Polarization-Sensitive and Light-Sensitive Neurons in Two Parallel Pathways Passing Through the Anterior Optic Tubercle in the Locust Brain

2005 ◽  
Vol 94 (6) ◽  
pp. 3903-3915 ◽  
Author(s):  
Keram Pfeiffer ◽  
Michiyo Kinoshita ◽  
Uwe Homberg
Keyword(s):  
Schistocerca Gregaria ◽  
Polarized Light ◽  
Central Complex ◽  
Stimulus Position ◽  
Sun Compass ◽  
Lower Unit ◽  
Linearly Polarized ◽  
First Time ◽  
The Brain ◽  
Lateral Accessory Lobe

Many migrating animals use a sun compass for long-range navigation. One of the guiding cues used by insects is the polarization pattern of the blue sky. In the desert locust Schistocerca gregaria, neurons of the central complex, a neuropil in the center of the brain, are sensitive to polarized light and might serve a key role in compass navigation. Visual pathways to the central complex include signal processing in the upper and lower units of the anterior optic tubercle. To determine whether these pathways carry polarization-vision signals, we have recorded the responses of interneurons of the optic tubercle of the locust to visual stimuli including polarized light. All neurons of the lower unit but only one of five recorded neurons of the upper unit of the tubercle were sensitive to linearly polarized light presented in the dorsal visual field. These neurons showed polarization opponency, or a sinusoidal modulation of activity, during stimulation through a rotating polarizer. Two types of bilateral interneurons preferred particular e-vector orientations, reflecting the presence of bilateral pairs of these neurons in the brain. We show here for the first time neurons with projections to the lateral accessory lobe that are suited to provide polarization input to the central complex. All neurons of the tubercle, furthermore, responded to unpolarized light, mostly with tonic activity changes. These responses strongly depended on stimulus position and might reflect navigation-relevant signals such as direct sunlight or visual landmarks that are integrated with polarization responses in neurons of the lower unit.

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

2015 ◽  
Vol 113 (9) ◽  
pp. 3291-3311 ◽  
Author(s):  
Tobias Bockhorst ◽  
Uwe Homberg
Keyword(s):  
Schistocerca Gregaria ◽  
Sensory Information ◽  
Polarized Light ◽  
Polarization Plane ◽  
Field Vector ◽  
Central Complex ◽  
Output Stage ◽  
Heading Direction ◽  
Vector Angle ◽  
The Brain

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 compass-guided 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.

scholarly journals Neural coding underlying the cue preference for celestial orientation

2015 ◽  
Vol 112 (36) ◽  
pp. 11395-11400 ◽  
Author(s):  
Basil el Jundi ◽  
Eric J. Warrant ◽  
Marcus J. Byrne ◽  
Lana Khaldy ◽  
Emily Baird ◽  
...  
Keyword(s):  
Celestial Body ◽  
Neural Coding ◽  
Polarized Light ◽  
Central Complex ◽  
Visual Orientation ◽  
The Sun ◽  
Light Conditions ◽  
Celestial Orientation ◽  
First Time ◽  
The Brain

Diurnal and nocturnal African dung beetles use celestial cues, such as the sun, the moon, and the polarization pattern, to roll dung balls along straight paths across the savanna. Although nocturnal beetles move in the same manner through the same environment as their diurnal relatives, they do so when light conditions are at least 1 million-fold dimmer. Here, we show, for the first time to our knowledge, that the celestial cue preference differs between nocturnal and diurnal beetles in a manner that reflects their contrasting visual ecologies. We also demonstrate how these cue preferences are reflected in the activity of compass neurons in the brain. At night, polarized skylight is the dominant orientation cue for nocturnal beetles. However, if we coerce them to roll during the day, they instead use a celestial body (the sun) as their primary orientation cue. Diurnal beetles, however, persist in using a celestial body for their compass, day or night. Compass neurons in the central complex of diurnal beetles are tuned only to the sun, whereas the same neurons in the nocturnal species switch exclusively to polarized light at lunar light intensities. Thus, these neurons encode the preferences for particular celestial cues and alter their weighting according to ambient light conditions. This flexible encoding of celestial cue preferences relative to the prevailing visual scenery provides a simple, yet effective, mechanism for enabling visual orientation at any light intensity.

scholarly journals Matched-filter coding of sky polarization results in an internal sun compass in the brain of the desert locust

2020 ◽  
Vol 117 (41) ◽  
pp. 25810-25817
Author(s):  
Frederick Zittrell ◽  
Keram Pfeiffer ◽  
Uwe Homberg
Keyword(s):  
Spatial Orientation ◽  
Matched Filter ◽  
Polarized Light ◽  
Central Complex ◽  
Insect Brain ◽  
The Sun ◽  
Polarization Pattern ◽  
Sun Compass ◽  
Small Spot ◽  
Polarization Compass

