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Takeo Kubo - One of the best experts on this subject based on the ideXlab platform.
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Kenyon Cell subtypes populations in the honeybee mushroom bodies possible function based on their gene expression profiles differentiation possible evolution and application of genome editing
Frontiers in Psychology, 2018Co-Authors: Shota Suenami, Satoyo Oya, Hiroki Kohno, Takeo KuboAbstract:Honey bees are eusocial insects and the workers inform their nestmates of information regarding the location of food source using symbolic communication, called ‘dance communication’, that are based on their highly advanced learning abilities. Mushroom bodies (MBs), a higher-order center in the honey bee brain, comprise some subtypes/populations of interneurons termed Kenyon Cells (KCs) that are distinguished by their Cell body size and location in the MBs, as well as their gene expression profiles. Although the role of MBs in learning ability has been studied extensively in the honey bee, the roles of each KC subtype and their evolution in hymenopteran insects remain mostly unknown. This mini-review describes recent progress in the analysis of gene/protein expression profiles and possible functions of KC subtypes/populations in the honey bee. Especially, the discovery of novel KC subtype/population, ‘middle-type KCs’ and ‘KC population expressing FoxP’, necessitated a redefinition of the KC subtype/population. Analysis of the effects of inhibiting gene function in a KC subtype-preferential manner revealed the function of the gene product as well as of the subtype where it is expressed. Genes expressed in a KC subtype/population-preferential manner can be used to trace the differentiation of KC subtypes during the honey bee ontogeny and the possible evolution of KC subtypes in hymenopteran insects. Current findings suggest that the three KC subtypes are unique characteristics to the aculeate hymenopteran insects. Finally, recent application of genome editing for the study of KC subtype functions in the honey bee is described. Genes expressed in a KC subtype-preferential manner can be good candidate target genes for genome editing, because they are likely related to highly advanced brain functions and some of them are dispensable for normal development and sexual maturation in honey bees.
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Kenyon Cell subtypes populations in the honeybee mushroom bodies possible function based on their gene expression profiles differentiation possible evolution and application of genome editing
Frontiers in Psychology, 2018Co-Authors: Shota Suenami, Satoyo Oya, Hiroki Kohno, Takeo KuboAbstract:Mushroom bodies (MBs), a higher-order center in the honeybee brain, comprise some subtypes/populations of interneurons termed as Kenyon Cells (KCs), which are distinguished by their Cell body size and location in the MBs, as well as their gene expression profiles. Although the role of MBs in learning ability has been studied extensively in the honeybee, the roles of each KC subtype and their evolution in hymenopteran insects remain mostly unknown. This mini-review describes recent progress in the analysis of gene/protein expression profiles and possible functions of KC subtypes/populations in the honeybee. Especially, the discovery of novel KC subtypes/populations, the "middle-type KCs" and "KC population expressing FoxP," necessitated a redefinition of the KC subtype/population. Analysis of the effects of inhibiting gene function in a KC subtype-preferential manner revealed the function of the gene product as well as of the KC subtype where it is expressed. Genes expressed in a KC subtype/population-preferential manner can be used to trace the differentiation of KC subtypes during the honeybee ontogeny and the possible evolution of KC subtypes in hymenopteran insects. Current findings suggest that the three KC subtypes are unique characteristics to the aculeate hymenopteran insects. Finally, prospects regarding future application of genome editing for the study of KC subtype functions in the honeybee are described. Genes expressed in a KC subtype-preferential manner can be good candidate target genes for genome editing, because they are likely related to highly advanced brain functions and some of them are dispensable for normal development and sexual maturation in honeybees.
