In the eye, visual information is segregated into modalities such as color and motion, these being transferred to the central brain through separate channels. Here, we genetically dissect the achromatic motion channel in the fly Drosophila melanogaster at the level of the first relay station in the brain, the lamina, where it is split into four parallel pathways (L1-L3, amc/T1). The functional relevance of this divergence is little understood. We now show that the two most prominent pathways, L1 and L2, together are necessary and largely sufficient for motion-dependent behavior. At high pattern contrast, the two pathways are redundant. At intermediate contrast, they mediate motion stimuli of opposite polarity, L2 front-to-back, L1 back-to-front motion. At low contrast, L1 and L2 depend upon each other for motion processing. Of the two minor pathways, amc/T1 specifically enhances the L1 pathway at intermediate contrast. L3 appears not to contribute to motion but to orientation behavior.

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.

A serum raised against octopamine reveals in cockroaches and honey bees structurally comparable systems of perikarya and their extensive yet discrete systems of arborizations in neuropils. Numerous and prominent clusters of lateral cell bodies in the brain as well as many midline perikarya provide octopamine-like immunoreactive processes to circumscribed regions of the subesophageal ganglion, antennal lobe glomeruli, optic neuropils, and neuropils of the protocerebrum. There is dense octopaminergic innervation in the protocerebral bridge and ellipsoid body of the central complex. The antennal lobes are supplied by at least three octopamine-immunoreactive neurons. In contrast, the mushroom bodies show the fewest immunoreactive elements. In Apis a single axon supplies sparse immunoreactive processes to the calyces' basal ring, collar, and lip. A diffuse arrangement of immunoreactive processes invades all zones of the mushroom body calyces in Periplaneta. These processes derive from an ascending axon ascribed to a dorsal unpaired median neuron at the maxillary segment of the subesophageal ganglion. In both taxa octopamine-immunoreactive processes invade only the gamma lobes of the mushroom bodies, omitting their other divisions. The present observations are discussed with respect to possible roles of octopamine in sensory integration and association.

Golgi impregnations reveal a variety of dendritic morphologies amongst Kenyon cells in the mushroom bodies of Drosophila melanogaster. Different morphological types of Kenyon cells contribute axon-like processes to five divisions of the medial and vertical lobes. Four of these divisions have characteristic affinities to antibodies raised against aspartate, glutamate, and taurine. A newly described posterior subdivision of the medial lobe, here named the betac lobe with its vertical branch alphac, comprises glutamatergic Kenyon cells that are probably homologous to glutamatergic Kenyon cells in the cockroach and honey bee, and are the last neurons to differentiate. The first neurons to differentiate, which supply the gamma lobe, are equipped with clawed dendritic specializations and are the structural homologues of clawed class II Kenyon cells supplying the gamma lobes in cockroaches and honey bees. Three intermediate divisions lie between the betac lobe and gamma lobe. These are, from the back towards the front, the beta lobe, the beta' lobe, and a narrow division between beta' and gamma called the beta" lobe. The fused calyx of the Drosophila mushroom body is comparable to the double calyces of Hymenoptera, here exemplified by a basal taxon, Diprion pini. Further similarities between the hymenopteran calyces and those of Drosophila are suggested by the segregation of different types of Kenyon cell dendrites within the calyx neuropil. The organization of afferents from the antennal lobes also defines regions in the Drosophila calyx that may be homologous to the lip and basal ring regions of the honey bee calyces. As in honey bees, GABAergic processes densely invade Drosophila's calyces, which also contain a sparse but uniform distribution of octopaminergic elements. Microsc. Res. Tech. 62:151-169, 2003.

