoyer, 2005, Biogenic amines in the ponerine ant Harpegnathos saltator: serotonin and dopamine immunoreactivity in the brain, Arthropod Struct. Dev., 34, 429, 10.1016/j.asd.2005.03.003 Ito, 1998, The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen, Learn. Mem., 5, 5277, 10.1101/lm.5.1.52 Ito, 2014, A systematic nomenclature for the insect brain, Neuron, 81, 755, 10.1016/j.neuron.2013.12.017 Iwasaki, 1999, Ultrastructural analyses of modular subunits in the mushroom bodies of the cockroach, J. Electr. Microsc., 48, 55, 10.1093/oxfordjournals.jmicro.a023651 Johard, 2008, Intrinsic neurons of Drosophila mushroom bodies express short neuropeptide F: relations to extrinsic neurons expressing different neurotransmitters, J. Comp. Neurol., 507, 1479, 10.1002/cne.21636 Kasai, 2010, Learning rules and persistence of dendritic spines, Eur. J. Neurosci., 32, 241, 10.1111/j.1460-9568.2010.07344.x Kenyon, 1896, The brain of the bee, J. Comp. Neurol., 6, 133, 10.1002/cne.910060302 Killmann, 1999, Types, numbers and distribution of synapses on the dendritic tree of an identified visual interneuron in the brain of the locust, Cell Tiss. Res., 296, 645, 10.1007/s004410051325 Kinoshita, 2015, Topographically distinct visual and olfactory inputs to the mushroom body in the Swallow tail butterfly Papilio xantuas, J. Comp. Neurol., 523, 162, 10.1002/cne.23674 Kirschner, 2006, Dual olfactory pathway in the honey bee, Apis mellifera, J. Comp. Neurol., 499, 933, 10.1002/cne.21158 Kittel, 2006, Bruchpilot promotes active zone assembly, Ca+ channel clustering, and vesicle release, Science, 312, 1051, 10.1126/science.1126308 Klagges, 1996, Invertebrate Synapsins: a single gene codes for several isoforms in Drosophila, J. Neurosci., 16, 3154, 10.1523/JNEUROSCI.16-10-03154.1996 Koper, 2012, Analysis of adhesion molecules and basement to synaptic adhesion at the Drosophila embryonic NJM, PLoS One, 7, 1, 10.1371/journal.pone.0036339 Kremer, 2010, Structural long-term changes at mushroom body input synapses, Curr. Biol., 20, 1938, 10.1016/j.cub.2010.09.060 Kühn-Bühlmann, 2006, Age-dependent and task-related volume changes in mushroom bodies of visually guided desert ants, Cataglyphis bicolor, Dev. Neurobiol., 511, 10.1002/neu.20235 Landolt, 1966, Electron microscope studies on soma-somatic interneuronal junctions in the corpora pedunculata of the wood ant (Formica lugubris Zett.), J. Cell Biol., 28, 391, 10.1083/jcb.28.2.391 Laurent, 2002, Olfactory network dynamics and the coding of multidimensional signals, Nat. Rev. Neurosci., 3, 884, 10.1038/nrn964 Leiss, 2009, Characterization of dendritic spines in the Drosophila nervous system, Dev. Neurobiol., 69, 221, 10.1002/dneu.20699 Leiss, 2009, Synaptic organization in the adult mushroom body calyx, J. Comp. Neurol., 517, 808, 10.1002/cne.22184 Leitch, 1996, GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system, J. Comp. Neurol., 372, 487, 10.1002/(SICI)1096-9861(19960902)372:4<487::AID-CNE1>3.0.CO;2-0 Leitinger, 2002, The organization of synaptic vesicles at tonically transmitting connections of locust visual interneurons, J. Comp. Neurol., 50, 93 Leitinger, 2004, Differential expression of synapsin in visual neurons of the locust Schistocerca gregaria, J. Comp. Neurol., 480, 89, 10.1002/cne.20333 Leitinger, 2012, Structural organization of the presynaptic density of identified synapses in the locust central nervous system, J. Comp. Neurol., 520, 384, 10.1002/cne.22744 Lent, 2007, Learning with half a brain, Dev. Neurobiol., 