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Kenyon Cell Subtypes/Populations in the Honeybee Mushroom Bodies: Possible Function Based on Their Gene Expression Profiles, Differentiation, Possible Evolution, and Application of Genome Editing
'Frontiers Media SA', 2018Co-Authors: Shota Suenami, Satoyo Oya, Hiroki Kohno, Takeo KuboAbstract:Mushroom bodies (MBs), a higher-order center in the honeybee brain, comprise some subtypes/populations of interneurons termed as Kenyon Cells (KCs), which are distinguished by their Cell body size and location in the MBs, as well as their gene expression profiles. Although the role of MBs in learning ability has been studied extensively in the honeybee, the roles of each KC subtype and their evolution in hymenopteran insects remain mostly unknown. This mini-review describes recent progress in the analysis of gene/protein expression profiles and possible functions of KC subtypes/populations in the honeybee. Especially, the discovery of novel KC subtypes/populations, the “middle-type KCs” and “KC population expressing FoxP,” necessitated a redefinition of the KC subtype/population. Analysis of the effects of inhibiting gene function in a KC subtype-preferential manner revealed the function of the gene product as well as of the KC subtype where it is expressed. Genes expressed in a KC subtype/population-preferential manner can be used to trace the differentiation of KC subtypes during the honeybee ontogeny and the possible evolution of KC subtypes in hymenopteran insects. Current findings suggest that the three KC subtypes are unique characteristics to the aculeate hymenopteran insects. Finally, prospects regarding future application of genome editing for the study of KC subtype functions in the honeybee are described. Genes expressed in a KC subtype-preferential manner can be good candidate target genes for genome editing, because they are likely related to highly advanced brain functions and some of them are dispensable for normal development and sexual maturation in honeybees
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Increased complexity of mushroom body Kenyon Cell subtypes in the brain is associated with behavioral evolution in hymenopteran insects
Nature Publishing Group, 2017Co-Authors: Satoyo Oya, Hiroki Kohno, Yooichi Kainoh, Masato Ono, Takeo KuboAbstract:Abstract In insect brains, the mushroom bodies (MBs) are a higher-order center for sensory integration and memory. Honeybee (Apis mellifera L.) MBs comprise four Kenyon Cell (KC) subtypes: class I large-, middle-, and small-type, and class II KCs, which are distinguished by the size and location of somata, and gene expression profiles. Although these subtypes have only been reported in the honeybee, the time of their acquisition during evolution remains unknown. Here we performed in situ hybridization of tachykinin-related peptide, which is differentially expressed among KC subtypes in the honeybee MBs, in four hymenopteran species to analyze whether the complexity of KC subtypes is associated with their behavioral traits. Three class I KC subtypes were detected in the MBs of the eusocial hornet Vespa mandarinia and the nidificating scoliid wasp Campsomeris prismatica, like in A. mellifera, whereas only two class I KC subtypes were detected in the parasitic wasp Ascogaster reticulata. In contrast, we were unable to detect class I KC subtype in the primitive and phytophagous sawfly Arge similis. Our findings suggest that the number of class I KC subtypes increased at least twice – first with the evolution of the parasitic lifestyle and then with the evolution of nidification
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Gene expression profiles and neural activities of Kenyon Cell subtypes in the honeybee brain: identification of novel ‘middle-type’ Kenyon Cells
Zoological Letters, 2016Co-Authors: Kumi Kaneko, Shota Suenami, Takeo KuboAbstract:In the honeybee ( Apis mellifera L.), it has long been thought that the mushroom bodies, a higher-order center in the insect brain, comprise three distinct subtypes of intrinsic neurons called Kenyon Cells. In class-I large-type Kenyon Cells and class-I small-type Kenyon Cells, the somata are localized at the edges and in the inner core of the mushroom body calyces, respectively. In class-II Kenyon Cells, the somata are localized at the outer surface of the mushroom body calyces. The gene expression profiles of the large- and small-type Kenyon Cells are distinct, suggesting that each exhibits distinct Cellular characteristics. We recently identified a novel gene, mKast ( middle-type Kenyon Cell-preferential arrestin-related gene-1 ), which has a distinctive expression pattern in the Kenyon Cells. Detailed expression analyses of mKast led to the discovery of novel ‘middle-type’ Kenyon Cells characterized by their preferential mKast -expression in the mushroom bodies. The somata of the middle-type Kenyon Cells are localized between the large- and small-type Kenyon Cells, and the size of the middle-type Kenyon Cell somata is intermediate between that of large- and small-type Kenyon Cells. Middle-type Kenyon Cells appear to differentiate from the large- and/or small-type Kenyon Cell lineage(s). Neural activity mapping using an immediate early gene, kakusei , suggests that the small-type and some middle-type Kenyon Cells are prominently active in the forager brain, suggesting a potential role in processing information during foraging flight. Our findings indicate that honeybee mushroom bodies in fact comprise four types of Kenyon Cells with different molecular and Cellular characteristics: the previously known class-I large- and small-type Kenyon Cells, class-II Kenyon Cells, and the newly identified middle-type Kenyon Cells described in this review. As the Cellular characteristics of the middle-type Kenyon Cells are distinct from those of the large- and small-type Kenyon Cells, their careful discrimination will be required in future studies of honeybee Kenyon Cell subtypes. In this review, we summarize recent progress in analyzing the gene expression profiles and neural activities of the honeybee Kenyon Cell subtypes, and discuss possible roles of each Kenyon Cell subtype in the honeybee brain.
Sarah M. Farris - One of the best experts on this subject based on the ideXlab platform.
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evolution of insect mushroom bodies old clues new insights
Arthropod Structure & Development, 2005Co-Authors: Sarah M. FarrisAbstract:Abstract The mushroom bodies are a morphologically diverse sensory integration and learning and memory center in the brains of various invertebrate species, of which those of insects are the best described. Insect mushroom bodies are composed of numerous tiny intrinsic neurons (Kenyon Cells) that form calyces with their dendrites and a pedunculus and lobes with their axons. The identities of conserved Kenyon Cell subpopulations and the correlations between morphological and functional specializations of the mushroom bodies are just beginning to be elucidated, providing insight into mechanisms of mushroom body evolution. Comparisons of mushroom body organization in different insect lineages reveal trends in the evolution of subcompartments correlated with the elaboration, reduction, acquisition or loss of Kenyon Cell subpopulations. Furthermore, these changes often appear correlated with variation in type and strength of afferent input and in behavioral ecology. These and other features of mushroom body organization suggest a striking convergence with mammalian cortex, with Kenyon Cell subpopulations displaying evolutionary modularity in a manner reminiscent of cortical areas.
