Different Roles for Homologous Interneurons in Species Exhibiting Similar Rhythmic Behaviors

Sakurai, Akira; Newcomb, James M.; Lillvis, Joshua L.; Katz, Paul S.

doi:10.1016/j.cub.2011.04.040

Cited by 60 publications

(102 citation statements)

References 31 publications

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“…The independent evolution of click-type calling in these species thus represents convergence on a similar behavioural phenotype or parallel evolution [21]. Our findings provide an example of behavioural similarity that occurred via distinct reconfigurations of neural circuits, similar to the case of swimming behaviours and neural circuits of nudibranchs [22].…”

Section: Discussionsupporting

confidence: 51%

Distinct neural and neuromuscular strategies underlie independent evolution of simplified advertisement calls

Leininger

Kelley

2013

Proc. R. Soc. B.

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Independent or convergent evolution can underlie phenotypic similarity of derived behavioural characters. Determining the underlying neural and neuromuscular mechanisms sheds light on how these characters arose. One example of evolutionarily derived characters is a temporally simple advertisement call of male African clawed frogs (Xenopus) that arose at least twice independently from a more complex ancestral pattern. How did simplification occur in the vocal circuit? To distinguish shared from divergent mechanisms, we examined activity from the calling brain and vocal organ (larynx) in two species that independently evolved simplified calls. We find that each species uses distinct neural and neuromuscular strategies to produce the simplified calls. Isolated Xenopus borealis brains produce fictive vocal patterns that match temporal patterns of actual male calls; the larynx converts nerve activity faithfully into muscle contractions and single clicks. In contrast, fictive patterns from isolated Xenopus boumbaensis brains are short bursts of nerve activity; the isolated larynx requires stimulus bursts to produce a single click of sound. Thus, unlike X. borealis, the output of the X. boumbaensis hindbrain vocal pattern generator is an ancestral burst-type pattern, transformed by the larynx into single clicks. Temporally simple advertisement calls in genetically distant species of Xenopus have thus arisen independently via reconfigurations of central and peripheral vocal neuroeffectors.

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Section: Discussionsupporting

confidence: 51%

Distinct neural and neuromuscular strategies underlie independent evolution of simplified advertisement calls

Leininger

Kelley

2013

Proc. R. Soc. B.

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“…Given that such tracts are laid down early in development and are highly conserved among insect groups (28), it is possible that this variation in pathway reflects a change in the neural "wiring" of the wing control circuitry. For example, a homologous neuron involved in swimming pattern generation has been found to carry out different functions in two closely related sea slugs (nudibranchs) that exhibit similar swimming modalities (29). To address such evolutionary questions about the dichotomy between the TSDNs in hawker and percher dragonflies, the mesothoracic and metathoracic branching patterns of the Aeshnid TSDNs also need to be investigated.…”

Section: Discussionmentioning

confidence: 99%

Eight pairs of descending visual neurons in the dragonfly give wing motor centers accurate population vector of prey direction

