Dipteran Halteres: Perspectives on Function and Integration for a Unique Sensory Organ

Yarger, Alexandra M.; Fox, Jessica L.

doi:10.1093/icb/icw086

Cited by 30 publications

(36 citation statements)

References 56 publications

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“…Although it is formally possible that the haltere clock supports temperature synchronization of the central brain clock (see above), it seems more likely that it fulfils a more direct physiological function in this proprioceptive sensory organ. Clock gene expression in the Drosophila haltere was observed in cells that most likely represent campaniform sensilla, the principle haltere mechanosensory neurons Yarger and Fox, 2016). In contrast, no clock gene expression in the other haltere mechanosensory cell type, the chordotonal organ neuron, could be detected ).…”

Section: Why a Peripheral Clock In The Haltere?mentioning

confidence: 92%

“…(Glaser and Stanewsky, 2005)). We identified a robust, self-sustained 24-hr oscillator in the fly's haltere, an organ important for proprioceptive feedback during flight and in some insects also walking (Yarger and Fox, 2016). Surprisingly, the haltere clock is over-compensated against temperature changes, i.e., it slows down with increasing temperature rather than speeding up.…”

Section: Introductionmentioning

confidence: 94%

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A robust and self-sustained peripheral circadian oscillator reveals differences in temperature compensation properties with central brain clocks

Versteven

Ernst

Stanewsky

2020

Preprint

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Circadian clocks temporally organize physiology and behavior of organisms exposed to the daily changes of light and temperature on our planet, thereby contributing to fitness and health. Circadian clocks and the biological rhythms they control are characterized by three properties. (1) The rhythms are self-sustained in constant conditions with a period of ~ 24 hr,(2), they can be synchronized to the environmental cycles of light and temperature, and (3), they are temperature compensated, meaning they run with the same speed at different temperatures within the physiological range of the organism. Apart from the central clocks located in or near the brain, which regulate the daily activity rhythms of animals, the so-called peripheral clocks are dispersed throughout the body of insects and vertebrates. Based on the three defining properties, it has been difficult to determine if these peripheral clocks are true circadian clocks. We used a set of clock gene -luciferase reporter genes to address this question in Drosophila circadian clocks. We show that self-sustained fly peripheral oscillators over compensate temperature changes, i.e., they slow down with increasing temperature.This over-compensation is not observed in central clock neurons in the fly brain, both in intact flies and in cultured brains, suggesting that neural network properties contribute to temperature compensation. However, an important neuropeptide for synchronizing the circadian neuronal network, the Pigment Dispersing Factor (PDF), is not required for selfsustained and temperature-compensated oscillations in subsets of the central clock neurons.Our findings reveal a fundamental difference between central and peripheral clocks, which likely also applies for vertebrate clocks.

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Section: Why a Peripheral Clock In The Haltere?mentioning

confidence: 92%

Section: Introductionmentioning

confidence: 94%

A robust and self-sustained peripheral circadian oscillator reveals differences in temperature compensation properties with central brain clocks

Versteven

Ernst

Stanewsky

2020

Preprint

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“…This inertial force is manifest as Coriolis forces (see Glossary) that cause the haltere stalk to bend in directions orthogonal to the rotation plane, thereby stimulating the mechanosensory fields located at the base (Pringle, 1948;Nalbach, 1993Nalbach, , 1994. The mechanosensory feedback, encoding information about pitch, roll and yaw turns, thus rapidly informs the fly about its own body rotations (Nalbach and Hengstenberg, 1994;Fox and Daniel, 2008;Fox et al, 2010, Yarger andFox, 2016). Although insects also combine visual and olfactory information with mechanosensory feedback to stabilize flight and steer towards a target (Götz, 1968;Heide and Götz, 1996;Willis and Arbas, 1998;Egelhaaf and Kern, 2002), the mechanosensory feedback acts on a much shorter time scale than vision or olfaction (Hengstenberg et al, 1986;Hengstenberg, 1988;Trimarchi and Schneiderman, 1995a,b;Dickinson, 2003, 2004;Bender and Dickinson, 2006).…”

