In most insects with olfactory glomeruli, each side of the brain possesses a mushroom body equipped with calyces supplied by olfactory projection neurons. Kenyon cells providing dendrites to the calyces supply a pedunculus and lobes divided into subdivisions supplying outputs to other brain areas. It is with reference to these components that most functional studies are interpreted. However, mushroom body structures are diverse, adapted to different ecologies and likely to serve various functions. In insects whose derived life styles preclude the detection of airborne odorants there is a loss of the antennal lobes and attenuation or loss of the calyces. Such taxa retain mushroom body lobes that as elaborate as those of mushroom bodies equipped with calyces. Antennal lobe loss and calycal regression also typifies taxa with short non-feeding adults where olfaction is redundant. Examples are cicadas and mayflies, the latter representing the most basal lineage of winged insects. Mushroom bodies of another basal taxon, the Odonata, possess a remnant calyx that may reflect the visual ecology of this group. That mushroom bodies persist in brains of secondarily anosmic insects suggests that they play roles in higher functions other than olfaction. Mushroom bodies are not ubiquitous: the most basal living insects, the wingless Archaeognatha, possess glomerular antennal lobes but lack mushroom bodies, suggesting that the ability to process airborne odorants preceded the acquisition of mushroom bodies. Archaeognathan brains are like those of higher malacostracans, which lack mushroom bodies but have elaborate olfactory centers laterally in the brain.
Malacostracan crustaceans and dicondylic insects possess large second-order olfactory neuropils called, respectively, hemiellipsoid bodies and mushroom bodies. Because these centers look very different in the two groups of arthropods, it has been debated whether these second-order sensory neuropils are homologous or whether they have evolved independently. Here we describe the results of neuroanatomical observations and experiments that resolve the neuronal organization of the hemiellipsoid body in the terrestrial Caribbean hermit crab, Coenobita clypeatus, and compare this organization with the mushroom body of an insect, the cockroach Periplaneta americana. Comparisons of the morphology, ultrastructure, and immunoreactivity of the hemiellipsoid body of C. clypeatus and the mushroom body of the cockroach P. americana reveal in both a layered motif provided by rectilinear arrangements of extrinsic and intrinsic neurons as well as a microglomerular organization. Furthermore, antibodies raised against DC0, the major catalytic subunit of protein kinase A, specifically label both the crustacean hemiellipsoid bodies and insect mushroom bodies. In crustaceans lacking eyestalks, where the entire brain is contained within the head, this antibody selectively labels hemiellipsoid bodies, the superior part of which approximates a mushroom body's calyx in having large numbers of microglomeruli. We propose that these multiple correspondences indicate homology of the crustacean hemiellipsoid body and insect mushroom body and discuss the implications of this with respect to the phylogenetic history of arthropods. We conclude that crustaceans, insects, and other groups of arthropods share an ancestral neuronal ground pattern that is specific to their second-order olfactory centers.
The primary antennal sensory centers (antennal lobes) in the brain of the honeybee are highly compartmentalized into discrete spheres of synaptic neuropil called glomeruli, many of which can be identified according to their predictable size and location. Glomeruli undergo significant changes in volume during the lifetime of the adult worker bee, at least some of which are activity dependent. This study tests the commonly expressed assumption that increases in neuropil volume are accompanied by an underlying increase in the number of synapses present in the tissue. A combination of light and electron microscopy was used to determine total synapse number within two glomeruli, T1-44 and T4-2(1). The Cavalieri direct estimator of volume was applied to 1.5 microm sections of resin-embedded brains. Selected sections were then re-embedded and prepared for transmission electron microscopy. Synapse densities were determined using the physical disector method on electron micrographs. Synapse density and glomerulus volume were combined to give an unbiased estimate of the total number of synapses. In glomerulus T1-44, a significant increase in volume was accompanied by a significant increase in the total number of synapses. In contrast, synapse counts in T4-2(1) remained unchanged, despite a significant increase in the volume of this glomerulus. These results demonstrate that synapse proliferation in antennal lobes of the adult worker bee is highly site specific. Although volumetric changes and changes in synapse number both contribute to the structural plasticity of the antennal lobes, these two components of plasticity appear to be independent processes.
The primary antennal sensory centers (antennal lobes) in the brain of the honeybee are highly compartmentalized into discrete spheres of synaptic neuropil called glomeruli. Many of the glomeruli can be identified according to their predictable size and location. This study examines T1-44, a prominent glomerulus on the dorsal surface of the antennal lobe. Previously, we have shown that the volume of T1-44 in 4-day-old workers performing tasks within the hive is significantly smaller than in foragers and that increases in volume are accompanied by an increase in total synapse number in this glomerulus. Here we examine whether foraging experience is essential for either changes in volume or for changes in synapse numbers in glomerulus T1-44. Five-day-old bees reared under normal colony conditions were compared with 5-day-old bees reared under isolated conditions, and also to 5-day-old bees that had been induced to forage precociously. A combination of light and electron microscopy was used to compare T1-44 volumes and synapse numbers in these three groups. Two groups of 11-day-old bees, precocious foragers and nonforagers, were also examined. The Cavalieri direct estimator of volume was applied to 1.5 microm sections of resin embedded brains. Selected sections were then re-embedded and prepared for transmission electron microscopy. Synapse densities were determined using the physical disector method on electron micrographs. Synapse density and glomerulus volume were combined to give an unbiased estimate of the total number of synapses. This study shows that while both volume and synapse numbers can be induced to increase prematurely in young (5-day-old) precocious foragers, foraging experience is not essential for these structural changes to occur in glomerulus T1-44.
