Nicholas J. Strausfeld

Subdivision of the drosophila mushroom bodies by enhancer-trap expression patterns

Phylogenetically conserved brain centers known as mushroom bodies are implicated in insect associative learning and in several other aspects of insect behavior. Kenyon cells, the intrinsic neurons of mushroom bodies, have been generally considered to be disposed as homogenous arrays. Such a simple picture imposes constraints on interpreting the diverse behavioral and computational properties that mushroom bodies are supposed to perform. Using a P[GAL4] enhancer-trap approach, we have revealed axonal processes corresponding to intrinsic cells of the Drosophila mushroom bodies. Rather than being homogenous, we find the Drosophila mushroom bodies to be compound neuropils in which parallel subcomponents exhibit discrete patterns of gene expression. Different patterns correspond to hitherto unobserved differences in Kenyon cell trajectory and placement. On the basis of this unexpected complexity, we propose a model for mushroom body function in which parallel channels of information flow, perhaps with different computational properties, subserve different behavioral roles.

Organization of the honey bee mushroom body: Representation of the calyx within the vertical and gamma lobes

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 bodys lobes. J. Comp. Neurol. 450:4–33, 2002.

A Systematic Nomenclature for the Insect Brain

Despite the importance of the insect nervous system for functional and developmental neuroscience, descriptions of insect brains have suffered from a lack of uniform nomenclature. Ambiguous definitions of brain regions and fiber bundles have contributed to the variation of names used to describe the same structure. The lack of clearly determined neuropil boundaries has made it difficult to document precise locations of neuronal projections for connectomics study. To address such issues, a consortium of neurobiologists studying arthropod brains, the Insect Brain Name Working Group, has established the present hierarchical nomenclature system, using the brain of Drosophila melanogaster as the reference framework, while taking the brains of other taxa into careful consideration for maximum consistency and expandability. The following summarizes the consortiums nomenclature system and highlights examples of existing ambiguities and remedies for them. This nomenclature is intended to serve as a standard of reference for the study of the brain of Drosophila and other insects.

Mushroom bodies of the cockroach: Their participation in place memory

Insects and other arthropods use visual landmarks to remember the location of their nest, or its equivalent. However, so far, only olfactory learning and memory have been claimed to be mediated by any particular brain region, notably the mushroom bodies. Here we describe the results of experiments that demonstrate that the mushroom bodies of the cockroach (Periplaneta americana), already shown to be involved in multimodal sensory processing, play a crucial role in place memory. Behavioral tests, based on paradigms similar to those originally used to demonstrate place memory in rats, demonstrate a rapid improvement in the ability of individual cockroaches to locate a hidden target when its position is provided by distant visual cues. Bilateral lesions of selected areas of the mushroom bodies abolish this ability but leave unimpaired the ability to locate a visible target. The present results demonstrate that the integrity of the pedunculus and medial lobe of a single mushroom body is required for place memory. The results are comparable to the results obtained from hippocampal lesions in rats and are relevant to recent studies on the effects of ablations of Drosophila mushroom bodies on locomotion. J. Comp. Neurol. 402:520–537, 1998.

Olfactory systems: Common design, uncommon origins?

In both vertebrates and invertebrates, odorant molecules reach the dendrites of olfactory receptor cells through an aqueous medium, which reflects the evolutionary origin of these systems in a marine environment. Important recent advances, however, have demonstrated striking interphyletic differences between the structure of vertebrate and invertebrate olfactory receptor proteins, as well as the organization of the genes encoding them. While these disparities support independent origins for odor-processing systems in craniates and protostomes (and even between the nasal and vomeronasal systems of craniates), olfactory neuropils share close neuroanatomical and physiological characters. Whereas there is a case to be made for homology among members of the two great protostome clades (the ecdysozoans and lophotrochozoans), the position of the craniates remains ambiguous.

Crustacean – Insect Relationships: The Use of Brain Characters to Derive Phylogeny amongst Segmented Invertebrates

Conserved neural characters identified in the brains of a variety of segmented invertebrates and outgroups have been used to reconstruct phylogenetic relationships. The analysis suggests that insects and crustaceans are sister groups and that the ‘myriapods’ are an artificial construct comprising unrelated chilopods and diplopods. Certain elements of the optic lobes and mid-brain support the notion that insects are more closely related to crustaceans than they are to any other arthropods. However, deep optic neuropils and optic chiasmata are homoplastic in insects and crustaceans. The organization of olfactory pathways suggests that insect olfactory lobes originated late, probably first appearing in orthopteroid or blattoid pterygotes. The present results are discussed with respect to recent studies on early development of arthropod nervous systems and the fossil record.

