The auditory efferent system in mosquitoes

Loh, YuMin M.; Su, Matthew P.; Ellis, D. S.; Andrés, Marta

doi:10.3389/fcell.2023.1123738

Cited by 16 publications

(15 citation statements)

References 115 publications

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“…However, mosquitoes possess serotonergic innervation of the primary auditory neurons of the Johnston organ (JO). This innervation is believed to be involved in the efferent control of hearing [ 75 , 76 ], and several types of 5-HT receptors (5-HT 1 , 5-HT 2 , and 5-HT 7 ) are expressed there [ 58 ]. Thoracically injected 5-HT caused an increase in the mechanical tuning frequency of the JO, reversed by the injection of methiothepin [ 58 ].…”

Section: Discussionmentioning

confidence: 99%

Monoaminergic Systems in Flight-Induced Potentiation of Phonotactic Behavior in Female Crickets Gryllus bimaculatus

Mezheritskiy,

Melnikova,

Dyakonova

et al. 2024

Insects

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We have recently shown that experience of flight remarkably enhanced subsequent terrestrial phonotaxis in females in response to the male calling song. Here, we elucidated the possible roles of octopamine and serotonin in the enhancing effect of flying on phonotactic behavior. Octopamine is known to be released into the hemolymph during flight in insects; however, the octopamine receptor antagonist epinastine did not abolish the effects of flight in our study. On the contrary, the drug significantly potentiated the influence of flying on phonotactic behavior. The octopamine receptor agonist chlordimeform, at a concentration of 2 mM, which was previously found to activate aggression in crickets, dramatically reduced the phonotactic response. However, at a 10-times-lower dose, chlordimeform produced a light but significant decrease in the time that females took to reach the source of the calling song. A similar effect was produced by octopamine itself, which hardly passes the blood–brain barrier in insects. The effect of flight was completely abolished in female crickets treated with alpha-methyl tryptophan (AMTP). AMPT suppresses the synthesis of serotonin, decreasing its content in the nervous systems of insects, including crickets. An activation of the serotonin synthesis with 5-hydroxytryptophan mimicked the effect of flight by increasing the number of visits to and the time spent in the zone near the source of the calling song. The 5-HT content in the third thoracic ganglion was significantly higher in flyers compared to the control group. In contrast, no changes in the octopamine level were observed in the third thoracic ganglion, which is known to play a crucial role in decision-making involved in intraspecific interactions. Therefore, the results suggest that although octopamine is known to be released into the hemolymph during flight, it is likely to inhibit rather than activate the central mechanisms related to phonotaxis. The weak facilitating effect of a low dose of chlordimeform can be attributed to the activation of peripheral octopaminergic receptors. Our results suggest that the serotoninergic system may contribute to the facilitation of female phonotactic behavior by flying. We suggest that both flying and serotonin enhance sexual motivation in females and, by these means, impact their behavioral response to the male calling song.

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Section: Discussionmentioning

confidence: 99%

Monoaminergic Systems in Flight-Induced Potentiation of Phonotactic Behavior in Female Crickets Gryllus bimaculatus

Mezheritskiy,

Melnikova,

Dyakonova

et al. 2024

Insects

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“…It is highly expressed in many brain regions, including the primary olfactory center, the antennal lobe (AL) ( Okada et al, 2009 ), the optic lobe ( Raghu et al, 2013 ), the mushroom bodies (MBs) ( Yasuyama et al, 2002 )—a site involved in learning and memory ( Heisenberg et al, 1985 ; Davis, 1993 ), and the central complex ( Enell et al, 2007 ). Accordingly, GABA is involved in many different sensory behaviors, including the processing of odors ( Waldrop et al, 1987 ; Stopfer et al, 1997 ; Olsen and Wilson, 2008 ) and visual ( Brotz et al, 2001 ; Freifeld et al, 2013 ) and auditory stimuli ( Loh et al, 2023 ). The neuronal circuits and behaviors associated with learning and memory are also modulated by GABA, with GABAergic processes that broadly innervate the MBs ( Liu and Davis, 2009 ).…”

Section: Introductionmentioning

confidence: 99%

“…Despite the importance of GABA in mosquitoes, only a handful of studies have examined GABA expression in the mosquito brain ( Lahondère et al, 2020 ; Loh et al, 2023 ; Singh et al, 2023 ), and none have examined GABA-receptor expression. In particular, the GABA-B1-receptors are involved in many vital physiological processes and constitutes a promising pharmacological target in insecticide development where resistance problems targeting GABA A receptor subunit are now observed ( Zulfa et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Transgenic line for characterizing GABA-receptor expression to study the neural basis of olfaction in the yellow-fever mosquito

Rouyar,

Patil,

Leon-Noreña

et al. 2024

Front. Physiol.