67, 740, 10.1002/dneu.20374 Li, 1997, Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach, Periplaneta americana, J. Comp. Neurol., 387, 331, 10.1002/(SICI)1096-9861(19971103)387:4<631::AID-CNE9>3.0.CO;2-3 Liu, 2009, The GABAergic anterior paired lateral neuron suppressed by olfactory learning, Nat. Neurosci., 12, 53, 10.1038/nn.2235 Liu, 2016, Gap junction networks in mushroom bodies participate in visual learning and memory, eLife, 5, e 1328, 10.7554/eLife.13238 Mancini, 1967, Fine structure of the mushroom body neuropil of the brain of the roach, Periplaneta americana, Z. Zellforsch., 83, 334, 10.1007/BF00336862 Marin, 2002, Representation of the glomerular olfactory map in the Drosophila brain, Cell, 109, 243, 10.1016/S0092-8674(02)00700-6 Mashaly, 2004 Mashaly, 2003, A substrate for plasticity: sprouting neurons in an olfactory neuropile of the mature cricket brain, Comp. Biochem. Physiol., 134, 67 Mashaly, 2008, Sprouting interneurons in mushroom bodies of adult cricket brains, J. Comp. Neurol., 508, 153, 10.1002/cne.21660 Matus, 2000, Actin-based plasticity in dendritic spines, Science, 290, 754, 10.1126/science.290.5492.754 Maynard, 1967, Organisation of central ganglia, 231 Meinertzhagen, 1996, Ultrastructure and quantification of synapses in the insect nervous system, J. Neurosci. Methods, 69, 59, 10.1016/S0165-0270(96)00021-0 Meinertzhagen, 2001, Plasticity in the insect nervous system, Adv. Insect Physiol., 28, 84, 10.1016/S0065-2806(01)28009-6 Menzel, 1996, Learning and memory in honeybees: from behaviour to neural substrates, Annu. Rev. Neurosci., 19, 379, 10.1146/annurev.ne.19.030196.002115 Menzel, 2010, Antennal lobe of the honeybee, 427 Meynert, 1868, 88 Micheva, 1998, ß-Actin is confined to structures having high capacity of remodeling in developing and adult rat cerebellum, Eur. J. Neurosci., 10, 3785, 10.1046/j.1460-9568.1998.00391.x Miskiewicz, 2004, Ultrastructural characteristics of circadian pacemakers, immunoreactive to an antibody against a pigment-dispersing hormone in the flie's brain, Neurosci. Lett., 363, 73, 10.1016/j.neulet.2004.03.051 Miskiewicz, 2008, Circadian release of pigment dispersing factor in the visual system of the housefly, Musca domestica, J. Comp. Neurol., 509, 422, 10.1002/cne.21765 Mizunami, 1998, Mushroom bodies of the cockroach: their participation in place memory, J. Comp. Neurol., 402, 520, 10.1002/(SICI)1096-9861(19981228)402:4<520::AID-CNE6>3.0.CO;2-K Mizunami, 2004, Further exploration into the adaptive design of the arthropod “Microbrain”: I. Sensory and memory-processing systems, Zool. Sci., 21, 1141, 10.2108/zsj.21.1141 Mizunami, 1997, Modular structures in the mushroom bodies of the cockroach, Neurosci. Lett., 229, 153, 10.1016/S0304-3940(97)00438-2 Mizunami, 1998, Topography of modular subunits in the mushroom bodies of cockroaches, J. Comp. Neurol., 399, 153161 Mobbs, 1982, The brain of the honey bee Apis mellifera. The connections and spatial organization of the mushroom bodies, Philos. Trans. R. Soc. Lond. Biol., 298, 309, 10.1098/rstb.1982.0086 Mobbs, 1985, Brain structure, vol. 5, 299 Montgomery, 2016, Brain composition in Heliconius butterflies, post-eclosion growth and experience-dependent neuropil plasticity, J. Comp. Neurol., 524, 10.1002/cne.23993 Nässel, 1991, Neurotransmitters and neuromodulators in the insect visual system, Prog. Neurobiol., 37, 179, 10.1016/0301-0082(91)90027-X Nässel, 2002, Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones, Prog. Neurobiol., 68, 1, 