Physiology and morphology of projection neurons in the antennal lobe of the male mothManduca sexta

Summary1.We have used intracellular recording and staining, followed by reconstruction from serial sections, to characterize the responses and structure of projection neurons (PNs) that link the antennal lobe (AL) to other regions of the brain of the male sphinx mothManduca sexta.2.Dendritic arborizations of the AL PNs were usually restricted either to ordinary glomeruli or to the male-specific macroglomerular complex (MGC) within the AL neuropil. Dendritic fields in the MGC appeared to belong to distinct partitions within the MGC (Figs. 2, 3). PNs innervating the ordinary glomeruli had arborizations in a single glomerulus (uniglomerular) (Figs. 6, 7, 9, 11, 12A) or in more than one ordinary glomerulus of one AL (multiglomerular) (Figs. 12B, C, 14, 15), or in one case, in single glomeruli in both ALs (bilateral-uniglomerular) (Fig. 16). One PN innervated the MGC and many or all ordinary glomeruli of the AL (Fig. 13).3.PNs with dendritic arborizations in the ordinary glomeruli and PNs associated with the MGC typically projected both to the calyces of the ipsilateral mushroom body and to the lateral protocerebrum, but some differences in the patterns of termination in those regions have been noted for the two classes of PNs (Figs. 2, 3, 6, 7, 9, 16). One PN conspicuously lacked branches in the calyces but did project to the lateral protocerebrum (Fig. 14). The PN innervating the MGC and many ordinary glomeruli projected to the calyces of the ipsilateral mushroom body and the superior protocerebrum (Fig. 13).4.Crude sex-pheromone extracts excited all neurons with arborizations in the MGC, although some were inhibited by other odors (Figs. 3, 4). One P(MGC) was excited by crude sex-pheromone extract and by a mimic of one component of the pheromone blend but was inhibited by another component of the blend (Fig. 5).5.PNs with dendritic arborizations in ordinary glomeruli were excited (Figs. 7, 8, 10) or inhibited (Figs. 9, 11) by certain non-pheromonal odors. Some of these PNs also responded to mechanosensory stimulation of the antennae (Figs. 10, 11, 15, 16).6.The PN with dendritic arborizations in the MGC and many ordinary glomeruli was excited by crude sex-pheromone extracts and non-pheromonal odors and also responded to mechanosensory stimulation of the antenna (Fig. 13).

Dissection of the Peripheral Motion Channel in the Visual System of Drosophila melanogaster

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.

Deep Homology of Arthropod Central Complex and Vertebrate Basal Ganglia

Of Flies and Men Similarities of brain structure, function, and behavior are usually ascribed to convergent evolution. In their review, Strausfeld and Hirth (p. 157) identify multiple commonalities shared by vertebrate basal ganglia and a system of forebrain centers in arthropods called the central complex. The authors conclude that circuits essential to behavioral choice originated very early across phyla. The arthropod central complex and vertebrate basal ganglia derive from embryonic basal forebrain lineages that are specified by an evolutionarily conserved genetic program leading to interconnected neuropils and nuclei that populate the midline of the forebrain-midbrain boundary region. In the substructures of both the central complex and basal ganglia, network connectivity and neuronal activity mediate control mechanisms in which inhibitory (GABAergic) and modulatory (dopaminergic) circuits facilitate the regulation and release of adaptive behaviors. Both basal ganglia and central complex dysfunction result in behavioral defects including motor abnormalities, impaired memory formation, attention deficits, affective disorders, and sleep disturbances. The observed multitude of similarities suggests deep homology of arthropod central complex and vertebrate basal ganglia circuitries underlying the selection and maintenance of behavioral actions.

The organization of the insect visual system (Light microscopy) - I. Projections and arrangements of neurons in the lamina ganglionaris of Diptera

SummaryThe structure of optic cartridges in the frontal part of the lamina ganglionaris (the outermost synaptic region of the visual system of insects) has been analysed from selective and reduced silver stained preparations. The results, obtained from studies on five different species of Diptera, confirm that six retinula cells, together situated in a single ommatidium, project to six optic cartridges in a manner no different from that described by Braitenberg (1967) from Musca domestica. Each optic cartridge contains five first order interneurons (monopolar cells) which project together to a single column in the second synaptic region, the medulla. The dendritic arrangement of two of these neurons (L1 and L2) indicates that they must make contact with all six retinula cell terminals of a cartridge (R1–R6). Two others (L3 and L5) have processes that reach to only some of the retinula cell endings. A fifth form of monopolar cell (L4) sometimes has an arrangement of processes which could establish contact with all six retinula cells: other cells of the same type may contact only a proportion of them. This neuron (L4) also has an arrangement of collaterals such as to allow lateral interaction between neigbouring optic cartridges. The processes of the other four monopolar cells (L1, L2, L3 and L5) are usually contained within a single cartridge. In addition to these elements there is a pair of receptor prolongations (the long visual fibres, R7 and R8) that bypasses all other elements of a cartridge, including the receptor terminals R1–R6, and finally terminates in the medulla. Four types of neurons, which are derived from perikarya lying just beneath or just above the second synaptic region, send fibres across the first optic chiasma to the lamina. Like all the other interneuronal elements of cartridges the terminals of these so-called “centrifugal” cells have characteristic topographical relationships with the cyclic arrangement of retinula cell terminals. Apart from the above mentioned neurons there is also a system of tangential fibres whose processes invade single cartridges but which together could provide a substrate for relaying information to the medulla derived from aggregates of cartridges.Optic cartridges contain at least 15 neural elements other than retinula cells. This complex structure is discussed with respect to the receptor physiology, as it is known from electrophysiological and behavioural experiments. The arrangements of neurons in cartridges is tentatively interpreted as a means of providing at least 6 separate channels of information to the medulla, four of which may serve special functions such as relaying color coded information or information about the angle of polarised light at high light intensities.