The insect central complex and vertebrate basal ganglia are forebrain centres involved in selection and maintenance of behavioural actions. However, little is known about the formation of the underlying circuits, or how they integrate sensory information for motor actions. Here, we show that paired embryonic neuroblasts generate central complex ring neurons that mediate sensory-motor transformation and action selection in Drosophila. Lineage analysis resolves four ring neuron subtypes, R1-R4, that form GABAergic inhibition circuitry among inhibitory sister cells. Genetic manipulations, together with functional imaging, demonstrate subtype-specific R neurons mediate the selection and maintenance of behavioural activity. A computational model substantiates genetic and behavioural observations suggesting that R neuron circuitry functions as salience detector using competitive inhibition to amplify, maintain or switch between activity states. The resultant gating mechanism translates facilitation, inhibition and disinhibition of behavioural activity as R neuron functions into selection of motor actions and their organisation into action sequences.
Electron microscopical observations of the hemiellipsoid bodies of the land hermit crab Coenobita clypeatus resolve microglomerular synaptic complexes that are comparable to those observed in the calyces of insect mushroom bodies and which characterize olfactory inputs onto intrinsic neurons. In an adult hermit crab, intrinsic neurons and one class of efferent neurons originate from neuronal somata of globuli cells covering the hemiellipsoid bodies. Counts of their nucleoli show that about 120,000 globuli cells supply each hemiellipsoid body in an adult hermit crab. This number is comparable to the number of globuli cells supplying mushroom bodies of certain insects, such as honey bees and cockroaches. Counts of axons in tracts leading from the olfactory lobes to the hemiellipsoid bodies resolve 20,000 afferent axons, however, an order of magnitude greater than known for any insect. These afferent axons provide numerous swollen varicosities, each presynaptic to many small profiles, and thus comparable to the microglomeruli that characterize insect mushroom body calyces. Also, common to mushroom bodies and hemiellipsoid bodies are arrangements of intrinsic neurons, afferent neurons containing dense core vesicles, and systems of serial synaptic complexes that relate to postsynaptic profiles of efferent neurons. Together, the ultrastructural organization of the hemiellipsoid bodies of C. clypeatus supports the proposition that this center may share a common origin with the insect mushroom body despite obvious divergent evolution of overall shape.
Copepods are a diverse and ecologically crucial group of minute crustaceans that are relatively neglected in terms of studies on nervous system organization. Recently, morphological neural characters have helped clarify evolutionary relationships within Arthropoda, particularly among Tetraconata (i.e., crustaceans and hexapods), and indicate that copepods occupy an important phylogenetic position relating to both Malacostraca and Hexapoda. This taxon therefore provides the opportunity to evaluate those neural characters common to these two clades likely to be results of shared ancestry (homology) versus convergence (homoplasy). Here we present an anatomical characterization of the brain and central nervous system of the well-studied harpacticoid copepod species Tigriopus californicus. We show that this species is endowed with a complex brain possessing a central complex comprising a protocerebral bridge and central body. Deutocerebral glomeruli are supplied by the antennular nerves, and a lateral protocerebral olfactory neuropil corresponds to the malacostracan hemiellipsoid body. Glomeruli contain synaptic specializations comparable to the presynaptic "T-bars" typical of dipterous insects, including Drosophila melanogaster. Serotonin-like immunoreactivity pervades the brain and ventral nervous system, with distinctive deutocerebral distributions. The present observations suggest that a suite of morphological characters typifying the Tigriopus brain reflect a ground pattern organization of an ancestral Tetraconata, which possessed an elaborate and structurally differentiated nervous system.
Neuronal modifications that accompany normal aging occur in brain neuropils and might share commonalties across phyla including the most successful group, the Insecta. This study addresses the kinds of neuronal modifications associated with loss of memory that occur in the hemimetabolous insect Periplaneta americana. Among insects that display considerable longevity, the American cockroach lives up to 64 wk and reveals specific cellular alterations in its mushroom bodies, higher centers that have been shown to be associated with learning and memory. The present results describe a vision-based learning paradigm, based on a modified Barnes maze, that compares memory in young (10-wk old), middle-aged (30-wk old), and aged adults (50-wk old). We show that not only is the performance of this task during the 14 training trials significantly decremented in aged cockroaches, but that aged cockroaches show significant impairment in successfully completing a crucial test involving cue rotation. Light and electron microscopical examination of the brains of these different age groups reveal major changes in neuron morphology and synaptology in the mushroom body lobes, centers shown to underlie place memory in this taxon.
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