Topographic organization and possible function of the posterior optic tubercles in the brain of the desert locust Schistocerca gregaria

Abstract

Migrating desert locusts, Schistocerca gregaria, are able to use the skylight polarization pattern for navigation. They detect polarized light with a specialized dorsal rim area in their compound eye. After multistage processing, polarization signals are transferred to the central complex, a midline-spanning brain area involved in locomotor control. Polarization-sensitive tangential neurons (TB-neurons) of the protocerebral bridge, a part of the central complex, give rise to a topographic arrangement of preferred polarization angles in the bridge, suggesting that the central complex acts as an internal sky compass. TB-neurons connect the protocerebral bridge with two adjacent brain areas, the posterior optic tubercles. To analyze the polarotopic organization of the central complex further, we investigated the number and morphologies of TB-neurons and the presence and colocalization of three neuroactive substances in these neurons. Triple immunostaining with antisera against Diploptera punctata allatostatin (Dip-AST), Manduca sexta allatotropin (Mas-AT), and serotonin (5HT) raised in the same host species revealed three spatially distinct TB-neuron clusters, each consisting of 10 neurons per hemisphere: cluster 1 and 3 showed Dip-AST/5HT immunostaining, whereas cluster 2 showed Dip-AST/Mas-AT immunostaining. Five subtypes of TB-neuron could be distinguished based on ramification patterns. Corresponding to ramification domains in the protocerebral bridge, the neurons invaded distinct but overlapping layers within the posterior optic tubercle. Similarly, neurons interconnecting the tubercles of the two hemispheres also targeted distinct layers of these neuropils. From these data we propose a neuronal circuit that may be suited to stabilize the internal sky compass in the central complex of the locust.

Development of the Neurochemical Architecture of the Central Complex

“…This neuroarchitecture is paralleled by a neurochemical architecture as revealed, for example, in the axonal projections of subsets of neurons from the PI expressing serotonin (5HT) and allatostatin (AST) in the adult (Figure 5A), or by diaphorase (NADPHd) staining as a marker for nitric oxide (NO) already at 85% of embryogenesis (Figures 5Bi,ii). This congruence of anatomical and neurochemical architecture can also be demonstrated using a range of other molecules (Homberg, 2002; Herbert et al, 2010; Pfeiffer and Homberg, 2014; Beetz et al, 2015) whose contributions to adult behaviors are steadily being revealed (Seidel and Bicker, 1996, 2002; Homberg, 2002; Nässel, 2002; Winther et al, 2006; Kahsai and Winther, 2011; Kunst et al, 2011). The question at the center of this study is when and how these stereotypic neurochemical projection patterns arise during embrygenesis.…”

“…Since most of the substances examined here are expressed in subsets of tangential and columnar neurons, and some additionally in pontine neurons, our current level of resolution does not allow us to relate a given temporal expression pattern to the functional morphology of individual neuron types. This may eventually prove possible for certain columnar (CPU1, 2) or tangential (TB1a, TB1d) neurons with regionalized morphologies spanning different modules (see Heinze and Homberg, 2008; Pfeiffer and Homberg, 2014; Beetz et al, 2015) if these neurons were to also regionalize their developmental expression of a given neurochemical.…”

“…For instance, our studies reveal no co-localization of serotonergic and peptidergic cells in embryonic W, X, Y Z lineages (Figure 7), and no cells co-expressing 5HT and neuropeptides in the FB or noduli during embryogenesis (Figures 6, 9, 10). This is clearly not the case in the adult where 5HT and AST are co-localized both in columnar neurons innervating the noduli (Vitzthum et al, 1996; Homberg, 2002) and in clusters of TB neurons projecting into the tract linking the posterior optic tubercle and the PB (Beetz et al, 2015). The lineages of these co-expressing TB neurons have yet to be determined, but as far as the columnar neurons from the W, X, Y, Z lineages are concerned, two possible explanations can be offered: either distinct populations of neurons from the same lineage, but with different biochemical profiles, differentially innervate the FB and noduli, or at least some neurons have changed their biochemical profile during larval development.…”

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

“…These neurons gave rise to immunostaining in particular layers of the medulla. In S. gregaria , Homberg, Brandl, Clynen, Schoofs, & Veenstra () and Beetz, el Jundi, Heinze, and Homberg () have distinguished 10 layers, numbered 1–10 from distal to proximal. GABA immunostaining was particularly dense in layers 4, 8, 9, and 10, and had a columnar appearance in distal layers 1‐3 (Figure b,e).…”

Principles of Insect Path Integration

“…To prevent this excitation to spread across the entire circuit, lateral inhibition is required [94–96,100]. Whereas direct evidence for the cell-type providing this inhibition is lacking, local interneurons of the PB (closely resembling TB1 neurons from other insects [92,101]) appear to be the most promising candidates [100]. These cells have complex branching patterns [84,102] covering the entire PB and could connect all E-PG cells to one another in ways compatible with ring attractor circuits.…”