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Developmental organization of the mushroom bodies of Thermobia domestica (Zygentoma, Lepismatidae): insights into mushroom body evolution from a basal insect
Evolution & development, 2005Co-Authors: Sarah M. FarrisAbstract:The mushroom bodies of the insect brain are sensory integration centers best studied for their role in learning and memory. Studies of mushroom body structure and development in neopteran insects have revealed conserved morphogenetic mechanisms. The sequential production of morphologically distinct intrinsic neuron (Kenyon Cell) subpopulations by mushroom body neuroblasts and the integration of newborn neurons via a discrete ingrowth tract results in an age-based organization of modular subunits in the primary output neuropil of the mushroom bodies, the lobes. To determine whether these may represent ancestral characteristics, the present account assesses mushroom body organization and development in the basal wingless insect Thermobia domestica. In this insect, a single calyx supplied by the progeny of two neuroblast clusters, and three perpendicularly oriented lobes are readily identifiable. The lobes are subdivided into 15 globular subdivisions (Trauben). Lifelong neurogenesis is observed, with axons of newborn Kenyon Cells entering the lobes via an ingrowth core. The Trauben do not appear progressively during development, indicating that they do not represent the ramifications of sequentially produced subpopulations of Kenyon Cells. Instead, a single Kenyon Cell population produces highly branched axons that supply all lobe subdivisions. This suggests that although the ground plan for neopteran mushroom bodies existed in early insects, the organization of modular subunits composed of separate Kenyon Cell subpopulations is a later innovation. Similarities between the calyx of Thermobia and the highly derived fruit fly Drosophila melanogaster also suggest a correlation between calyx morphology and Kenyon Cell number.
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Development of laminar organization in the mushroom bodies of the cockroach: Kenyon Cell proliferation, outgrowth, and maturation.
The Journal of comparative neurology, 2001Co-Authors: Sarah M. Farris, Nicholas J. StrausfeldAbstract:The mushroom bodies of the insect brain are lobed integration centers made up of tens of thousands of parallel-projecting axons of intrinsic (Kenyon) Cells. Most of the axons in the medial and vertical lobes of adult cockroach mushroom bodies derive from class I Kenyon Cells and are organized into regular, alternating pairs (doublets) of pale and dark laminae. Organization of Kenyon Cell axons into the adult pattern of laminae occurs gradually over the course of nymphal development. Newly hatched nymphs possess tiny mushroom bodies with lobes containing a posterior lamina of ingrowing axons, followed by a single doublet, which is flanked anteriorly by a γ layer composed of class II Kenyon Cells. Golgi impregnations show that throughout nymphal development, regardless of the number of doublets present, the most posterior lamina serves as the “ingrowth lamina” for axons of newborn Kenyon Cells. Axons of the ingrowth lamina are taurine- and synaptotagmin-immunonegative. They produce fine growth cone tipped filaments and long perpendicularly oriented collaterals along their length. The maturation of these Kenyon Cells and the formation of a new lamina are marked by the loss of filaments and collaterals, as well as the onset of taurine and synaptotagmin expression. Class I Kenyon Cells thus show plasticity in both morphology and transmitter expression during development. In a hemimetabolous insect such as the cockroach, juvenile stages are morphologically and behaviorally similar to the adult. The mushroom bodies of these insects must be functional from hatching onward, while thousands of new neurons are added to the existing structure. The observed developmental plasticity may serve as a mechanism by which extensive postembryonic development of the mushroom bodies can occur without disrupting function. This contrasts with the more evolutionarily derived holometabolous insects, such as the honey bee and the fruit fly, in which nervous system development is accomplished in a behaviorally simple larval stage and a quiescent pupal stage. J. Comp. Neurol. 430:331–351, 2001. © 2001 Wiley-Liss, Inc.
