Sensory signal processing in the central complex of the cockroach Rhyparobia maderae

• Applicant: Professor Dr. Uwe Homberg
• Subject Area: Cognitive, Systems and Behavioural Neurobiology
• Term: from 2019 to 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 418011225

• Final Report Year: 2024

Final Report Abstract

Insects master, like vertebrates, sophisticated ways of spatial orientation that allow them to perform goal-directed seasonal migrations, or the return to a distant nest. For determining navigational directions, insects often rely on the position of the sun (sun compass orientation), and in doing so can not only adjust their orientation relative to direct sunlight, but also relative to the polarization pattern of the blue sky, which is generated by the sun, but not visible to humans. These signals are evaluated by a central brain structure, the central complex, and transformed into goal-directed steering commands during walking or flight. The central complex is composed of a neural network, consisting of horizontal layers and orthogonal arrays of vertical columns. In desert locust and fruit flies it resembles an internal compass, which provides a 360° representation of spatial directions used for orientation purposes. The present project was aimed at investigating the anatomical organization of the central complex in a nocturnal insect, the Madeira cockroach Rhyparobia maderae. In addition, we wanted to explore whether central-complex neurons are sensitive to sky compass signals, and whether these are integrated with other navigation-related sensory inputs such as mechanosensory signals from the antennae. The anatomical organization of the central complex was studied in detail. The neuroarchitecture of the cockroach central complex resembles that of the locust, but shows several specialties compared to other insects. The input stage of the central complex, the lower division of the central body, is not organized in layers as in other insects, but instead consists of intercalated arrays of cone- and tooth-like components. Many neurons have prominent connections with a neighboring brain region, the anterior lip, which is highly reduced in other insects and completely missing in flies. The anterior optic tubercle, a relay station in the polarization vision pathway to the central complex, is present, but highly reduced in size. Intracellular recordings showed that neurons, which are sensitive to skycompass signals in other insects, are also sensitive to polarized light and the direction of an unpolarized light spot (sun) in the cockroach, however, these responses were less prominent and even completely missing in some recordings. Taken together, the project showed that like in day-active species, sky compass signals are processed in the central complex of the nocturnal cockroach. We assume, however, that these are combined with other unexplored sensory inputs for head- and goal-direction coding in the cockroach.

Publications

• A unified platform to manage, share, and archive morphological and functional data in insect neuroscience. eLife, 10.
  Heinze, Stanley; el Jundi, Basil; Berg, Bente G.; Homberg, Uwe; Menzel, Randolf; Pfeiffer, Keram; Hensgen, Ronja; Zittrell, Frederick; Dacke, Marie; Warrant, Eric; Pfuhl, Gerit; Rybak, Jürgen & Tedore, Kevin
  
• Distribution and daily oscillation of GABA in the circadian system of the cockroach Rhyparobia maderae. Journal of Comparative Neurology, 530(5), 770-791.
  Massah, Azar; Neupert, Susanne; Brodesser, Susanne; Homberg, Uwe & Stengl, Monika
  
• Tyrosine hydroxylase immunostaining in the central complex of dicondylian insects. Journal of Comparative Neurology, 529(12), 3131-3154.
  Timm, Josephine; Scherner, Mara; Matschke, Jannik; Kern, Martina & Homberg, Uwe
  
• 3D‐atlas of the brain of the cockroach Rhyparobia maderae. Journal of Comparative Neurology, 530(18), 3126-3156.
  Althaus, Vanessa; Jahn, Stefanie; Massah, Azar; Stengl, Monika & Homberg, Uwe
  
• Comparative morphology of serotonin‐immunoreactive neurons innervating the central complex in the brain of dicondylian insects. Journal of Comparative Neurology, 531(14), 1482-1508.
  Homberg, Uwe; Kirchner, Michelle; Kowalewski, Kevin; Pitz, Vanessa; Kinoshita, Michiyo; Kern, Martina & Seyfarth, Jutta
  
• Neuroarchitecture of the central complex in the Madeira cockroach Rhyparobia maderae: Pontine and columnar neuronal cell types. Journal of Comparative Neurology, 531(16), 1689-1714.
  Jahn, Stefanie; Althaus, Vanessa; Heckmann, Jannik; Janning, Mona; Seip, Ann‐Katrin; Takahashi, Naomi; Grigoriev, Clara; Kolano, Juliana & Homberg, Uwe
  
• Anatomical organization of the cerebrum of the praying mantis Hierodula membranacea. Journal of Comparative Neurology, 532(3).
  Althaus, Vanessa; Exner, Gesa; von Hadeln, Joss; Homberg, Uwe & Rosner, Ronny