Anatomical organization of the cerebrum of the praying mantis Hierodula membranacea.

Many predatory animals, such as the praying mantis, use vision for prey detection and capture. Mantises are known in particular for their capability to estimate distances to prey by stereoscopic vision. While the initial visual processing centers have been extensively documented, we lack knowledge on the architecture of central brain regions, pivotal for sensory motor transformation and higher brain functions. To close this gap, we provide a three-dimensional (3D) reconstruction of the central brain of the Asian mantis, Hierodula membranacea. The atlas facilitates in-depth analysis of neuron ramification regions and aides in elucidating potential neuronal pathways. We integrated seven 3D-reconstructed visual interneurons into the atlas. In total, 42 distinct neuropils of the cerebrum were reconstructed based on synapsin-immunolabeled whole-mount brains. Backfills from the antenna and maxillary palps, as well as immunolabeling of γ-aminobutyric acid (GABA) and tyrosine hydroxylase (TH), further substantiate the identification and boundaries of brain areas. The composition and internal organization of the neuropils were compared to the anatomical organization of the brain of the fruit fly (Drosophila melanogaster) and the two available brain atlases of Polyneoptera-the desert locust (Schistocerca gregaria) and the Madeira cockroach (Rhyparobia maderae). This study paves the way for detailed analyses of neuronal circuitry and promotes cross-species brain comparisons. We discuss differences in brain organization between holometabolous and polyneopteran insects. Identification of ramification sites of the visual neurons integrated into the atlas supports previous claims about homologous structures in the optic lobes of flies and mantises.

Neuroarchitecture of the central complex of the desert locust: Tangential neurons.

The central complex (CX) comprises a group of midline neuropils in the insect brain, consisting of the protocerebral bridge (PB), the upper (CBU) and lower division (CBL) of the central body and a pair of globular noduli. It receives prominent input from the visual system and plays a major role in spatial orientation of the animals. Vertical slices and horizontal layers of the CX are formed by columnar, tangential, and pontine neurons. While pontine and columnar neurons have been analyzed in detail, especially in the fruit fly and desert locust, understanding of the organization of tangential cells is still rudimentary. As a basis for future functional studies, we have studied the morphologies of tangential neurons of the CX of the desert locust Schistocerca gregaria. Intracellular dye injections revealed 43 different types of tangential neuron, 8 of the PB, 5 of the CBL, 24 of the CBU, 2 of the noduli, and 4 innervating multiple substructures. Cell bodies of these neurons were located in 11 different clusters in the cell body rind. Judging from the presence of fine versus beaded terminals, the vast majority of these neurons provide input into the CX, especially from the lateral complex (LX), the superior protocerebrum, the posterior slope, and other surrounding brain areas, but not directly from the mushroom bodies. Connections are largely subunit- and partly layer-specific. No direct connections were found between the CBU and the CBL. Instead, both subdivisions are connected in parallel with the PB and distinct layers of the noduli.

A neuronal correlate of insect stereopsis.

A puzzle for neuroscience-and robotics-is how insects achieve surprisingly complex behaviours with such tiny brains. One example is depth perception via binocular stereopsis in the praying mantis, a predatory insect. Praying mantids use stereopsis, the computation of distances from disparities between the two retinal images, to trigger a raptorial strike of their forelegs when prey is within reach. The neuronal basis of this ability is entirely unknown. Here we show the first evidence that individual neurons in the praying mantis brain are tuned to specific disparities and eccentricities, and thus locations in 3D-space. Like disparity-tuned cortical cells in vertebrates, the responses of these mantis neurons are consistent with linear summation of binocular inputs followed by an output nonlinearity. Our study not only proves the existence of disparity sensitive neurons in an insect brain, it also reveals feedback connections hitherto undiscovered in any animal species.

Anatomical organization of the cerebrum of the desert locust Schistocerca gregaria.

The desert locust Schistocerca gregaria is a major agricultural pest in North Africa and the Middle East. As such, it has been intensely studied, in particular with respect to population dynamics, sensory processing, feeding behavior flight and locomotor control, migratory behavior, and its neuroendocrine system. Being a long-range migratory species, neural mechanisms underlying sky compass orientation have been studied in detail. To further understand neuronal interactions in the brain of the locust, a deeper understanding of brain organization in this insect has become essential. As a follow-up of a previous study illustrating the layout of the locust brain (Kurylas et al. in J Comp Neurol 484:206-223, 2008), we analyze the cerebrum, the central brain minus gnathal ganglia, of the desert locust in more detail and provide a digital three-dimensional atlas of 48 distinguishable brain compartments and 7 major fiber tracts and commissures as a basis for future functional studies. Neuropils were three-dimensionally reconstructed from synapsin-immunostained whole mount brains. Neuropil composition and their internal organization were analyzed and compared to the neuropils of the fruit fly Drosophila melanogaster. Most brain areas have counterparts in Drosophila. Some neuropils recognized in the locust, however, have not been identified in the fly while certain areas in the fly could not be distinguished in the locust. This study paves the way for more detailed anatomical descriptions of neuronal connections and neuronal cell types in the locust brain, facilitates interspecies comparisons among insect brains and points out possible evolutionary differences in brain organization between hemi- and holometabolous insects.

Anatomy of the lobula complex in the brain of the praying mantis compared to the lobula complexes of the locust and cockroach.

The praying mantis is an insect which relies on vision for capturing prey, avoiding being eaten and for spatial orientation. It is well known for its ability to use stereopsis for estimating the distance of objects. The neuronal substrate mediating visually driven behaviors, however, is not very well investigated. To provide a basis for future functional studies, we analyzed the anatomical organization of visual neuropils in the brain of the praying mantis Hierodula membranacea and provide supporting evidence from a second species, Rhombodera basalis, with particular focus on the lobula complex (LOX). Neuropils were three-dimensionally reconstructed from synapsin-immunostained whole mount brains. The neuropil organization and the pattern of γ-aminobutyric acid immunostaining of the medulla and LOX were compared between the praying mantis and two related polyneopteran species, the Madeira cockroach and the desert locust. The investigated visual neuropils of the praying mantis are highly structured. Unlike in most insects the LOX of the praying mantis consists of five nested neuropils with at least one neuropil not present in the cockroach or locust. Overall, the mantis LOX is more similar to the LOX of the locust than the more closely related cockroach suggesting that the sensory ecology plays a stronger role than the phylogenetic distance of the three species in structuring this center of visual information processing.