Section: Coordination Of Wings and Halteres Involves Passive Linkagesmentioning

confidence: 99%

Mechanics of the thorax in flies

Deora

Gundiah

Sane

2017

Journal of Experimental Biology

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Insects represent more than 60% of all multicellular life forms, and are easily among the most diverse and abundant organisms on earth. They evolved functional wings and the ability to fly, which enabled them to occupy diverse niches. Insects of the hyper-diverse orders show extreme miniaturization of their body size. The reduced body size, however, imposes steep constraints on flight ability, as their wings must flap faster to generate sufficient forces to stay aloft. Here, we discuss the various physiological and biomechanical adaptations of the thorax in flies which enabled them to overcome the myriad constraints of small body size, while ensuring very precise control of their wing motion. One such adaptation is the evolution of specialized myogenic or asynchronous muscles that power the high-frequency wing motion, in combination with neurogenic or synchronous steering muscles that control higher-order wing kinematic patterns. Additionally, passive cuticular linkages within the thorax coordinate fast and yet precise bilateral wing movement, in combination with an actively controlled clutch and gear system that enables flexible flight patterns. Thus, the study of thoracic biomechanics, along with the underlying sensory-motor processing, is central in understanding how the insect body form is adapted for flight.

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“…In flies, stable flight requires proprioceptive organs called halteres that detect body rotations (Yarger and Fox, 2016). Rapid flight maneuvers used in visually guided behaviors (Land and Collett, 1974) require fast feedback about body position, with delays no longer than tens of milliseconds (Dickinson and Muijres, 2016).…”

Section: Introductionmentioning

confidence: 99%

Representation of Haltere Oscillations and Integration with Visual Inputs in the Fly Central Complex

Kathman

Fox

2019

J. Neurosci.

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The reduced hindwings of flies, known as halteres, are specialized mechanosensory organs that detect body rotations during flight. Primary afferents of the haltere encode its oscillation frequency linearly over a wide bandwidth and with precise phase-dependent spiking. However, it is not currently known whether information from haltere primary afferent neurons is sent to higher brain centers where sensory information about body position could be used in decision making, or whether precise spike timing is useful beyond the peripheral circuits that drive wing movements. We show that in cells in the central brain, the timing and rates of neural spiking can be modulated by sensory input from experimental haltere movements (driven by a servomotor). Using multichannel extracellular recording in restrained flesh flies (Sarcophaga bullata of both sexes), we examined responses of central complex cells to a range of haltere oscillation frequencies alone, and in combination with visual motion speeds and directions. Haltere-responsive units fell into multiple response classes, including those responding to any haltere motion and others with firing rates linearly related to the haltere frequency. Cells with multisensory responses showed higher firing rates than the sum of the unisensory responses at higher haltere frequencies. They also maintained visual properties, such as directional selectivity, while increasing response gain nonlinearly with haltere frequency. Although haltere inputs have been described extensively in the context of rapid locomotion control, we find haltere sensory information in a brain region known to be involved in slower, higher-order behaviors, such as navigation.Many animals use vision for navigation; however, these cues must be interpreted in the context of the body's position. In mammalian brains, hippocampal cells combine visual and vestibular information to encode head direction. A region of the arthropod brain, known as the central complex (CX), similarly encodes heading information, but it is unknown whether proprioceptive information is integrated here as well. We show that CX neurons respond to input from halteres, specialized proprioceptors in flies that detect body rotations. These neurons also respond to visual input, providing one of the few examples of multiple sensory modalities represented in individual CX cells. Haltere stimulation modifies neural responses to visual signals, providing a mechanism for integrating vision with proprioception.

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Dipteran Halteres: Perspectives on Function and Integration for a Unique Sensory Organ

Cited by 30 publications

References 56 publications

A robust and self-sustained peripheral circadian oscillator reveals differences in temperature compensation properties with central brain clocks

A robust and self-sustained peripheral circadian oscillator reveals differences in temperature compensation properties with central brain clocks

Mechanics of the thorax in flies

Representation of Haltere Oscillations and Integration with Visual Inputs in the Fly Central Complex

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