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experience and age related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee
The Journal of Neuroscience, 2001Co-Authors: Sarah M. Farris, Gene E Robinson, Susan E. FahrbachAbstract:A worker honeybee performs tasks within the hive for approximately the first 3 weeks of adult life. After this time, it becomes a forager, flying repeatedly to collect food outside of the hive for the remainder of its 5–6 week life. Previous studies have shown that foragers have an increased volume of neuropil associated with the mushroom bodies, a brain region involved in learning, memory, and sensory integration. We report here that growth of the mushroom body neuropil in adult bees occurs throughout adult life and continues after bees begin to forage. Studies using Golgi impregnation asked whether the growth of the collar region of the mushroom body neuropil was a result of growth of the dendritic processes of the mushroom body intrinsic neurons, the Kenyon Cells. Branching and length of dendrites in the collar region of the calyces were strongly correlated with worker age, but when age-matched bees were directly compared, those with foraging experience had longer, more branched dendrites than bees that had foraged less or not at all. The density of Kenyon Cell dendritic spines remained constant regardless of age or behavioral state. Older and more experienced foragers therefore have a greater total number of dendritic spines in the mushroom body neuropil. Our findings indicate that, under natural conditions, the cytoarchitectural complexity of neurons in the mushroom bodies of adult honeybees increases as a function of increasing age, but that foraging experience promotes additional dendritic branching and growth.
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larval and pupal development of the mushroom bodies in the honey bee apis mellifera
The Journal of Comparative Neurology, 1999Co-Authors: Sarah M. Farris, Ronald L Davis, Gene E Robinson, Susan E. FahrbachAbstract:The mushroom bodies are paired neuropils in the insect brain that act as multimodal sensory integration centers and are involved in learning and memory. Our studies, by using 5-bromo-2-deoxyuridine incorporation and the Feulgen technique, show that immediately before pupation, the brain of the developing honey bee (Apis mellifera) contains approximately 2,000 neuroblasts devoted to the production of the mushroom body intrinsic neurons (Kenyon Cells). These neuroblasts are descended from four clusters of 45 or fewer neuroblasts each already present in the newly hatched larva. Subpopulations of Kenyon Cells, distinct in cytoarchitecture, position, and immunohistochemical traits, are born at different, but overlapping, periods during the development of the mushroom bodies, with the final complement of these neurons in place by the mid-pupal stage. The mushroom bodies of the adult honey bee have a concentric arrangement of Kenyon Cell types, with the outer layers born first and pushed to the periphery by later born neurons that remain nearer the center of proliferation. This concentricity is further reflected in morphologic and immunohistochemical traits of the adult neurons, and is demonstrated clearly by the pattern of expression of Drosophila myocyte enhancer factor 2 (DMEF2)-like immunoreactivity. This is the first comprehensive study of larval and pupal development of the honey bee mushroom bodies. Similarities to patterns of neurogenesis observed in the mushroom bodies of other insects and in the vertebrate cerebral cortex are discussed. J. Comp. Neurol. 414:97–113, 1999. © 1999 Wiley-Liss, Inc.
Susan E. Fahrbach - One of the best experts on this subject based on the ideXlab platform.
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Muscarinic regulation of Kenyon Cell dendritic arborizations in adult worker honey bees.
Arthropod Structure & Development, 2011Co-Authors: Scott E. Dobrin, J. Daniel Herlihy, Susan E. FahrbachAbstract:The experience of foraging under natural conditions increases the volume of mushroom body neuropil in worker honey bees. A comparable increase in neuropil volume results from treatment of worker honey bees with pilocarpine, an agonist for muscarinic-type cholinergic receptors. A component of the neuropil growth induced by foraging experience is growth of dendrites in the collar region of the calyces. We show here, via analysis of Golgi-impregnated collar Kenyon Cells with wedge arborizations, that significant increases in standard measures of dendritic complexity were also found in worker honey bees treated with pilocarpine. This result suggests that signaling via muscarinic-type receptors promotes the increase in Kenyon Cell dendritic complexity associated with foraging. Treatment of worker honey bees with scopolamine, a muscarinic inhibitor, inhibited some aspects of dendritic growth. Spine density on the Kenyon Cell dendrites varied with sampling location, with the distal portion of the dendritic field having greater total spine density than either the proximal or medial section. This observation may be functionally significant because of the stratified organization of projections from visual centers to the dendritic arborizations of the collar Kenyon Cells. Pilocarpine treatment had no effect on the distribution of spines on dendrites of the collar Kenyon Cells.
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experience and age related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee
The Journal of Neuroscience, 2001Co-Authors: Sarah M. Farris, Gene E Robinson, Susan E. FahrbachAbstract:A worker honeybee performs tasks within the hive for approximately the first 3 weeks of adult life. After this time, it becomes a forager, flying repeatedly to collect food outside of the hive for the remainder of its 5–6 week life. Previous studies have shown that foragers have an increased volume of neuropil associated with the mushroom bodies, a brain region involved in learning, memory, and sensory integration. We report here that growth of the mushroom body neuropil in adult bees occurs throughout adult life and continues after bees begin to forage. Studies using Golgi impregnation asked whether the growth of the collar region of the mushroom body neuropil was a result of growth of the dendritic processes of the mushroom body intrinsic neurons, the Kenyon Cells. Branching and length of dendrites in the collar region of the calyces were strongly correlated with worker age, but when age-matched bees were directly compared, those with foraging experience had longer, more branched dendrites than bees that had foraged less or not at all. The density of Kenyon Cell dendritic spines remained constant regardless of age or behavioral state. Older and more experienced foragers therefore have a greater total number of dendritic spines in the mushroom body neuropil. Our findings indicate that, under natural conditions, the cytoarchitectural complexity of neurons in the mushroom bodies of adult honeybees increases as a function of increasing age, but that foraging experience promotes additional dendritic branching and growth.
