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The Journal of Neuroscience, September 23, 2009, 29(38):11783-11793; doi:10.1523/JNEUROSCI.1870-09.2009

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Behavioral/Systems/Cognitive
Transformation of Polarized Light Information in the Central Complex of the Locust

Stanley Heinze, Sascha Gotthardt, and Uwe Homberg

Fachbereich Biologie, Tierphysiologie, Philipps-Universität Marburg, D-35032 Marburg, Germany

Correspondence should be addressed to Uwe Homberg, Fachbereich Biologie, Tierphysiologie, Universität Marburg, D-35032 Marburg, Germany. Email: homberg{at}staff.uni-marburg.de

Many insects perceive the E-vector orientation of polarized skylight and use it for compass navigation. In locusts, polarized light is detected by photoreceptors of the dorsal rim area of the eye. Polarized light signals from both eyes are integrated in the central complex (CC), a group of neuropils in the center of the brain. Thirteen types of CC neuron are sensitive to dorsally presented, polarized light (POL-neurons). These neurons interconnect the subdivisions of the CC, particularly the protocerebral bridge (PB), the upper and lower divisions of the central body (CBU, CBL), and the adjacent lateral accessory lobes (LALs). All POL-neurons show polarization-opponency, i.e., receive excitatory and inhibitory input at orthogonal E-vector orientations. To provide physiological evidence for the direction of information flow through the polarization vision network in the CC, we analyzed the functional properties of the different cell types through intracellular recordings. Tangential neurons of the CBL showed highest signal-to-noise ratio, received either ipsilateral polarized-light input only or, together with CL1 columnar neurons, had eccentric receptive fields. Bilateral polarized-light inputs with zenith-centered receptive fields were found in tangential neurons of the PB and in columnar neurons projecting to the LALs. Together with other physiological parameters, these data suggest a flow of information from the CBL (input) to the PB and from here to the LALs (output). This scheme is supported by anatomical data and suggests transformation of purely sensory E-vector coding at the CC input stage to position-invariant coding of 360°-compass directions at the output stage.

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Received April 20, 2009; revised July 16, 2009; accepted Aug. 7, 2009.

Correspondence should be addressed to Uwe Homberg, Fachbereich Biologie, Tierphysiologie, Universität Marburg, D-35032 Marburg, Germany. Email: homberg{at}staff.uni-marburg.de

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