10.1016/S0301-0082(02)00057-6 Nässel, 2006, Neuropeptides in interneurons of the insect brain, Cell Tiss. Res., 326, 1, 10.1007/s00441-006-0210-8 Nässel, 2010, Drosophila neuropeptides in regulation of physiology and behaviour, Prog. Neurobiol., 92, 42, 10.1016/j.pneurobio.2010.04.010 Nishikawa, 1998, Function specific distribution patterns of axon terminals of input neurons in the calyces of mushroom body of the cockroach Periplaneta americana, Neurosci. Lett., 245, 33, 10.1016/S0304-3940(98)00162-1 Nishikawa, 2012, Higher brain centers for social tasks in worker ants, Camponotus japonicus, J. Comp. Neurol., 520, 1584, 10.1002/cne.23001 Nishino, 2003, Projection neurons originating from thermo- and hygrosensory glomeruli in the antennal lobe of the cockroach, J. Comp. Neurol., 455, 40, 10.1002/cne.10450 Nishino, 2012, Visual and olfactory input segregation in the mushroom body calyces in a basal neopteran, the American cockroach, Arthropod Struct. Dev., 41, 3, 10.1016/j.asd.2011.08.005 Oginsky, 2010, D2 receptors receive paracrine neurotransmission and are consistently targeted to a subset of synaptic structures in an identified neuron of the crustacean stomatogastric nervous system, J. Comp. Neurol., 518, 255, 10.1002/cne.22225 Okada, 2009, Gamma-aminobutyric acid (GABA)-mediated neural connections in the Drosophila antennal lobe, J. Comp. Neurol., 514, 74, 10.1002/cne.21971 Ott, 2007, Enhanced fidelity of diffusive nitric oxide signalling by the spatial segregation of source and target neurones in the memory centre of an insect brain, Eur. J. Neurosci., 25, 181, 10.1111/j.1460-9568.2006.05271.x Owald, 2015, Activity of defined mushroom body output neurons underlies learned olfactory behavior in Drosophila, Neuron, 86, 417, 10.1016/j.neuron.2015.03.025 Pasch, 2011, CaMK II is differentially localized in synaptic regions of Kenyon cells within the mushroom bodies of the honeybee brain, J. Comp. Neurol., 519, 3700, 10.1002/cne.22683 Pearson, 1979, Local neurons and local interactions in the nervous system of invertebrates, 145 Pech, 2013, Localization of the contacts between Kenyon cells and aminergic neurons in the Drosophila melanogaster brain using SplitGFP reconstitution, J. Comp. Neurol., 521, 3992 Pech, 2015, Optical dissection of experience-dependent pre- and postsynaptic plasticity in the Drosophila brain, Cell Rep., 10, 2083, 10.1016/j.celrep.2015.02.065 Peters, 1987, Novel synaptic structures in the central nervous system of the locust Schistocerca gregaria, Cell Tiss. Res., 249, 341, 10.1007/BF00215518 Pfenninger, 1973, Synaptic Morphology and Cytochemistry, vol. 5 Prokop, 1999, Integrating bits and pieces: synapse structure and formation in Drosophila embryos, Cell Tiss. Res., 29, 169, 10.1007/s004410051345 Prokop, 2006, Development and structure of synaptic contacts in Drosophila, Semin. Cell Dev. Biol., 17, 20, 10.1016/j.semcdb.2005.11.010 Rensch, 1959, Trends towards progress of brains and sense organs, vol. 24, 291 Rössler, 2002, Aggregation of f-actin in olfactory glomeruli: a common feature of glomeruli across phyla, Chem. Senses, 27, 803, 10.1093/chemse/27.9.803 Rybak, 2003, Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe, J. Comp. Neurol., 334, 444, 10.1002/cne.903340309 Rybak, 2010, Mushroom body of the honey bee, 433 Rybak, 2010, The digital bee brain: integrating and managing neurons in a common 3D reference system, Front. Syst. Neurosci., 4, 30 y Sánchez, 1933, 149 Schildberger, 1984, Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells, J. Comp. Physiol. (A), 