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A prevailing opinion since 1926 has been that optic lobe organization in malacostracan crustaceans and insects reflects a corresponding organization in their common ancestor. Support for this refers to malacostracans and insects both possessing three, in some instances four, nested retinotopic neuropils beneath their compound eyes. Historically, the rationale for claiming homology of malacostracan and insect optic lobes referred to those commonalities, and to comparable arrangements of neurons. However, recent molecular phylogenetics has firmly established that Malacostraca belong to Multicrustacea, whereas Hexapoda and its related taxa Cephalocarida, Branchiopoda, and Remipedia belong to the phyletically distinct clade Allotriocarida. Insects are more closely related to remipedes than are either to malacostracans. Reconciling neuroanatomy with molecular phylogenies has been complicated by studies showing that the midbrains of remipedes share many attributes with the midbrains of malacostracans. Here we review the organization of the optic lobes in Malacostraca and Insecta to inquire which of their characters correspond genealogically across Pancrustacea and which characters do not. We demonstrate that neuroanatomical characters pertaining to the third optic lobe neuropil, called the lobula complex, may indicate convergent evolution. Distinctions of the malacostracan and insect lobula complexes are sufficient to align neuroanatomical descriptions of the pancrustacean optic lobes within the constraints of molecular-based phylogenies.

Just one superorder of insects is known to possess a neuronal network that mediates extremely rapid reactions in flight in response to changes in optic flow. Research on the identity and functional organization of this network has over the course of almost half a century focused exclusively on the order Diptera, a member of the approximately 300-million-year-old clade Holometabola defined by its mode of development. However, it has been broadly claimed that the pivotal neuropil containing the network, the lobula plate, originated in the Cambrian before the divergence of Hexapoda and Crustacea from a mandibulate ancestor. This essay defines the traits that designate the lobula plate and argues against a homologue in Crustacea. It proposes that the origin of the lobula plate is relatively recent and may relate to the origin of flight.

The middle Cambrian taxon Waptia fieldensis offers insights into early evolution of sensory arrangements that may have supported a range of actions such as exploratory behavior, burrowing, scavenging, swimming, and escape, amongst others. Less elaborate than many modern pancrustaceans, specific features of Waptia that suggest a possible association with the pancrustacean evolutionary trajectory, include mandibulate mouthparts, a single pair of antennae, reflective triplets on the head comparable to ocelli, and traces of brain and optic lobes that conform to the pancrustacean ground pattern. This account revisits an earlier description of Waptia to further interpret the distribution of its overall morphology and receptor arrangements in the context of plausible behavioral repertoires.

SummaryThe record of arthropod body fossils is traceable back to the “Cambrian explosion,” marked by the appearance of most major animal phyla. Exceptional preservation provides crucial evidence for panarthropod early radiation. However, due to limited representation in the fossil record of internal anatomy, particularly the CNS, studies usually rely on exoskeletal and appendicular morphology. Recent studies [1–3] show that despite extreme morphological disparities, euarthropod CNS evolution appears to have been remarkably conservative. This conclusion is supported by descriptions from Cambrian panarthropods of neural structures that contribute to understanding early evolution of nervous systems and resolving controversies about segmental homologies [4–12]. However, the rarity of fossilized CNSs, even when exoskeletons and appendages show high levels of integrity, brought into question data reproducibility because all but one of the aforementioned studies were based on single specimens [13]. Foremost among objections is the lack of taphonomic explanation for exceptional preservation of a tissue that some see as too prone to decay to be fossilized. Here we describe newly discovered specimens of the Chengjiang euarthropod Fuxianhuia protensa with fossilized brains revealing matching profiles, allowing rigorous testing of the reproducibility of cerebral structures. Their geochemical analyses provide crucial insights of taphonomic pathways for brain preservation, ranging from uniform carbon compressions to complete pyritization, revealing that neural tissue was initially preserved as carbonaceous film and subsequently pyritized. This mode of preservation is consistent with the taphonomic pathways of gross anatomy, indicating that no special mode is required for fossilization of labile neural tissue.