Gonzalez-Bellido

Peng

Yang

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Intercepting a moving object requires prediction of its future location. This complex task has been solved by dragonflies, who intercept their prey in midair with a 95% success rate. In this study, we show that a group of 16 neurons, called target-selective descending neurons (TSDNs), code a population vector that reflects the direction of the target with high accuracy and reliability across 360°. The TSDN spatial (receptive field) and temporal (latency) properties matched the area of the retina where the prey is focused and the reaction time, respectively, during predatory flights. The directional tuning curves and morphological traits (3D tracings) for each TSDN type were consistent among animals, but spike rates were not. Our results emphasize that a successful neural circuit for target tracking and interception can be achieved with few neurons and that in dragonflies this information is relayed from the brain to the wing motor centers in population vector form.vision | invertebrate | predatory behavior | electrophysiology | confocal microscopy D ragonflies continuously track their prey (1) during short predatory flights (∼200-500 ms) (1-3) by keeping the image of the moving prey on the specialized dorsal area of their eyes (1). If the prey image drifts on the retina, compensatory motor signals sent to the wings adjust the dragonfly body position to bring the prey image back. This process allows a dragonfly to visually track the prey by locking on to it, a process also named fixation (4).The ability to fixate on a moving target is a common feature among most predatory animals. Once a pursuer's eyes are fixated on the prey, it can aim toward the current or the future prey location. The first choice results in classical pursuit, whereas the second one yields interception. Dragonflies are thought to intercept their prey by keeping a constant bearing to their target. This strategy is also used by other species, e.g., a human catching a ball (5, 6), but the nervous system of dragonflies presents a favorable substrate for studying the neural basis of this behavior. This ancient prey-targeting system is tractable and tuned for extreme performance, as evidenced by the accuracy (around 95%) (1, 2) and speed at which it functions.We aimed to understand the information sent to the wings when a target moves across the dragonfly visual field. In particular, we have tested whether the population vector algorithm can successfully decode the directional component of the descending information. The population vector is the weighted sum activity of an ensemble of neurons with directional tuning. It was first shown to predict the direction of an upcoming arm movement in monkeys (7,8). Since then, the population vector algorithm has described successfully the directional responses to mechanical stimulation in several invertebrate species (9-12). The dragonfly predatory flight provides a challenge for a reliable vector code. Not only are these animals highly maneuverable, with independent control of the fore and hind wings (13) a...

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“…The exact copy of the syllable period of the solo chirp together with the robustness of coding in natural background noise (see below) suggests that the pair of TN1 neurons might also play an important role in intraspecific communication in M. elongata . Thus, similar to the neuronal network for swimming in molluscs (Sakurai et al, 2011), homologous interneurons might have different roles in different species.…”

Section: Discussionmentioning

confidence: 98%

Neuronal correlates of a preference for leading signals in the synchronizing bushcricketMecopoda elongata(Orthoptera, Tettigoniidae)

Siegert

Römer

Hashim

et al. 2011

Journal of Experimental Biology

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SUMMARYAcoustically interacting males of the tropical katydid Mecopoda elongata synchronize their chirps imperfectly, so that one male calls consistently earlier in time than the other. In choice situations, females prefer the leader signal, and it has been suggested that a neuronal mechanism based on directional hearing may be responsible for the asymmetric, stronger representation of the leader signal in receivers. Here, we investigated the potential mechanism in a pair of interneurons (TN1 neuron) of the afferent auditory pathway, known for its contralateral inhibitory input in directional hearing. In this interneuron, conspecific signals are reliably encoded under natural conditions, despite high background noise levels. Unilateral presentations of a conspecific chirp elicited a TN1 response where each suprathreshold syllable in the chirp was reliably copied in a phase-locked fashion. Two identical chirps broadcast with a 180 deg spatial separation resulted in a strong suppression of the response to the follower signal, when the time delay was 20 ms or more. Muting the ear on the leader side fully restored the response to the follower signal compared with unilateral controls. Time–intensity trading experiments, in which the disadvantage of the follower signal was traded against higher sound pressure levels, demonstrated the dominating influence of signal timing on the TN1 response, and this was especially pronounced at higher sound levels of the leader. These results support the hypothesis that the female preference for leader signals in M. elongata is the outcome of a sensory mechanism that originally evolved for directional hearing.

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Different Roles for Homologous Interneurons in Species Exhibiting Similar Rhythmic Behaviors

Cited by 60 publications

References 31 publications

Distinct neural and neuromuscular strategies underlie independent evolution of simplified advertisement calls

Distinct neural and neuromuscular strategies underlie independent evolution of simplified advertisement calls

Eight pairs of descending visual neurons in the dragonfly give wing motor centers accurate population vector of prey direction

Neuronal correlates of a preference for leading signals in the synchronizing bushcricketMecopoda elongata(Orthoptera, Tettigoniidae)

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