A serum raised against conjugated octopamine reveals structurally comparable systems of perikarya and arborizations in protocerebral neuropils of two species of Diptera, Drosophila melanogaster and Phaenicia sericata; the latter is used extensively for electrophysiological studies of the optic lobes and their central projections. Clusters of cell bodies in the brain as well as midline perikarya provide octopamine-like immunoreactive processes to the optic lobes, circumscribed regions of the protocerebrum and the central complex, particularly the protocerebral bridge, fan-shaped body, and ellipsoid body. Ventral unpaired median somata provide immunoreactive processes within the subesophageal ganglion and tritocerebrum. Ascending neurites from these cells also supply the antennal lobe glomeruli, regions of the lateral protocerebrum, the mushroom body calyces, and the lobula complex. The mushroom body's gamma lobes contain immunoreactive processes that originate from processes that arborize in the protocerebrum. The present observations are discussed with respect to similarities and differences between two species of Diptera, one of which has neurons large enough for intracellular penetrations. The results are also discussed with respect to recent studies on octopamine-immunoreactive organization in honey bees and cockroaches and the suggested roles of octopamine in sensory processing, learning, and memory.

The shared organization of three optic lobe neuropils-the lamina, medulla, and lobula-linked by chiasmata has been used to support arguments that insects and malacostracans are sister groups. However, in certain insects, the lobula is accompanied by a tectum-like fourth neuropil, the lobula plate, characterized by wide-field tangential neurons and linked to the medulla by uncrossed axons. The identification of a lobula plate in an isopod crustacean raises the question of whether the lobula plate of insects and isopods evolved convergently or are derived from a common ancestor. This question is here investigated by comparisons of insect and crustacean optic lobes. The basal branchiopod crustacean Triops has only two visual neuropils and no optic chiasma. This finding contrasts with the phyllocarid Nebalia pugettensis, a basal malacostracan whose lamina is linked by a chiasma to a medulla that is linked by a second chiasma to a retinotopic outswelling of the lateral protocerebrum, called the protolobula. In Nebalia, uncrossed axons from the medulla supply a minute fourth optic neuropil. Eumalacostracan crustaceans also possess two deep neuropils, one receiving crossed axons, the other uncrossed axons. However, in primitive insects, there is no separate fourth optic neuropil. Malacostracans and insects also differ in that the insect medulla comprises two nested neuropils separated by a layer of axons, called the Cuccati bundle. Comparisons suggest that neuroarchitectures of the lamina and medulla distal to the Cuccati bundle are equivalent to the eumalacostracan lamina and entire medulla. The occurrence of a second optic chiasma and protolobula are suggested to be synapomorphic for a malacostracan/insect clade.

No abstract

In Diptera, subsets of small retinotopic neurons provide a discrete channel from achromatic photoreceptors to large motion-sensitive neurons in the lobula complex. This pathway is distinguished by specific affinities of its neurons to antisera raised against glutamate, aspartate, gamma-aminobutyric acid (GABA), choline acetyltransferase (ChAT), and a N-methyl-D-aspartate type 1 receptor protein (NMDAR1). Large type 2 monopolar cells (L2) and type 1 amacrine cells, which in the external plexiform layer are postsynaptic to the achromatic photoreceptors R1-R6, express glutamate immunoreactivity as do directionally selective motion-sensitive tangential neurons of the lobula plate. L2 monopolar cells ending in the medulla are accompanied by terminals of a second efferent neuron T1, the dendrites of which match NMDAR1-immunoreactive profiles in the lamina. L2 and T1 endings visit ChAT and GABA-immunoreactive relays (transmedullary neurons) that terminate from the medulla in a special layer of the lobula containing the dendrites of directionally selective retinotopic T5 cells. T5 cells supply directionally selective wide-field neurons in the lobula plate. The present results suggest a circuit in which initial motion detection relies on interactions among amacrines and T1, and the subsequent convergence of T1 and L2 at transmedullary cell dendrites. Convergence of ChAT-immunoreactive and GABA-immunoreactive transmedullary neurons at T5 dendrites in the lobula, and the presence there of local GABA-immunoreactive interneurons, are suggested to provide excitatory and inhibitory elements for the computation of motion direction. A comparable immunocytological organization of aspartate- and glutamate-immunoreactive neurons in honeybees and cockroaches further suggests that neural arrangements providing directional motion vision in flies may have early evolutionary origins.