Computations and mechanisms underlying sky- compass dependent head direction coding in the desert locust

• Applicants: Professor Dominik M. Endres, Ph.D.; Professor Dr. Uwe Homberg
• Subject Area: Cognitive, Systems and Behavioural Neurobiology ; Experimental and Theoretical Network Neuroscience
• Term: from 2020 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 452193090

• Final Report Year: 2024

Final Report Abstract

Orientation in space is of fundamental importance in all animals, particularly in species that are able to cover large distances in short time, such as insects and vertebrates. Local and global cues as well as internal signals allow these animals to efficiently navigate within familiar terrain and beyond, return to a nest, or perform goal oriented long-range seasonal migrations. In insects the central complex plays a fundamental role in navigational control. It receives a multitude of sensory inputs to its layers, and as shown in desert locusts and fruit flies, consist of arrays of columns which together form an internal representation of space around the animal (head-direction coding). Desert locusts are seasonally migratory insects. Compass coding in the locust central complex largely depends on the position of the sun, more precisely on solar azimuth and the corresponding polarization pattern of the sky. While computational modelling using data from the fly Drosophila suggest a ring-attractor mechanism to establish the internal compass in the central complex, the mechanisms underlying compass formation and its shift during turns are less well understood in the locust. Several striking differences in neural organization of the central complex between the fly and the locust prompted us to investigate through computational modelling whether a stable representation of heading directions can be maintained by the locust central complex network and how shifts in this representation might occur during turns of the animal. These modelling data should be complemented by further analysis of the functional properties of the constituent neurons. Modelling showed that the neural network of the locust central complex is capable of robust head-direction coding. It can produce and maintain goal-directed steering output even under perturbations such as simulated wind gusts. Unlike in Drosophila, however, we did not find a solution for shifts in the activity peak across the compass during right or left turns by feed forward input, instead our model requires turning direction-dependent neuromodulation. Our modelling was constrained by data on the physiological and anatomical properties of central-complex neurons. Columnar neurons of the central complex sensitive to rotational self-motion were identified in the locust and appear to be homologous to rotation sensitive neurons in the fly. Taken together, the data and modelling results show that goal-directed steering is possible with a neural network constrained by data from the desert locust.

Publications

• Organization and neural connections of the lateral complex in the brain of the desert locust. Journal of Comparative Neurology, 529(15), 3533-3560.
  Hensgen, Ronja; Göthe, Jonas; Jahn, Stefanie; Hümmert, Sophie; Schneider, Kim Lucia; Takahashi, Naomi; Pegel, Uta; Gotthardt, Sascha & Homberg, Uwe
  
• A model for optic flow integration in locust central-complex neurons tuned to head direction. Proc Annu Meeting Cog Science Soc 44.
  Pabst K., Zittrell F., Homberg U. & Endres D.M.
  
• Myoinhibitory peptides in the central complex of the locust Schistocerca gregaria and colocalization with locustatachykinin‐related peptides. Journal of Comparative Neurology, 530(15), 2782-2801.
  Hensgen, Ronja; Dippel, Stefan; Hümmert, Sophie; Jahn, Stefanie; Seyfarth, Jutta & Homberg, Uwe
  
• Performance of polarization-sensitive neurons of the locust central complex at different degrees of polarization. Journal of Comparative Physiology A, 208(3), 387-403.
  Hensgen, Ronja; Zittrell, Frederick; Pfeiffer, Keram & Homberg, Uwe
  
• Receptive field structures for two celestial compass cues at the input stage of the central complex in the locust brain. Journal of Experimental Biology, 225(4).
  Takahashi, Naomi; Zittrell, Frederick; Hensgen, Ronja & Homberg, Uwe
  
• The sky compass network in the brain of the desert locust. Journal of Comparative Physiology A, 209(4), 641-662.
  Homberg, Uwe; Hensgen, Ronja; Jahn, Stefanie; Pegel, Uta; Takahashi, Naomi; Zittrell, Frederick & Pfeiffer, Keram
  
• Integration of optic flow into the sky compass network in the brain of the desert locust. Frontiers in Neural Circuits, 17.
  Zittrell, Frederick; Pabst, Kathrin; Carlomagno, Elena; Rosner, Ronny; Pegel, Uta; Endres, Dominik M. & Homberg, Uwe
  
• Organization of descending neurons in the brain of the desert locust. Journal of Comparative Neurology, 531(14), 1350-1380.
  Staudacher, Erich M.; Cigan, Michel‐Leon; Wenz, Felix; Pollun, Aleksandra; Beck, Sascha; Beck, Marius; Reh, Fabienne; Haas, Judith & Homberg, Uwe
  
• A computational model for angular velocity integration in a locust heading circuit. openRxiv.
  Pabst, Kathrin; Gkanias, Evripidis; Webb, Barbara; Homberg, Uwe & Endres, Dominik
  
• From sky to compass: a model of the desert locust sky-compass circuit. Bernstein Conference
  Pabst K., Homberg U. & Endres D.