154, 71, 10.1007/BF00605392 Schmitt, 1979, The role of structural, electrical and chemical circuitry in brain function, 5 Schröter, 2003, A new ascending sensory tract to the calyces of the honeybee mushroom body, the suboesophageal-calycal tract, J. Comp. Neurol., 465, 168, 10.1002/cne.10843 Schürmann, 1970, Über die Struktur der Pilzkörper des Insektengehirns. I. Synapsen im Pedunculus, Z. Zellforsch., 103, 365, 10.1007/BF00335280 Schürmann, 1971, Synaptic contacts of association fibres in the brain of the bee, Brain Res., 26, 169, 10.1016/0006-8993(71)90552-X Schürmann, 1972, Über die Struktur der Pilzkörper des Insektengehirns. II. Synaptische Schaltungen im Alpha-Lobus des Heimchens Acheta domesticus L, Z. Zellforsch., 127, 240, 10.1007/BF00306806 Schürmann, 1973, Über die Struktur der Pilzkörper des Insektengehirns. III. Die Anatomie der Nervenfasern in den Corpora pedunculata bei Acheta domesticus L. (Orthopt.), Z. Zellforsch., 145, 247, 10.1007/BF00307391 Schürmann, 1974, Bemerkungen zur Funktion der Corpora pedunculata im Gehirn der Insekten aus morphologischer Sicht, Exp. Brain Res., 19, 406, 10.1007/BF00234464 Schürmann, 1987, The architecture of the mushroom bodies and related neuropils in the insect brain, 231 Schürmann, 1970, Synapsen im Antennenhügel von Locusta migratoria, Z. Zellforsch., 108, 563, 10.1007/BF00339659 Schürmann, 1987, Synaptic connectivity in the mushroom bodies of the honey bee brain: electron microscopy and immunocytochemistry of neuroactive compounds, 225 Schürmann, 1973, Zur Monoaminverteilung in den Corpora pedunculata des Gehirns von Acheta domesticus L. (Orthoptera, Insecta). Histochemische Untersuchungen mit Vergleichen zur Struktur und Ultrastruktur, Z. Zellforsch., 136, 393, 10.1007/BF00307042 Schürmann, 1984, Serotonin immunoreactive neurons in the brain of the honeybee, J. Comp. Neurol., 5, 570, 10.1002/cne.902250407 Schürmann, 1990, FMRF-amide-like immunoreactivity in the brain of the honeybee Apis mellifera: a light and electron microscopy study, Neurosci, 38, 797807, 10.1016/0306-4522(90)90072-C Schürmann, 1989, Dopamine-like immunoreactivity in the bee brain, Cell Tiss. Res., 256, 399, 10.1007/BF00218898 Schürmann, 2000, Glutamate-like immunoreactivity marks compartments of the mushroom bodies in the brain of the cricket, J. Comp. Neurol., 418, 227, 10.1002/(SICI)1096-9861(20000306)418:2<227::AID-CNE8>3.0.CO;2-H Schürmann, 2001, Dense core vesicles and non-synaptic exocytosis in the central body of the crayfish brain, Cell Tiss. Res., 265, 493, 10.1007/BF00340872 Schürmann, 2008, GABAergic synaptic connections in mushroom bodies of insect brains, Acta Biol. Hung, 59, 173, 10.1556/ABiol.59.2008.Suppl.26 Schwaerzel, 2002, Extinction antagonizes olfactory memory at the sub-cellular level, Neuron, 35, 951, 10.1016/S0896-6273(02)00832-2 Seid, 2005, Age related changes in the number and structure of synapses in the lip region of the mushroom bodies of the ant Pheidole dentata, J. Comp. Neurol., 488, 269, 10.1002/cne.20545 Seid, 2008, Ultrastructure and synaptic differences of the boutons of the projection neurons between the lip and collar regions of the mushroom bodies in the ant, Cataglyphis albicans, J. Comp. Neurol., 507, 1102, 10.1002/cne.21600 Shaw, 1986, Evolutionary progression at synaptic connections made by identified homologous neurones, Proc. Nat. Acad. Sci., 83, 79617975, 10.1073/pnas.83.20.7961 Shepherd, 2010 Shepherd, 2010, Olfactory bulb, 251 Shinomiya, 2011, Flybrain