Electrical synapses in the neural network of insects found to have unexpected role in controlling flight power

A team of experimental neurobiologists at Johannes Gutenberg University Mainz (JGU) and theoretical biologists at Humboldt-Universität zu Berlin has managed to solve a mystery that has been baffling scientists for decades. They have been able to determine the nature of the electrical activity in the nervous system of insects that controls their flight. In a paper recently published in Nature, they report on a previously unknown function of electrical synapses employed by fruit flies during flight.

The fruit fly Drosophila melanogaster beats its wings around 200 times per second in order to move forward. Other small insects manage even 1,000 wingbeats per second. It is this high frequency of wingbeats that generates the annoying high-pitched buzzing sound we commonly associate with mosquitoes. Every insect has to beat its wings at a certain frequency to not get “stuck” in the air, which acts as a viscous medium due to their small body size. For this purpose, they employ a clever strategy that is widely used in the insect world. This involves reciprocal stretch activation of the antagonistic muscles that raise and depress the wings. The system can oscillate at high frequencies, thus producing the high rate of wingbeats required for propulsion. The motor neurons are unable to keep pace with the speed of the wings so that each neuron generates an electrical pulse that controls the wing muscles only about every 20th wingbeat. These pulses are precisely coordinated with the activity of other neurons. Special activity patterns are generated in the motor neurons that regulate the wingbeat frequency. Each neuron fires at a regular rate but not at the same time as the other neurons. There are fixed intervals between which each of them fires. While it has been known since the 1970s that neural activity patterns of this kind occur in the fruit fly, there was no explanation of the underlying controlling mechanism.

Neural circuit regulates insect flight

Collaborating in the RobustCircuit Research Unit 5289 funded by the German Research Foundation, researchers at Johannes Gutenberg University Mainz and Humboldt-Universität zu Berlin have finally managed to find the solution to the puzzle. "Wing movement in the fruit fly Drosophila melanogaster is governed by a miniaturized circuit solution that comprises only a very few neurons and synapses," explained Professor Carsten Duch of JGU's Faculty of Biology. And it is extremely probable that this is not just the case in the fruit fly. The researchers presume that the more than 600,000 known species of insects that rely on a similar method of propulsion also employ a neural circuit of this kind.

Drosophila melanogaster is the ideal subject for research in the field of neurobiology as it is possible to genetically manipulate the various components of its neural circuit. Individual synapses can be switched on and off and even the activity of individual neurons can be directly influenced, to name just two examples. In this case, the researchers used a combination of these genetic tools to measure the activity and electrical properties of the neurons in the circuit. Thus they were able to identify all the cells and synaptic interactions of the neural circuit that are involved in the generation of flight patterns. As a result, they found that the neural network regulating flight is composed of just a small number of neurons that communicate with each other through electrical synapses only.

New concepts of information processing by the central nervous system

It had previously been assumed that when one neuron fired, inhibitory neurotransmitter substances were released between neurons of the flight network, thus preventing these from firing at the same time. Using experimentation and mathematical modeling, the researchers have been able to show that such a sequential distribution of pulse generation can also occur when neural activity is directly controlled electrically, without the presence of neurotransmitters. The neurons then create a special kind of pulse and 'listen' closely to each other, especially if they have just been active.

Mathematical analyses predicted that this would not be possible with "normal" pulses. Hence, it would appear unlikely that transmission between neurons in a purely electrical form would result in this sequenced firing pattern. In order to test this theoretical hypothesis experimentally, certain ion channels in the neurons of the network were manipulated. As expected, the activity pattern of the flight circuit became synchronized – just as the mathematical model had predicted. This experimental manipulation caused significant variations in the power generated during flight. It is thus apparent that the desynchronization of the activity pattern determined by the electrical synapses of the neural circuit is necessary to ensure that the flight muscles are able to generate a consistent power output.

The findings of the team based in Mainz and Berlin are particularly surprising given that it was previously thought that interconnections by electrical synapses actually result in a synchronized activity of neurons. The activity pattern generated by the electrical synapses detected here indicates that there may well be forms of information processing by the nervous system that are as yet unexplained. The same mechanism may not only play a role in thousands of other insect species but also in the human brain, where the purpose of electrical synapses is still not fully understood.

Related links:

• https://idn.biologie.uni-mainz.de/ – JGU Institute of Developmental Biology and Neurobiology (IDN)
• https://www.crc1080.com/ – DFG-funded Collaborative Research Center 1080: Neural Homeostasis
• https://robustcircuit.flygen.org/ – DFG-funded Research Unit 5289: RobustCircuit

Read more:

• https://press.uni-mainz.de/mechanisms-to-separately-regulate-synaptic-vesicle-release-and-recycling/ – press release "Mechanisms to separately regulate synaptic vesicle release and recycling" (19 July 2021)
• https://press.uni-mainz.de/synapses-compete-for-neuronal-building-blocks/ – press release "Synapses compete for neuronal building blocks" (9 Feb. 2017)
• https://press.uni-mainz.de/fruit-fly-motoneuron-dendrites-are-not-essential-for-basic-functions/ – press release "Fruit fly motoneuron dendrites are not essential for basic functions" (22 Jan. 2015)