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

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.

2005 ◽  
Vol 94 (6) ◽  
pp. 3903-3915 ◽  
Author(s):  
Keram Pfeiffer ◽  
Michiyo Kinoshita ◽  
Uwe Homberg

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.


Author(s):  
Roy E. Ritzmann ◽  
Sasha N. Zill

This article discusses legged locomotion in insects. It describes the basic patterns of coordinated movement both within each leg and among the various legs. The nervous system controls these actions through groups of joint pattern generators coupled through interneurons and interjoint reflexes in a range of insect species. These local control systems within the thoracic ganglia rely on leg proprioceptors that monitor joint movement and cuticular strain interacting with central pattern generation interneurons. The local control systems can change quantitatively and qualitatively as needed to generate turns or more forceful movements. In dealing with substantial obstacles or changes in navigational movements, more profound changes are required. These rely on sensory information processed in the brain that projects to the multimodal sensorimotor neuropils collectively referred to as the central complex. The central complex affects descending commands that alter local control circuits to accomplish appropriate redirected movements.


2019 ◽  
Author(s):  
Ioannis Pisokas ◽  
Stanley Heinze ◽  
Barbara Webb

AbstractRecent studies of the Central Complex in the brain of the fruit fly have identified neurons with activity that tracks the animal’s heading direction. These neurons are part of a neuronal circuit with dynamics resembling those of a ring attractor. Other insects have a homologous circuit sharing a generally similar topographic structure but with significant structural and connectivity differences. We model the connectivity patterns in two insect species to investigate the effect of the differences on the dynamics of the circuit. We illustrate that the circuit found in locusts can also operate as a ring attractor and identify differences that enable the fruit fly circuit to respond faster to heading changes while they render the locust circuit more tolerant to noise. Our findings demonstrate that subtle differences in neuronal projection patterns can have a significant effect on the circuit performance and emphasise the need for a comparative approach in neuroscience.


2017 ◽  
Vol 118 (1) ◽  
pp. 496-506 ◽  
Author(s):  
Tobias Bockhorst ◽  
Uwe Homberg

Goal-directed behavior is often complicated by unpredictable events, such as the appearance of a predator during directed locomotion. This situation requires adaptive responses like evasive maneuvers followed by subsequent reorientation and course correction. Here we study the possible neural underpinnings of such a situation in an insect, the desert locust. As in other insects, its sense of spatial orientation strongly relies on the central complex, a group of midline brain neuropils. The central complex houses sky compass cells that signal the polarization plane of skylight and thus indicate the animal’s steering direction relative to the sun. Most of these cells additionally respond to small moving objects that drive fast sensory-motor circuits for escape. Here we investigate how the presentation of a moving object influences activity of the neurons during compass signaling. Cells responded in one of two ways: in some neurons, responses to the moving object were simply added to the compass response that had adapted during continuous stimulation by stationary polarized light. By contrast, other neurons disadapted, i.e., regained their full compass response to polarized light, when a moving object was presented. We propose that the latter case could help to prepare for reorientation of the animal after escape. A neuronal network based on central-complex architecture can explain both responses by slight changes in the dynamics and amplitudes of adaptation to polarized light in CL columnar input neurons of the system. NEW & NOTEWORTHY Neurons of the central complex in several insects signal compass directions through sensitivity to the sky polarization pattern. In locusts, these neurons also respond to moving objects. We show here that during polarized-light presentation, responses to moving objects override their compass signaling or restore adapted inhibitory as well as excitatory compass responses. A network model is presented to explain the variations of these responses that likely serve to redirect flight or walking following evasive maneuvers.


2020 ◽  
Vol 20 (4) ◽  
Author(s):  
Erica Ehrhardt ◽  
George Boyan

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.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Ioannis Pisokas ◽  
Stanley Heinze ◽  
Barbara Webb

Recent studies of the Central Complex in the brain of the fruit fly have identified neurons with activity that tracks the animal’s heading direction. These neurons are part of a neuronal circuit with dynamics resembling those of a ring attractor. The homologous circuit in other insects has similar topographic structure but with significant structural and connectivity differences. We model the connectivity patterns of two insect species to investigate the effect of these differences on the dynamics of the circuit. We illustrate that the circuit found in locusts can also operate as a ring attractor but differences in the inhibition pattern enable the fruit fly circuit to respond faster to heading changes while additional recurrent connections render the locust circuit more tolerant to noise. Our findings demonstrate that subtle differences in neuronal projection patterns can have a significant effect on circuit performance and illustrate the need for a comparative approach in neuroscience.


2015 ◽  
Vol 112 (36) ◽  
pp. 11395-11400 ◽  
Author(s):  
Basil el Jundi ◽  
Eric J. Warrant ◽  
Marcus J. Byrne ◽  
Lana Khaldy ◽  
Emily Baird ◽  
...  

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.


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