Newswise — A group of neurobiologists at Johannes Gutenberg University Mainz (JGU) and theoretical biologists at Humboldt-Universität zu Berlin has successfully unraveled a long-standing enigma that has puzzled researchers for many years. They have unveiled the essence of the electrical signals governing the flight behavior of insects. In a recent publication in Nature, they disclose an unexplored role of electrical synapses utilized by fruit flies while in flight.

The fruit fly Drosophila melanogaster, known for its rapid wing movements, beats its wings around 200 times per second, while other small insects can manage an astonishing 1,000 wingbeats per second. This high frequency of wingbeats is responsible for the familiar annoying high-pitched buzzing sound associated with mosquitoes. Insects must maintain a specific wingbeat frequency to navigate through the air, which behaves like a thick fluid due to their small size. To achieve this, they employ a clever strategy widely employed in the insect world. This strategy involves the reciprocal stretch activation of antagonistic muscles responsible for raising and depressing the wings. By utilizing this mechanism, the insects can oscillate their wings at high frequencies, generating the propulsion required for flight. However, the motor neurons controlling the wing muscles cannot keep up with the rapid wing movements. As a result, each neuron produces an electrical pulse that controls the wing muscles only approximately every 20th wingbeat, coordinating its activity precisely with other neurons. These motor neurons generate specific activity patterns that regulate the wingbeat frequency. While it has been observed since the 1970s that fruit flies exhibit such neural activity patterns, the exact mechanism underlying this control remained unexplained.

Neural circuit regulates insect flight

Under the collaboration of the RobustCircuit Research Unit 5289, which received funding from the German Research Foundation (DFG), researchers from Johannes Gutenberg University Mainz and Humboldt-Universität zu Berlin have made a significant breakthrough. They have successfully unraveled the mystery surrounding wing movement in the fruit fly Drosophila melanogaster. Professor Carsten Duch from JGU's Faculty of Biology explained that they discovered a remarkably efficient solution in the form of a miniaturized neural circuit involving only a few neurons and synapses. This finding is not limited to fruit flies alone; the researchers strongly believe that this neural circuitry is prevalent among the vast array of over 600,000 known insect species that rely on a similar propulsion method.

Due to its genetic manipulability, Drosophila melanogaster serves as an excellent model organism for studying neurobiology. Researchers have the ability to manipulate the various components of its neural circuitry, including individual synapses and even the activity of specific neurons. This level of control enables them to directly influence and investigate the functioning of the neural circuit. In the study at hand, the researchers utilized a combination of genetic tools to assess the activity and electrical properties of the neurons within the circuit. Through this approach, they were able to identify all the cells and synaptic interactions involved in generating flight patterns. Remarkably, the findings revealed that the neural network responsible for regulating flight behavior comprises only a small number of neurons that communicate with each other solely through electrical synapses.

New concepts of information processing by the central nervous system

Prior to this study, the prevailing assumption was that inhibitory neurotransmitter substances were responsible for preventing simultaneous firing of neurons within the flight network. It was believed that when one neuron fired, it released inhibitory neurotransmitters, which inhibited the firing of other neurons. However, through a combination of experimentation and mathematical modeling, the researchers have made a fascinating discovery. They found that a sequential distribution of pulse generation can occur even in the absence of neurotransmitters when neural activity is directly controlled electrically. In this scenario, the neurons generate a unique type of pulse and closely "listen" to each other, particularly if they have recently been active. This finding challenges the previous notion and sheds new light on the intricate mechanisms underlying the coordination of neural activity within the flight network.

According to mathematical analyses, it was initially believed that achieving a sequential firing pattern solely through electrical transmission of "normal" pulses would be unlikely. To experimentally test this theoretical hypothesis, the researchers manipulated specific ion channels within the neurons of the flight network. As anticipated, the manipulation led to synchronization of the activity pattern in the flight circuit, aligning with the predictions of the mathematical model. This experimental manipulation had a significant impact on the power generated during flight, causing notable variations. Consequently, it became evident that maintaining a desynchronized activity pattern, facilitated by the electrical synapses within the neural circuit, is crucial for ensuring consistent power output by the flight muscles. These findings highlight the intricate relationship between the activity pattern of the neural circuit and the efficient generation of power for flight.

The discoveries made by the research team from Mainz and Berlin are highly intriguing, especially considering the prevailing belief that electrical synapses typically lead to synchronized neuronal activity. The observed activity pattern generated by the electrical synapses challenges this notion and suggests the existence of unexplained forms of information processing within the nervous system. These findings have broader implications beyond fruit flies and insect species, as they raise the possibility that similar mechanisms may operate in the human brain. Despite extensive research, the exact purpose and functioning of electrical synapses in the human brain remain incompletely understood. Therefore, these new insights shed light on the complex nature of information processing within neural circuits and hint at the potential for novel discoveries in neuroscience.

Journal Link: Nature