Subdivisions of hymenopteran mushroom body calyces by their afferent supply
TL;DR: The data suggest that the many parallel channels of intrinsic neurons may each process different aspects of sensory input information within the mushroom body's calyx, which is particularly large in social Hymenoptera.
Abstract: The mushroom bodies are regions in the insect brain involved in processing complex multimodal information. They are composed of many parallel sets of intrinsic neurons that receive input from and transfer output to extrinsic neurons that connect the mushroom bodies with the surrounding neuropils. Mushroom bodies are particularly large in social Hymenoptera and are thought to be involved in the control of conspicuous orientation, learning, and memory capabilities of these insects. The present account compares the organization of sensory input to the mushroom body's calyx in different Hymenoptera. Tracer and conventional neuronal staining procedures reveal the following anatomic characteristics: The calyx comprises three subdivisions, the lip, collar, and basal ring. The lip receives antennal lobe afferents, and these olfactory input neurons can terminate in two or more segregated zones within the lip. The collar receives visual afferents that are bilateral with equal representation of both eyes in each calyx. Visual inputs provide two to three layers of processes in the collar subdivision. The basal ring is subdivided into two modality-specific zones, one receiving visual, the other antennal lobe input. Some overlap of modality exists between calycal subdivisions and within the basal ring, and the degree of segregation of sensory input within the calyx is species-specific. The data suggest that the many parallel channels of intrinsic neurons may each process different aspects of sensory input information.
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TL;DR: The author wished to relate the three phases of research on insects and to express insect sociology as population biology in this detailed survey of knowledge of insect societies.
Abstract: In his introduction to this detailed survey of knowledge of insect societies, the author points out that research on insect sociology has proceeded in three phases, the natural history phase, the physiological phase and the population-biology phase. Advances in the first two phases have permitted embarkation in the third phase on a more rigorous theory of social evolution based on population genetics and writing this book, the author wished to relate the three phases of research on insects and to express insect sociology as population biology. A glossary of terms, a considerable bibliography and a general index are included. Other CABI sites
1,394 citations
868 citations
TL;DR: It is shown that the age-related transition by honey bees from hive work to foraging is associated with an increase in the expression of the foraging (for) gene, which encodes a guanosine 3′,5′-monophosphate (cGMP)–dependent protein kinase (PKG).
Abstract: Genes can affect natural behavioral variation in different ways. Allelic variation causes alternative behavioral phenotypes, whereas changes in gene expression can influence the initiation of behavior at different ages. We show that the age-related transition by honey bees from hive work to foraging is associated with an increase in the expression of the foraging (for) gene, which encodes a guanosine 3',5'-monophosphate (cGMP)-dependent protein kinase (PKG). cGMP treatment elevated PKG activity and caused foraging behavior. Previous research showed that allelic differences in PKG expression result in two Drosophila foraging variants. The same gene can thus exert different types of influence on a behavior.
461 citations
TL;DR: The laminar arrangement of the Kenyon cell axons and segmented organization of the MBENs together divide the lobes into smaller synaptic units, possibly facilitating characteristic interaction between intrinsic and extrinsic neurons in each unit for different functional activities along the longitudinal lobe axes and between lobes.
Abstract: The mushroom body (MB) of the insect brain has important roles in odor learning and memory and in diverse other brain functions. To elucidate the anatomical basis underlying its function, we studied how the MB of Drosophila is organized by its intrinsic and extrinsic neurons. We screened for the GAL4 enhancer-trap strains that label specific subsets of these neurons and identified seven subtypes of Kenyon cells and three other intrinsic neuron types. Laminar organization of the Kenyon cell axons divides the pedunculus into at least five concentric strata. The alpha', beta', alpha, and beta lobes are each divided into three strata, whereas the gamma lobe appears more homogeneous. The outermost stratum of the alpha/beta lobes is specifically connected with a small, protruded subregion of the calyx, the accessory calyx, which does not receive direct olfactory input. As for the MB extrinsic neurons (MBENs), we found three types of antennal lobe projection neurons, among which two are novel. In addition, we resolved 17 other types of MBENs that arborize in the calyx, lobes, and pedunculus. Lobe-associated MBENs arborize in only specific areas of the lobes, being restricted along their longitudinal axes, forming two to five segmented zones in each lobe. The laminar arrangement of the Kenyon cell axons and segmented organization of the MBENs together divide the lobes into smaller synaptic units, possibly facilitating characteristic interaction between intrinsic and extrinsic neurons in each unit for different functional activities along the longitudinal lobe axes and between lobes. Structural differences between lobes are also discussed.