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larval and pupal development of the mushroom bodies in the honey bee apis mellifera
The Journal of Comparative Neurology, 1999Co-Authors: Sarah M. Farris, Ronald L Davis, Gene E Robinson, Susan E. FahrbachAbstract:The mushroom bodies are paired neuropils in the insect brain that act as multimodal sensory integration centers and are involved in learning and memory. Our studies, by using 5-bromo-2-deoxyuridine incorporation and the Feulgen technique, show that immediately before pupation, the brain of the developing honey bee (Apis mellifera) contains approximately 2,000 neuroblasts devoted to the production of the mushroom body intrinsic neurons (Kenyon Cells). These neuroblasts are descended from four clusters of 45 or fewer neuroblasts each already present in the newly hatched larva. Subpopulations of Kenyon Cells, distinct in cytoarchitecture, position, and immunohistochemical traits, are born at different, but overlapping, periods during the development of the mushroom bodies, with the final complement of these neurons in place by the mid-pupal stage. The mushroom bodies of the adult honey bee have a concentric arrangement of Kenyon Cell types, with the outer layers born first and pushed to the periphery by later born neurons that remain nearer the center of proliferation. This concentricity is further reflected in morphologic and immunohistochemical traits of the adult neurons, and is demonstrated clearly by the pattern of expression of Drosophila myocyte enhancer factor 2 (DMEF2)-like immunoreactivity. This is the first comprehensive study of larval and pupal development of the honey bee mushroom bodies. Similarities to patterns of neurogenesis observed in the mushroom bodies of other insects and in the vertebrate cerebral cortex are discussed. J. Comp. Neurol. 414:97–113, 1999. © 1999 Wiley-Liss, Inc.
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larval and pupal development of the mushroom bodies in the honey bee apis mellifera
The Journal of Comparative Neurology, 1999Co-Authors: Sarah M. Farris, Ronald L Davis, Gene E Robinson, Susan E. FahrbachAbstract:The mushroom bodies are paired neuropils in the insect brain that act as multimodal sensory integration centers and are involved in learning and memory. Our studies, by using 5-bromo-2-deoxyuridine incorporation and the Feulgen technique, show that immediately before pupation, the brain of the developing honey bee (Apis mellifera) contains approximately 2,000 neuroblasts devoted to the production of the mushroom body intrinsic neurons (Kenyon Cells). These neuroblasts are descended from four clusters of 45 or fewer neuroblasts each already present in the newly hatched larva. Subpopulations of Kenyon Cells, distinct in cytoarchitecture, position, and immunohistochemical traits, are born at different, but overlapping, periods during the development of the mushroom bodies, with the final complement of these neurons in place by the mid-pupal stage. The mushroom bodies of the adult honey bee have a concentric arrangement of Kenyon Cell types, with the outer layers born first and pushed to the periphery by later born neurons that remain nearer the center of proliferation. This concentricity is further reflected in morphologic and immunohistochemical traits of the adult neurons, and is demonstrated clearly by the pattern of expression of Drosophila myocyte enhancer factor 2 (DMEF2)-like immunoreactivity. This is the first comprehensive study of larval and pupal development of the honey bee mushroom bodies. Similarities to patterns of neurogenesis observed in the mushroom bodies of other insects and in the vertebrate cerebral cortex are discussed. J. Comp. Neurol. 414:97–113, 1999. © 1999 Wiley-Liss, Inc.
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effects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees
Journal of Neurobiology, 1995Co-Authors: Ginger S. Withers, Susan E. Fahrbach, Gene E RobinsonAbstract:There is an age-related division of labor in the honey bee colony that is regulated by juvenile hormone. After completing metamorphosis, young workers have low titers of juvenile hormone and spend the first several weeks of their adult lives performing tasks within the hive. Older workers, approximately 3 weeks of age, have high titers of juvenile hormone and forage outside the hive for nectar and pollen. We have previously reported that changes in the volume of the mushroom bodies of the honey bee brain are temporally associated with the performance of foraging. The neuropil of the mushroom bodies is increased in volume, whereas the volume occupied by the somata of the Kenyon Cells is significantly decreased in foragers relative to younger workers. To study the effect of flight experience and juvenile hormone on these changes within the mushroom bodies, young worker bees were treated with the juvenile hormone analog methoprene but a subset was prevented from foraging (big back bees). Stereological volume estimates revealed that, regardless of foraging experience, bees treated with methoprene had a significantly larger volume of neuropil in the mushroom bodies and a significantly smaller Kenyon Cell somal region volume than did 1-day-old bees. The bees treated with methoprene did not differ on these volume estimates from untreated foragers (presumed to have high endogenous levels of juvenile hormone) of the same age sampled from the same colony. Bees prevented from flying and foraging nonetheless received visual stimulation as they gathered at the hive entrance. These results, coupled with a subregional analysis of the neuropil, suggest a potentially important role of visual stimulation, possibly interacting with juvenile hormone, as an organizer of the mushroom bodies. In an independent study, the brains of worker bees in which the transition to foraging was delayed (overaged nurse bees) were also studied. The mushroom bodies of overaged nurse bees had a Kenyon Cell somal region volume typical of normal aged nurse bees. However, they displayed a significantly expanded neuropil relative to normal aged nurse bees. Analysis of the big back bees demonstrates that certain aspects of adult brain plasticity associated with foraging can be displayed by worker bees treated with methoprene independent of foraging experience. Analysis of the over-aged nurse bees suggests that the post-metamorphic expansion of the neuropil of the mushroom bodies of worker honey bees is not a result of foraging experience. © 1995 John Wiley & Sons, Inc.