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The mosquito Aedes aegypti is an important vector of diseases including dengue, Zika, chikungunya, and yellow fever. Olfaction is a critical modality for mosquitoes enabling them to locate hosts, sources of nectar, and sites for oviposition. GABA is an essential neurotransmitter in olfactory processing in the insect brain, including the primary olfactory center, the antennal lobe. Previous work with Ae. aegypti has suggested that antennal lobe inhibition via GABA may be involved in the processing of odors. However, little is known about GABA receptor expression in the mosquito brain, or how they may be involved in odor attraction. In this context, generating mutants that target the mosquito’s olfactory responses, and particularly the GABAergic system, is essential to achieve a better understanding of these diverse processes and olfactory coding in these disease vectors. Here we demonstrate the potential of a transgenic line using the QF2 transcription factor, GABA-B1QF2−ECFP, as a new neurogenetic tool to investigate the neural basis of olfaction in Ae. aegypti. Our results show that the gene insertion has a moderate impact on mosquito fitness. Moreover, the line presented here was crossed with a QUAS reporter line expressing the green fluorescent protein and used to determine the location of the metabotropic GABA-B1 receptor expression. We find high receptor expression in the antennal lobes, especially the cell bodies surrounding the antennal lobes. In the mushroom bodies, receptor expression was high in the Kenyon cells, but had low expression in the mushroom body lobes. Behavioral experiments testing the fruit odor attractants showed that the mutants lost their behavioral attraction. Together, these results show that the GABA-B1QF2−ECFP line provides a new tool to characterize GABAergic systems in the mosquito nervous system.

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Section: Introductionmentioning

confidence: 99%

“…Despite the extensive GABAergic innervation of the mosquito auditory nerve (4,5), GABA’s role in audition has not been studied in detail. It has been shown that GABA is released from type I efferent terminals in the auditory nerve of Culex quinquefasciatus mosquitoes (4,5), where it modulates the mechanical frequency tuning and nerve responses. We recently reported the transcriptome of the Anopheles gambiae ear (12), and found a number of GABA receptors expressed, including ionotropic (GABA A ) and metabotropic (GABA B ) receptors.…”

Section: Introductionmentioning

confidence: 99%

The GABAA receptor RDL modulates the auditory sensitivity of malaria mosquitoes.

Ellis,

Alampounti,

Suppermpool

et al. 2024

Preprint

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Malaria mosquitoes mate in crowded, and noisy, swarms. A vital stage of their precopulatory behaviour involves detecting the faint flight tone of a mating partner amidst the noise from hundreds of other mosquitoes. This exquisite sensory performance is enabled by a complex auditory system with remarkable features. One such feature is their vast efferent control system, which provides the mosquito ear with the required plasticity to adapt to various external and internal changes. In this paper, we study the auditory role of GABA, one of the main efferent signalling molecules in the mosquito ear, and its interactions with octopamine, another neurotransmitter of the efferent network. We show that GABA is released in the malaria mosquito auditory nerve and that GABA receptors are expressed in the ear, including the GABAA receptor Resistance to Dieldrin (RDL), a target for the evolution of insecticide resistance. Using picrotoxin to antagonize RDL receptors, we discovered multiple auditory effects of GABA at the mechanical and electrical level. At the mechanical level, blocking RDL promotes the erection of antennal fibrillae and the cessation of flagellar self-sustained oscillations. These effects are not observed in knockouts of the octopamine receptor AgOctbeta2, suggesting that RDL auditory mechanical effects are mediated through octopamine release in the mosquito ear. Electrically, picrotoxin injection increases the spontaneous firing of auditory neurons and direct current (DC) responses of the nerve to mechanical stimulation both in wildtype and AgOctbeta2 mutants, indicating that RDL may also modulate auditory sensitivity via octopamine-independent pathways. In summary, our experiments uncover distinct auditory roles of GABA, as well as synergistic roles with octopamine. The data show a fundamental role of RDL in controlling the auditory function of malaria mosquitoes and implicate RDL signalling in mating of natural malaria mosquito populations.

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The auditory efferent system in mosquitoes

Cited by 16 publications

References 115 publications

Monoaminergic Systems in Flight-Induced Potentiation of Phonotactic Behavior in Female Crickets Gryllus bimaculatus

Monoaminergic Systems in Flight-Induced Potentiation of Phonotactic Behavior in Female Crickets Gryllus bimaculatus

Transgenic line for characterizing GABA-receptor expression to study the neural basis of olfaction in the yellow-fever mosquito

The GABAA receptor RDL modulates the auditory sensitivity of malaria mosquitoes.

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