Polarized Skylight Navigation in Insects: Model and Electrophysiology of e-Vector Coding by Neurons in the Central Complex

Abstract

Sakura M, Lambrinos D, Labhart T. Polarized skylight navigation in insects: model and electrophysiology of e-vector coding by neurons in the central complex. J Neurophysiol 99: 667-682, 2008. First published December 5, 2007 doi:10.1152/jn.00784.2007. Many insects exploit skylight polarization for visual compass orientation or course control. As found in crickets, the peripheral visual system (optic lobe) contains three types of polarization-sensitive neurons (POL neurons), which are tuned to different (ϳ60°diverging) e-vector orientations. Thus each e-vector orientation elicits a specific combination of activities among the POL neurons coding any e-vector orientation by just three neural signals. In this study, we hypothesize that in the presumed orientation center of the brain (central complex) e-vector orientation is population-coded by a set of "compass neurons." Using computer modeling, we present a neural network model transforming the signal triplet provided by the POL neurons to compass neuron activities coding e-vector orientation by a population code. Using intracellular electrophysiology and cell marking, we present evidence that neurons with the response profile of the presumed compass neurons do indeed exist in the insect brain: each of these compass neuron-like (CNL) cells is activated by a specific e-vector orientation only and otherwise remains silent. Morphologically, CNL cells are tangential neurons extending from the lateral accessory lobe to the lower division of the central body. Surpassing the modeled compass neurons in performance, CNL cells are insensitive to the degree of polarization of the stimulus between 99% and at least down to 18% polarization and thus largely disregard variations of skylight polarization due to changing solar elevations or atmospheric conditions. This suggests that the polarization vision system includes a gain control circuit keeping the output activity at a constant level.

Linking the Input to the Output: New Sets of Neurons Complement the Polarization Vision Network in the Locust Central Complex

“…The polarity of CL1a cells is unique among columnar neurons in the locust central complex and suggests signaling from dendrites in the CBL to axonal outputs in the PB. Presumed input arborizations of CL1a neurons are concentrated in dorsal layers of the CBL, coinciding with layers served by TL2 tangential neurons, which are regarded as the dominant polarization-vision input to the CBL and have been also characterized in crickets (Sakura et al, 2008). In contrast, CL1b-d cells are likely to receive input in the PB and convey this information to the CBL.…”

Widespread Sensitivity to Looming Stimuli and Small Moving Objects in the Central Complex of an Insect Brain

“…In locusts, crickets, and monarch butterflies skylight polarization signals are processed in the CC (Sakura et al, 2008;Heinze and Reppert, 2011;Homberg et al, 2011). In desert locusts, a compass-like representation of zenithal E-vector tunings in the PB suggests that the CC plays a role as an internal sky compass (Heinze and Homberg, 2007).…”

Polarization-Sensitive Descending Neurons in the Locust: Connecting the Brain to Thoracic Ganglia

“…At the neuronal level, polarization vision pathways in the brain have been studied most extensively in locusts and crickets (Labhart and Meyer, 2002;Homberg, 2004). In these insects, the central complex is a major processing stage for polarized light (Vitzthum et al, 2002;Homberg, 2007, 2009;Sakura et al, 2008;). showed that polarization-sensitive (POL-) neurons connect the central complex to the lateral accessory lobes and the posterior protocerebrum, brain areas that are innervated by intersegmental neurons (Williams, 1975;Strausfeld and Seyan, 1985;Okada et al, 2003).…”