Amplitude and dynamics of polarization-plane signaling in the central complex of the locust brain

Abstract

The polarization pattern of skylight provides a compass cue that various insect species use for allocentric orientation. In the desert locust, Schistocerca gregaria, a network of neurons tuned to the electric field vector (E-vector) angle of polarized light is present in the central complex of the brain. Preferred E-vector angles vary along slices of neuropils in a compasslike fashion (polarotopy). We studied how the activity in this polarotopic population is modulated in ways suited to control compassguided locomotion. To this end, we analyzed tuning profiles using measures of correlation between spike rate and E-vector angle and, furthermore, tested for adaptation to stationary angles. The results suggest that the polarotopy is stabilized by antagonistic integration across neurons with opponent tuning. Downstream to the input stage of the network, responses to stationary E-vector angles adapted quickly, which may correlate with a tendency to steer a steady course previously observed in tethered flying locusts. By contrast, rotating E-vectors corresponding to changes in heading direction under a natural sky elicited nonadapting responses. However, response amplitudes were particularly variable at the output stage, covarying with the level of ongoing activity. Moreover, the responses to rotating E-vector angles depended on the direction of rotation in an anticipatory manner. Our observations support a view of the central complex as a substrate of higher-stage processing that could assign contextual meaning to sensory input for motor control in goal-driven behaviors. Parallels to higher-stage processing of sensory information in vertebrates are discussed.

Ultrastructure of GABA- and Tachykinin-Immunoreactive Neurons in the Lower Division of the Central Body of the Desert Locust

“…The present study supports electrophysiological data showing that CL1 neurons mainly receive inhibitory synaptic input from presynaptic neurons (Bockhorst and Homberg, 2015), likely to be the GABAergic TL2 and TL3 inputs to the CBL. The interactions between tangential and columnar neurons in the CBL is clearly an important step in shaping the topographic representation of preferred E -vector orientations in the slices of the PB, which occurs through neural computations and is not present at the level of TL neurons.…”

“…The lower division of the locust central body is composed of the processes of at least seven types of tangential neuron and two types of columnar neuron (Müller et al, 1997; Heinze and Homberg, 2008; Bockhorst and Homberg, 2015). Tangential neurons, termed TL1–6 and TLU1 ramify in distinct areas of the lateral complex and target certain (TL2, TL3, TL4) or all layers (TL1, TL5, TL6, TLU1) of the CBL.…”

What insects can tell us about the origins of consciousness

“…In locusts (Schistocerca gregaria) information on the distribution of polarized light in the sky is processed by the CX, which creates a central polarotopic representation of the sky polarization pattern (77). Outputs from this system could provide compass-like information to stabilize the direction of moving insects relative to the external celestial cue (78). This function for the CX has been described in locusts and butterflies (Danaus plexippus) but may be common across insect orders (79).…”

Spatial Navigation and the Central Complex: Sensory Acquisition, Orientation, and Motor Control

“…Included in this list are polarized light (Heinze and Homberg, 2007; Sakura et al, 2008; Heinze et al, 2009), mechanical deflection of the antenna (Ritzmann et al, 2008) and various forms of non-polarized signals (Heinze and Reppert, 2011; Rosner and Homberg, 2013; Seelig and Jayaraman, 2013; Kathman et al, 2014; Bockhorst and Homberg, 2015). For the goal-directed navigational task outlined above, antennal and visual cues appear to be very important.…”