neuron database: a comprehensive database system of the Drosophila brain neurons, J. Comp. Neurol., 519, 807, 10.1002/cne.22540 Sigrist, 2011, Structural and functional plasticity of the cytoplasmic active zone, Curr. Opin. Neurobiol., 21, 144, 10.1016/j.conb.2010.08.012 Sinakevitch, 2001, Taurine-, aspartate- and glutamate-like immunoreactivity identifies chemically distinct subdivions of Kenyon cells in the cockroach mushroom body, J. Comp. Neurol., 439, 352, 10.1002/cne.1355 Sinakevitch, 2011, Distribution of the octopamine receptor AmOA1 in the honey bee brain, PLoS One, 6, e14536, 10.1371/journal.pone.0014536 Smith, 1967, The organization of the insect neuropile, 79 Steiger, 1967, Über den Feinbau des Neuropils im Corpus pedunculatum der Waldameise, Z. Zellforsch., 81, 511, 10.1007/BF00541012 Stieb, 2010, Visual experience and age affect synaptic organization in the mushroom bodies of the desert ant Cataglyphis fortis, Dev. Neurobiol., 70, 408, 10.1002/dneu.20785 Stocker, 1994, The organization of the chemosensory system in Drosophila melanogaster: a review, Cell Tiss. Res., 275, 3, 10.1007/BF00305372 Strambi, 1998, Immunocytochemically mapping of an RDL-like GABA Receptor subunit and of GABA in brain structures related to learning and memory in the cricket Acheta domesticus, Learn. Mem., 5, 78, 10.1101/lm.5.1.78 Strausfeld, 1976 Strausfeld, 2002, Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes, J. Comp. Neurol., 450, 4, 10.1002/cne.10285 Strausfeld, 2012 Strausfeld, 1983, Cobalt coupled neurons of a giant fibre system in Diptera, J. Neurocytol., 12, 971, 10.1007/BF01153345 Strausfeld, 1999, Organization of olfactory and multimodal afferent neurons supplying the calyx and pedunculus of the cockroach mushroom bodies, J. Comp. Neurol., 409, 603, 10.1002/(SICI)1096-9861(19990712)409:4<603::AID-CNE7>3.0.CO;2-P Strausfeld, 1999, Representation of the calyces in the medial and vertical lobes of cockroach mushroom bodies, J. Comp. Neurol., 409, 626, 10.1002/(SICI)1096-9861(19990712)409:4<626::AID-CNE8>3.0.CO;2-B Strausfeld, 1998, The insect neuron: types, morphologies, fine structure and relationship to the architectonics of the insect nervous system, vol. 11(B), 487 Strausfeld, 2003, The mushroom bodies of Drosophila melanogaster: an immunocytological and Golgi study of Kenyon cell organization in the calyces and lobes, Microsc. Res. Tech., 62, 151, 10.1002/jemt.10368 Strausfeld, 2009, Ground plan of the insect mushroom body: functional and evolutionary implications, J. Comp. Neurol., 513, 10.1002/cne.21948 Strausfeld, 1998, Evolution discovery and interpretations of arthropod mushroom bodies, Learn. Mem., 5, 11, 10.1101/lm.5.1.11 Sun, 1997, Synaptic organization of the uniglomerular projection neurons of the antennal lobe of the moth Manduca sexta: a laser scanning confocal and electron microscopic study, J. Comp. Neurol., 379, 2, 10.1002/(SICI)1096-9861(19970303)379:1<2::AID-CNE2>3.0.CO;2-8 Tanaka, 2008, Neuronal assemblies of the Drosophila mushroom body, J. Comp. Neurol., 508, 711, 10.1002/cne.21692 Tanaka, 2004, Integration of chemosensory pathways in the Drosphila second-order olfactory centers, Curr. Biol., 14, 449, 10.1016/j.cub.2004.03.006 Technau, 1982 Technau, 1984, Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience, J. Neurogen., 1, 113, 10.3109/01677068409107077 Technau, 1982, Neural reorganization during metamorhosis of the corpora pedunculata in Drosophila melanogaster, Nature, 295, 405, 10.1038/295405a0 Tolbert, 1981, Organization