SummaryExcept in species that have undergone evolved loss, paired lobed centers referred to as “mushroom bodies” occur across invertebrate phyla [1–5]. Unresolved is the question of whether these centers, which support learning and memory in insects, correspond genealogically or whether their neuronal organization suggests convergent evolution. Here, anatomical and immunohistological observations demonstrate that across phyla, mushroom body-like centers share a neuroanatomical ground pattern and proteins required for memory formation. Paired lobed or dome-like neuropils characterize the first brain segment (protocerebrum) of mandibulate and chelicerate arthropods and the nonganglionic brains of polychaete annelids, polyclad planarians, and nemerteans. Structural and cladistic analyses resolve an ancestral ground pattern common to all investigated taxa: chemosensory afferents supplying thousands of intrinsic neurons, the parallel processes of which establish orthogonal networks with feedback loops, modulatory inputs, and efferents. Shared ground patterns and their selective labeling with antisera against proteins required for normal mushroom body function in Drosophila are indicative of genealogical correspondence and thus an ancestral presence predating arthropod and lophotrochozoan origins. Implications of this are considered in the context of mushroom body function and early ecologies of ancestral bilaterians.

The moth Spodoptera littoralis, is a major pest of agriculture whose olfactory system is tuned to odorants emitted by host plants and conspecifics. As in other insects, the paired mushroom bodies are thought to play pivotal roles in behaviors that are elicited by contextual and multisensory signals, amongst which those of specific odors dominate. Compared with species that have elaborate behavioral repertoires, such as the honey bee Apis mellifera or the cockroach Periplaneta americana, the mushroom bodies of S. littoralis were originally viewed as having a simple cellular organization. This has been since challenged by observations of putative transmitters and neuromodulators. As revealed by immunocytology, the spodopteran mushroom bodies, like those of other taxa, are subdivided longitudinally into discrete neuropil domains. Such divisions are further supported by the present study, which also demonstrates discrete affinities to different mushroom body neuropils by antibodies raised against two putative transmitters, glutamate and gamma-aminobutyric acid, and against three putative neuromodulatory substances: serotonin, A-type allatostatin, and tachykinin-related peptides. The results suggest that in addition to longitudinal divisions of the lobes, circuits in the calyces and lobes are likely to be independently modulated.

SummaryIn 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.

The aim of this study was to further reveal the organization of Kenyon cells in the mushroom body calyx and lobes of the male moth Spodoptera littoralis, by using immunocytochemical labeling. Subdivisions of the mushroom bodies were identified employing antisera raised against the amino acids taurine and aspartate, the neuropeptides FMRF-amide and Mas-allatotropin, and against the protein kinase A catalytic subunit DC0. These antisera have previously been shown to label subsets of Kenyon cells in other species. The present results show that the organization of the mushroom body lobes into discrete divisions, described from standard neuroanatomical methods, is confirmed by immunocytology and shown to be further elaborated. Anti-taurine labels the accessory Y-tract, the gamma division of the lobes, and a thin subdivision of the most posterior component of the lobes. Aspartate antiserum labels the entire mushroom body. FMRF-amide-like immunolabeling is pronounced in the gamma division and in the anterior perimeter of the alpha/beta and alpha'/beta' divisions. Mas-allatotropin-like immunolabeling shows the opposite of FMRF-amide-like and taurine-like immunolabeling: the gamma division and the accessory Y-system is immunonegative whereas strong labeling is seen in both the alpha/beta and alpha'/beta' divisions. The present results agree with findings from other insects that mushroom bodies are anatomically divided into discrete parallel units. Functional and developmental implications of this organization are discussed.