Shota Suenami - One of the best experts on this subject based on the ideXlab platform.
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Kenyon Cell subtypes populations in the honeybee mushroom bodies possible function based on their gene expression profiles differentiation possible evolution and application of genome editing
Frontiers in Psychology, 2018Co-Authors: Shota Suenami, Satoyo Oya, Hiroki Kohno, Takeo KuboAbstract:Honey bees are eusocial insects and the workers inform their nestmates of information regarding the location of food source using symbolic communication, called ‘dance communication’, that are based on their highly advanced learning abilities. Mushroom bodies (MBs), a higher-order center in the honey bee brain, comprise some subtypes/populations of interneurons termed Kenyon Cells (KCs) that are distinguished by their Cell body size and location in the MBs, as well as their gene expression profiles. Although the role of MBs in learning ability has been studied extensively in the honey bee, the roles of each KC subtype and their evolution in hymenopteran insects remain mostly unknown. This mini-review describes recent progress in the analysis of gene/protein expression profiles and possible functions of KC subtypes/populations in the honey bee. Especially, the discovery of novel KC subtype/population, ‘middle-type KCs’ and ‘KC population expressing FoxP’, necessitated a redefinition of the KC subtype/population. Analysis of the effects of inhibiting gene function in a KC subtype-preferential manner revealed the function of the gene product as well as of the subtype where it is expressed. Genes expressed in a KC subtype/population-preferential manner can be used to trace the differentiation of KC subtypes during the honey bee ontogeny and the possible evolution of KC subtypes in hymenopteran insects. Current findings suggest that the three KC subtypes are unique characteristics to the aculeate hymenopteran insects. Finally, recent application of genome editing for the study of KC subtype functions in the honey bee is described. Genes expressed in a KC subtype-preferential manner can be good candidate target genes for genome editing, because they are likely related to highly advanced brain functions and some of them are dispensable for normal development and sexual maturation in honey bees.
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Kenyon Cell subtypes populations in the honeybee mushroom bodies possible function based on their gene expression profiles differentiation possible evolution and application of genome editing
Frontiers in Psychology, 2018Co-Authors: Shota Suenami, Satoyo Oya, Hiroki Kohno, Takeo KuboAbstract:Mushroom bodies (MBs), a higher-order center in the honeybee brain, comprise some subtypes/populations of interneurons termed as Kenyon Cells (KCs), which are distinguished by their Cell body size and location in the MBs, as well as their gene expression profiles. Although the role of MBs in learning ability has been studied extensively in the honeybee, the roles of each KC subtype and their evolution in hymenopteran insects remain mostly unknown. This mini-review describes recent progress in the analysis of gene/protein expression profiles and possible functions of KC subtypes/populations in the honeybee. Especially, the discovery of novel KC subtypes/populations, the "middle-type KCs" and "KC population expressing FoxP," necessitated a redefinition of the KC subtype/population. Analysis of the effects of inhibiting gene function in a KC subtype-preferential manner revealed the function of the gene product as well as of the KC subtype where it is expressed. Genes expressed in a KC subtype/population-preferential manner can be used to trace the differentiation of KC subtypes during the honeybee ontogeny and the possible evolution of KC subtypes in hymenopteran insects. Current findings suggest that the three KC subtypes are unique characteristics to the aculeate hymenopteran insects. Finally, prospects regarding future application of genome editing for the study of KC subtype functions in the honeybee are described. Genes expressed in a KC subtype-preferential manner can be good candidate target genes for genome editing, because they are likely related to highly advanced brain functions and some of them are dispensable for normal development and sexual maturation in honeybees.