and synaptic ultrastructure of glomeruli in the antennal lobes of the moth Manduca sexta: a study using thin sections and freeze-fracture, Proc. R. Soc. Lond. B, 213, 279301 Trujillo-Cenoz, 1962, Electron microscope observations on the calyces of the insect brain, J. Ultrastruct. Res., 7, 389, 10.1016/S0022-5320(62)90035-7 Turner, 2008, Olfactory representations by Drosophila mushroom body neurons, J. Neurophysiol., 99, 734, 10.1152/jn.01283.2007 Ude, 1998, Submicroscopic characterization of proctolin-like immunoreactivity in the nervous system of the cockroach Periplaneta americana L, Cell Tiss. Res., 254, 197 Ude, 1995, FMRFamide-like and allatostatin-like immunoreactivity in the lateral heart nerve of Periplaneta americana: colocalization at the electronmicroscopic level, Cell Tiss. Res., 282, 69, 10.1007/BF00319134 Vizi, 1991, Non-synaptic interactions at presynaptic level, Prog. Neurobiol., 37, 145, 10.1016/0301-0082(91)90025-V Vogt, 2014, Shared mushroom body circuits underlie visual and olfactory memories in Drosophila, eLife, 3, e02395, 10.7554/eLife.02395 Vowles, 1955, The structure and connections of the corpora pedunculata in bees and ants, Q. J. Microsc. Sci., 96, 239 Waddell, 2010, Dopamine reveals neural circuit mechanisms of fly memory, Trends Neurosci., 33, 457, 10.1016/j.tins.2010.07.001 Waddell, 2013, Reinforcement signalling in Drosophila; dopamine does it all after all, Curr. Opin. Neurobiol., 23, 324, 10.1016/j.conb.2013.01.005 Wagh, 2006, Bruchpilot, a protein with homology to LKS/CAST, is required for structural integrity and function of synaptic active zone in Drosophila, Neuron, 49, 833, 10.1016/j.neuron.2006.02.008 Wang, 2004, Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging, J. Neurosci., 24, 6507, 10.1523/JNEUROSCI.3727-03.2004 Watson, 2002, Synaptic structure distribution and circuitry in the central nervous system of the locust and related insects, Microsc. Res. Tech., 56, 210, 10.1002/jemt.10031 Witthöft, 1967, Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene, Z. für Morphol. Tiere, 61, 160, 10.1007/BF00298776 Wood, 1977, Two types of presynaptic configurations in insect central synapses: an ultrastructural analysis, Brain Res., 130, 25, 10.1016/0006-8993(77)90840-X Xia, 2005, NMDA receptors mediate olfactory learning and memory in Drosophila, Curr. Biol., 15, 603, 10.1016/j.cub.2005.02.059 Yasuyama, 2010, Synaptic connections of PDFimmunoreactive lateral neurons projecting to the dorsal protocerebrum of Drosophila melanogaster, J. Comp. Neurol., 518, 292, 10.1002/cne.22210 Yasuyama, 2002, Synaptic organization of the mushroom body calyx in Drosophila melanogaster, J. Comp. Neurol., 445, 211, 10.1002/cne.10155 Yasuyama, 2003, Synaptic connections of cholinergic antennal lobe relay neurons innervating the lateral horn neuropile in the brain of Drosophila melanogaster, J. Comp. Neurol., 466, 299, 10.1002/cne.10867 Yew, 2009, Analysis of neuropeptide expression and localization in adult Drosophila melanogaster central nervous system by affinity cell-capture mass spectrometry, J. Proteome Res., 8, 1271, 10.1021/pr800601x Yu, 2005, Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning, Cell, 123, 945, 10.1016/j.cell.2005.09.037 Zars, 2000, Behavioral functions of the insect mushroom bodies, Curr. Opin. Neurobiol., 10, 790, 10.1016/S0959-4388(00)00147-1 Zhao, 2008, Metamorphosis and adult development of the mushroom bodies of the red flour beetle, Tribolium castaneum, Dev. Neurobiol., 68, 1487, 10.1002/dneu.20669