Many animals use celestial cues for spatial orientation. These include the sun and, in insects, the polarization pattern of the sky, which depends on the position of the sun. The central complex in the insect brain plays a key role in spatial orientation. In desert locusts, the angle of polarized light in the zenith above the animal and the direction of a simulated sun are represented in a compass-like fashion in the central complex, but how both compasses fit together for a unified representation of external space remained unclear. To address this question, we analyzed the sensitivity of intracellularly recorded central-complex neurons to the angle of polarized light presented from up to 33 positions in the animal’s dorsal visual field and injected Neurobiotin tracer for cell identification. Neurons were polarization sensitive in large parts of the virtual sky that in some cells extended to the horizon in all directions. Neurons, moreover, were tuned to spatial patterns of polarization angles that matched the sky polarization pattern of particular sun positions. The horizontal components of these calculated solar positions were topographically encoded in the protocerebral bridge of the central complex covering 360° of space. This whole-sky polarization compass does not support the earlier reported polarization compass based on stimulation from a small spot above the animal but coincides well with the previously demonstrated direct sun compass based on unpolarized light stimulation. Therefore, direct sunlight and whole-sky polarization complement each other for robust head direction coding in the locust central complex.

scholarly journals Sun compass neurons are tuned to migratory orientation in monarch butterflies 

2021 ◽  
Vol 288 (1945) ◽  
pp. 20202988
Author(s):  
Tu Anh Thi Nguyen ◽  
M. Jerome Beetz ◽  
Christine Merlin ◽  
Basil el Jundi
Keyword(s):  
North America ◽  
Neural Coding ◽  
Central Complex ◽  
Central Mexico ◽  
The Sun ◽  
Monarch Butterflies ◽  
Sun Compass ◽  
Migratory Form ◽  
Orientation Information ◽  
The Brain

Every autumn, monarch butterflies migrate from North America to their overwintering sites in Central Mexico. To maintain their southward direction, these butterflies rely on celestial cues as orientation references. The position of the sun combined with additional skylight cues are integrated in the central complex, a region in the butterfly's brain that acts as an internal compass. However, the central complex does not solely guide the butterflies on their migration but also helps monarchs in their non-migratory form manoeuvre on foraging trips through their habitat. By comparing the activity of input neurons of the central complex between migratory and non-migratory butterflies, we investigated how a different lifestyle affects the coding of orientation information in the brain. During recording, we presented the animals with different simulated celestial cues and found that the encoding of the sun was narrower in migratory compared to non-migratory butterflies. This feature might reflect the need of the migratory monarchs to rely on a precise sun compass to keep their direction during their journey. Taken together, our study sheds light on the neural coding of celestial cues and provides insights into how a compass is adapted in migratory animals to successfully steer them to their destination.

scholarly journals Evidence for the cholinergic markers ChAT and vAChT in sensory cells of the developing antennal nervous system of the desert locust Schistocerca gregaria

2020 ◽  
Vol 20 (4) ◽  
Author(s):  
Erica Ehrhardt ◽  
George Boyan
Keyword(s):  
Nervous System ◽  
Schistocerca Gregaria ◽  
Central Complex ◽  
Sensory Cells ◽  
Desert Locust ◽  
Cholinergic Transmission ◽  
Sensory Axons ◽  
First Instar ◽  
The Brain ◽  
Antennal Nerve

AbstractSensory and motor systems in insects with hemimetabolous development must be ready to mediate adaptive behavior directly on hatching from the egg. For the desert locust S. gregaria, cholinergic transmission from antennal sensillae to olfactory or mechanosensory centers in the brain requires that choline acetyltransferase (ChAT) and the vesicular acetylcholine transporter (vAChT) already be present in sensory cells in the first instar. In this study, we used immunolabeling to demonstrate that ChAT and vAChT are both expressed in sensory cells from identifiable sensilla types in the immature antennal nervous system. We observed ChAT expression in dendrites, neurites and somata of putative basiconic-type sensillae at the first instar stage. We also detected vAChT in the sensory axons of these sensillae in a major antennal nerve tract. We then examined whether evidence for cholinergic transmission is present during embryogenesis. Immunolabeling confirms that vAChT is expressed in somata typical of campaniform sensillae, as well as in small sensory cell clusters typically associated with either a large basiconic or coeloconic sensilla, at 99% of embryogenesis. The vAChT is also expressed in the somata of these sensilla types in multiple antennal regions at 90% of embryogenesis, but not at earlier (70%) embryonic stages. Neuromodulators are known to appear late in embryogenesis in neurons of the locust central complex, and the cholinergic system of the antenna may also only reach maturity shortly before hatching.

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