In malacostracan crustaceans and insects three nested optic lobe neuropils are linked by two successive chiasmata that reverse and then reverse again horizontal rows of retinotopic columns. Entomostracan crustaceans possess but two retinotopic neuropils connected by uncrossed axons: a distal lamina and an inner plate-like neuropil, here termed the visual tectum that is contiguous with the protocerebrum. This account proposes an evolutionary trajectory that explains the origin of chiasmata from an ancestral taxon lacking chiasmata. A central argument employed is that the two optic lobe neuropils of entomostracans are homologous to the lamina and lobula plate of insects and malacostracans, all of which contain circuits for motion detection—an archaic attribute of visual systems. An ancestral duplication of a cell lineage originally providing the entomostracan lamina is proposed to have given rise to an outer and inner plexiform layer. It is suggested that a single evolutionary step resulted in the separation of these layers and, as a consequence, their developmental connection by a chiasma with the inner layer, the malacostracan-insect medulla, still retaining its uncrossed connections to the deep plate-like neuropil. It is postulated that duplication of cell lineages of the inner proliferation zone gave rise to a novel neuropil, the lobula. An explanation for the second chiasma is that it derives from uncrossed axons originally supplying the visual tectum that subsequently supply collaterals to the opposing surface of the newly evolved lobula. A cladistic analysis based on optic lobe anatomy of taxa possessing compound eyes supports a common ancestor of the entomostracans, malacostracan crustaceans, and insects.

Most insects possess an assemblage of midline neuropils in their protocerebrum called the central complex. Recent studies have identified comparable assemblages in the malacostracan protocerebrum. Studies of Drosophila melanogaster locomotory mutants suggest that in insects one role for the central complex might be to orchestrate limb actions. This is anecdotally supported by comparisons amongst insects suggesting that elaboration of central complex architecture correlates with complexity of limb motor repertoires. The present account describes immunocytochemical and neuroanatomical observations that reveal common design principles amongst midline neuropils in four arthropod clades, the hexapods, crustaceans, chilopods, and chelicerates and the absence of midline neuropils in diplopods. The chilopod midline neuropil, which is columnar and stratified and lacks chiasmal axons to the dorsal protocerebrum or connections to discrete satellite regions, may represent the plesiomorphous condition. The complete absence of a midline neuropil in diplopods supports previous neuroanatomical studies suggesting that the ‘Myriapoda’ are an artificial paraphyletic group. The columnar and layered arcuate midline neuropils of chelicerates are compared with columnar and layered midline neuropils of chilopods. No midline neuropil has been identified in a lophotrochozoan outgroup, the Polychaeta.

Two major classes of Descending Neurones (DNs) originate in fly cerebral ganglia: (1) uniquely identifiable DNs, most of which arise preorally in duetocerebral neuropil of the supraoesophageal ganglion, the brain proper (2) parallel projecting DNs (PDNs) most originating in the suboesophageal ganglion. Brain DNs receive inputs directly from sensory systems and indirectly via higher center and peptidergic interconnections of the protocerebrum. Direct inputs include primary mechanosensory afferents, first order relay neurones from the olfactory lobes and ocellar receptor cups, and higher order visual neurones that interact with retinotopic inputs from compound eyes. Uniquely identifiable DNs arising in the brain are arranged in uniquely identifiable clusters. Each cluster receives a unique combination of inputs which are shared wholly or in part by the dendritic trees of its constituent DNs. Axons arising from a cluster diverge to different targets in the thoracic ganglia. PDNs form groups of as many as 40 neurones, as determined from outgoing axon bundles. Dendrites of PDNs are thin and diffuse, and arborize amongst collaterals from through-going axons of descending neurones arising in the brain. Axon bundles of PDNs are typically organized in rather simple ladder-like patterns in thoracic ganglion. A third type of uniquely identifiable DN also arises in the suboesophageal ganglion but does not seem to be arranged in clusters.

Optic cartridges of the first synaptic region of the fly's visual system are interconnected by a set of collaterals derived from the L4 monopolar cells. These neurones are the only efferent monopolar cells to contact elements in more than one cartridge. Electron microscopy of Golgi-impregnated cells has shown that sets of distal (outer) processes of L4 contact, and are postsynaptic to, the α profiles of lamina intrinsic cells at single cartridges. L4's proximal (inner) collaterals, situated at the inner face of the lamina, contact the receptor terminals and the radial monopolar cells (L1 and L2) of its own and of two adjacent cartridges. One L4 meets components of 6 other L4 cells of 6 surrounding cartridges. Conventionally fixed material shows that the proximal collaterals of L4 are presynaptic to radial monopolar cells and some receptor endings as well as being pre-and postsynaptic to the other L4 neuronal components to which they extend, or which extend to them. The numbers of the distal processes postsynaptic to α fibres vary across the eye. There is a graded increase from back to front and from the dorsal and ventral poles of the eye towards its equator.