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Kenyon Cell Subtypes/Populations in the Honeybee Mushroom Bodies: Possible Function Based on Their Gene Expression Profiles, Differentiation, Possible Evolution, and Application of Genome Editing
'Frontiers Media SA', 2018Co-Authors: Shota Suenami, Satoyo Oya, Hiroki Kohno, Takeo KuboAbstract:Mushroom bodies (MBs), a higher-order center in the honeybee brain, comprise some subtypes/populations of interneurons termed as Kenyon Cells (KCs), which are distinguished by their Cell body size and location in the MBs, as well as their gene expression profiles. Although the role of MBs in learning ability has been studied extensively in the honeybee, the roles of each KC subtype and their evolution in hymenopteran insects remain mostly unknown. This mini-review describes recent progress in the analysis of gene/protein expression profiles and possible functions of KC subtypes/populations in the honeybee. Especially, the discovery of novel KC subtypes/populations, the “middle-type KCs” and “KC population expressing FoxP,” necessitated a redefinition of the KC subtype/population. Analysis of the effects of inhibiting gene function in a KC subtype-preferential manner revealed the function of the gene product as well as of the KC subtype where it is expressed. Genes expressed in a KC subtype/population-preferential manner can be used to trace the differentiation of KC subtypes during the honeybee ontogeny and the possible evolution of KC subtypes in hymenopteran insects. Current findings suggest that the three KC subtypes are unique characteristics to the aculeate hymenopteran insects. Finally, prospects regarding future application of genome editing for the study of KC subtype functions in the honeybee are described. Genes expressed in a KC subtype-preferential manner can be good candidate target genes for genome editing, because they are likely related to highly advanced brain functions and some of them are dispensable for normal development and sexual maturation in honeybees
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Gene expression profiles and neural activities of Kenyon Cell subtypes in the honeybee brain: identification of novel ‘middle-type’ Kenyon Cells
Zoological Letters, 2016Co-Authors: Kumi Kaneko, Shota Suenami, Takeo KuboAbstract:In the honeybee ( Apis mellifera L.), it has long been thought that the mushroom bodies, a higher-order center in the insect brain, comprise three distinct subtypes of intrinsic neurons called Kenyon Cells. In class-I large-type Kenyon Cells and class-I small-type Kenyon Cells, the somata are localized at the edges and in the inner core of the mushroom body calyces, respectively. In class-II Kenyon Cells, the somata are localized at the outer surface of the mushroom body calyces. The gene expression profiles of the large- and small-type Kenyon Cells are distinct, suggesting that each exhibits distinct Cellular characteristics. We recently identified a novel gene, mKast ( middle-type Kenyon Cell-preferential arrestin-related gene-1 ), which has a distinctive expression pattern in the Kenyon Cells. Detailed expression analyses of mKast led to the discovery of novel ‘middle-type’ Kenyon Cells characterized by their preferential mKast -expression in the mushroom bodies. The somata of the middle-type Kenyon Cells are localized between the large- and small-type Kenyon Cells, and the size of the middle-type Kenyon Cell somata is intermediate between that of large- and small-type Kenyon Cells. Middle-type Kenyon Cells appear to differentiate from the large- and/or small-type Kenyon Cell lineage(s). Neural activity mapping using an immediate early gene, kakusei , suggests that the small-type and some middle-type Kenyon Cells are prominently active in the forager brain, suggesting a potential role in processing information during foraging flight. Our findings indicate that honeybee mushroom bodies in fact comprise four types of Kenyon Cells with different molecular and Cellular characteristics: the previously known class-I large- and small-type Kenyon Cells, class-II Kenyon Cells, and the newly identified middle-type Kenyon Cells described in this review. As the Cellular characteristics of the middle-type Kenyon Cells are distinct from those of the large- and small-type Kenyon Cells, their careful discrimination will be required in future studies of honeybee Kenyon Cell subtypes. In this review, we summarize recent progress in analyzing the gene expression profiles and neural activities of the honeybee Kenyon Cell subtypes, and discuss possible roles of each Kenyon Cell subtype in the honeybee brain.