444 citations
Cites background from "Subdivisions of hymenopteran mushro..."
...…input from the AL, visual input from the optic lobe, and putative gustatory input from the SOG, with distinct input areas for each modality (Mobbs, 1982; Abel et al., 2001; Gronenberg, 1999, 2001; Ehmer and Gronenberg, 2002; Schröter and Menzel, 2003; Gronenberg and Lopez-Riquelme, 2004)....
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...…Rybak and Menzel, 1998; Grünewald, 1999; Strausfeld, 2002; Ehmer and Gronenberg, 2002; Schröter and Menzel, 2003; Kirschner et al., 2006), ants (Gronenberg, 1999, 2001; Gronenberg and Lopez-Riquelme, 2004), moth (Sjöholm et al., 2005, 2006; Rø et al., 2007), crickets (Schildberger, 1983;…...
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TL;DR: The present account shows that, although these zones are represented in the lobes, they occupy only two thirds of the vertical lobe, and suggests the need for critical reinterpretation of studies that have been predicated on early descriptions of the mushroom body's lobes.
Abstract: Studies of the mushroom bodies of Drosophila melanogaster have suggested that their gamma lobes specifically support short-term memory, whereas their vertical lobes are essential for long-term memory. Developmental studies have demonstrated that the Drosophila gamma lobe, like its equivalent in the cockroach Periplaneta americana, is supplied by a special class of intrinsic neuron-the clawed Kenyon cells-that are the first to differentiate during early development. To date, however, no account identifies a corresponding lobe in the honey bee, another taxon used extensively for learning and memory research. Received opinion is that, in this taxon, each of the mushroom body lobes comprises three parallel divisions representing one of three concentric zones of the calyces, called the lip, collar, and basal ring. The present account shows that, although these zones are represented in the lobes, they occupy only two thirds of the vertical lobe. Its lowermost third receives the axons of the clawed class II Kenyon cells, which are the first to differentiate during early development and which represent the whole calyx. This component of the lobe is anatomically and developmentally equivalent to the gamma lobe of Drosophila and has been here named the gamma lobe of the honey bee. A new class of intrinsic neurons, originating from perikarya distant from the mushroom body, provides a second system of parallel fibers from the calyx to the gamma lobe. A region immediately beneath the calyces, called the neck, is invaded by these neurons as well as by a third class of intrinsic cell that provides connections within the neck of the pedunculus and the basal ring of the calyces. In the honey bee, the gamma lobe is extensively supplied by afferents from the protocerebrum and gives rise to a distinctive class of efferent neurons. The terminals of these efferents target protocerebral neuropils that are distinct from those receiving efferents from divisions of the vertical lobe that represent the lip, collar, and basal ring. The identification of a gamma lobe unites the mushroom bodies of evolutionarily divergent taxa. The present findings suggest the need for critical reinterpretation of studies that have been predicated on early descriptions of the mushroom body's lobes.
307 citations
Cites background from "Subdivisions of hymenopteran mushro..."
...In the honey bee, but not in Drosophila, the visual system is represented in the calyces by the endings of projection neurons that separately originate from the medulla and lobula (Gronenberg 1986, 2001)....
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...…class I Kenyon cells receive substantial inputs provided in the calyces by collateral terminals of sensory interneurons (Schürmann, 1971; MacLeod and Laurent, 1996; Gronenberg, 2001; Yusuyama et al., 2002), Kenyon cells are not necessarily the sole inputs to efferent neurons that leave the lobes....
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References
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Book•
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01 Jan 1971
TL;DR: In this article, a definitive study of the social structure and symbiotic relationships of termites, social wasps, bees, and ants was conducted. But the authors focused on the relationship between ants and termites.
Abstract: Conducts a definitive study of the social structure and symbiotic relationships of termites, social wasps, bees, and ants.
4,679 citations
Book•
01 Jan 1967
TL;DR: The Dance Language and Orientation of Bees as discussed by the authors is a seminal work in the field of honeybee behavior that describes in non-technical language what he discovered in a lifetime of study about honeybees - their methods of orientation, their sensory faculties, and their remarkable ability to communicate with one another.
Abstract: Until his death in 1982, Karl von Frisch was the world's most renowned authority on bees. "The Dance Language and Orientation of Bees" is his masterwork - the culmination of more than fifty years of research. Now available for the first time in paperback, it describes in non-technical language what he discovered in a lifetime of study about honeybees - their methods of orientation, their sensory faculties, and their remarkable ability to communicate with one another. Thomas Seeley's new foreword traces the revolutionary effects of von Frisch's work, not just for the study of bees, but for all subsequent research in animal behaviour. This new paperback edition also includes a "Personal Appreciation" of von Frisch by the distinguished biologist Martin Lindauer, who was von Frisch's protege and later his colleague and friend.
2,461 citations
Journal Article•
[...]
TL;DR: The author wished to relate the three phases of research on insects and to express insect sociology as population biology in this detailed survey of knowledge of insect societies.
Abstract: In his introduction to this detailed survey of knowledge of insect societies, the author points out that research on insect sociology has proceeded in three phases, the natural history phase, the physiological phase and the population-biology phase. Advances in the first two phases have permitted embarkation in the third phase on a more rigorous theory of social evolution based on population genetics and writing this book, the author wished to relate the three phases of research on insects and to express insect sociology as population biology. A glossary of terms, a considerable bibliography and a general index are included. Other CABI sites
1,394 citations
"Subdivisions of hymenopteran mushro..." refers background in this paper
...This behavior includes division of labor, landmark orientation and navigation, communication, and learning and memory (Lindauer, 1959; Frisch, 1967; Wilson, 1971; Menzel and Erber, 1978; Hölldobler and Wilson, 1990; Wehner, 1994; Collett, 1995; Zeil et al., 1996; Ugolini and Cannicci, 1996; Erber…...
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868 citations
"Subdivisions of hymenopteran mushro..." refers background in this paper
...This behavior includes division of labor, landmark orientation and navigation, communication, and learning and memory (Lindauer, 1959; Frisch, 1967; Wilson, 1971; Menzel and Erber, 1978; Hölldobler and Wilson, 1990; Wehner, 1994; Collett, 1995; Zeil et al., 1996; Ugolini and Cannicci, 1996; Erber…...
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TL;DR: The results demonstrate that MBs mediate associative odor learning in flies, and that adult flies developing without MBs are unable to perform in a classical conditioning paradigm that tests associative learning of odor cues and electric shock.
Abstract: The corpora pedunculata, or mushroom bodies (MBs), in the brain of Drosophila melanogaster adults consist of approximately 2500 parallel Kenyon cell fibers derived from four MB neuroblasts. Hydroxyurea fed to newly hatched larvae selectively deletes these cells, resulting in complete, precise MB albation. Adult flies developing without MBs behave normally in most respects, but are unable to perform in a classical conditioning paradigm that tests associative learning of odor cues and electric shock. This deficit cannot be attributed to reductions in olfactory sensitivity, shock reactivity, or locomotor behavior. The results demonstrate that MBs mediate associative odor learning in flies.
787 citations