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analysis of the differentiation of Kenyon Cell subtypes using three mushroom body preferential genes during metamorphosis in the honeybee apis mellifera l
PLOS ONE, 2016Co-Authors: Shota Suenami, Rajib Kumar Paul, Tomoko Fujiyuki, Hideaki Takeuchi, Genta Okude, Kenichi Shirai, Takeo KuboAbstract:The adult honeybee (Apis mellifera L.) mushroom bodies (MBs, a higher center in the insect brain) comprise four subtypes of intrinsic neurons: the class-I large-, middle-, and small-type Kenyon Cells (lKCs, mKCs, and sKCs, respectively), and class-II KCs. Analysis of the differentiation of KC subtypes during metamorphosis is important for the better understanding of the roles of KC subtypes related to the honeybee behaviors. In the present study, aiming at identifying marker genes for KC subtypes, we used a cDNA microarray to comprehensively search for genes expressed in an MB-preferential manner in the honeybee brain. Among the 18 genes identified, we further analyzed three genes whose expression was enriched in the MBs: phospholipase C epsilon (PLCe), synaptotagmin 14 (Syt14), and discs large homolog 5 (dlg5). Quantitative reverse transcription-polymerase chain reaction analysis revealed that expression of PLCe, Syt14, and dlg5 was more enriched in the MBs than in the other brain regions by approximately 31-, 6.8-, and 5.6-fold, respectively. In situ hybridization revealed that expression of both Syt14 and dlg5 was enriched in the lKCs but not in the mKCs and sKCs, whereas expression of PLCe was similar in all KC subtypes (the entire MBs) in the honeybee brain, suggesting that Syt14 and dlg5, and PLCe are available as marker genes for the lKCs, and all KC subtypes, respectively. In situ hybridization revealed that expression of PLCe is already detectable in the class-II KCs at the larval fifth instar feeding stage, indicating that PLCe expression is a characteristic common to the larval and adult MBs. In contrast, expression of both Syt14 and dlg5 became detectable at the day three pupa, indicating that Syt14 and dlg5 expressions are characteristic to the late pupal and adult MBs and the lKC specific molecular characteristics are established during the late pupal stages.
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growth and pruning of mushroom body Kenyon Cell dendrites during worker behavioral development in the paper wasp polybia aequatorialis hymenoptera vespidae
Neurobiology of Learning and Memory, 2009Co-Authors: Theresa A Jones, Nicole A Donlan, Sean OdonnellAbstract:Adult workers of some social insect species show dramatic behavioral changes as they pass through a sequence of task specializations. In the paper wasp, Polybia aequatorialis, female workers begin adult life within the nest tending brood, progress to maintaining and defending the nest exterior, and ultimately leave the nest to forage. The mushroom body (MB) calyx neuropil increases in volume as workers progress from in-nest to foraging tasks. In other social Hymenoptera (bees and ants), MB Kenyon Cell dendrites, axons and synapses change with the transition to foraging, but these neuronal effects had not been studied in wasps. Furthermore, the on-nest worker of Polybia wasps, an intermediate task specialization not identified in bees or ants, provides the opportunity to study pre-foraging worker class transitions. We asked whether Kenyon Cell dendritic arborization varies with the task specialization of Polybia workers observed in the field near Monteverde, Costa Rica. Golgi-impregnated arbors in the lip and collar calyces, which receive a predominance of olfactory and visual input, respectively, were quantified using Sholl’s concentric circles and a novel application of virtual spherical probes. Arbors of the lip varied in a manner reminiscent of honeybees, with foragers having the largest and in-nest workers having the smallest arbors. In contrast, arbors of the collar were largest in foragers but smallest in on-nest workers. Thus, progression through task specializations in P. aequatorialis involves subregion specific dendritic growth and regression in the MB neuropil. These results may reflect the sensitivity of Kenyon Cell dendritic structure to specialization dependent social and sensory experience.
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developmental and dominance associated differences in mushroom body structure in the paper wasp mischocyttarus mastigophorus
Developmental Neurobiology, 2007Co-Authors: Sean Odonnell, Nicole A Donlan, Theresa A JonesAbstract:Primitively eusocial paper wasps exhibit considerable plasticity in their division of labor. Dominance interactions among nest mates play a strong role in determining the task performance patterns of adult females. We asked whether dominance status and task performance differences were associated with the development of subregions of the mushroom bodies (MB) of female Mischocyttarus mastigophorus queens and workers. We found that the MB calycal neuropils were better developed (relative to the Kenyon Cell body layer) in the dominant females that spent more time on the nest. Increased MB calyx development was more strongly associated with social dominance than with high rates of foraging. The MB of queens resembled those of dominant workers. The results suggest that social interactions are particularly relevant to M. mastigophorus females' cognition. By examining the MB of newly emerged females, we also found evidence for significant age-related changes in MB structure.
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mushroom body structural change is associated with division of labor in eusocial wasp workers polybia aequatorialis hymenoptera vespidae
Neuroscience Letters, 2004Co-Authors: Sean Odonnell, Nicole A Donlan, Theresa A JonesAbstract:Abstract Highly eusocial insect workers exhibit age-related division of labor. Adults begin working inside the nest, moving to the nest periphery and later to foraging. Passage through this task sequence is associated with neuroanatomical changes in the mushroom bodies (MB) of honey bee (Apis) and ant (Camponotus) workers. We asked whether eusocial wasp workers (Polybia aequatorialis) exhibit similar changes in adult neuroanatomy. Wasps were identified as working in-nest, on-nest, or foraging. The volumes of the somata of workers’ MB intrinsic neurons (Kenyon Cells), and of the neuropils containing the Kenyon Cell dendritic arbors (calyces), were estimated using stereological methods. In-nest workers had significantly smaller calyx to Kenyon Cell volume ratios than on-nest and foraging workers. Age-related task specializations in Polybia workers are associated with major neuroanatomical reorganization in the mushroom bodies.
