Fast adaptation in invertebrate looming-sensitive descending neurons

Abstract

Motion vision plays a crucial role in guiding dynamic behaviors, such as determining when to escape from predators, pursue prey, navigate obstacles, or adjust flight patterns during migration. Adaptation to repetitive motion stimuli is a crucial aspect of this process, allowing animals to efficiently process new stimuli while avoiding sensory overload. This helps animals remain responsive to novel or important stimuli, ensuring appropriate behavioral reactions. Adaptation to looming stimuli, which often signal an approaching threat through the rapid expansion of an objects image on the retina, allows animals to distinguish harmless from harmful stimuli. While neural adaptation has been extensively studied in the flys optic lobes, less is known about how descending neurons, which link the optic lobes to the motor centers in the thoracic ganglia, adapt. To address this gap, we investigate adaptation in looming-sensitive descending neurons in the hoverfly Eristalis tenax. Using intracellular recordings, we show that these descending neurons adapt to looming stimuli with inter-stimulus intervals of 1-3 s. We show that the level of adaptation depends on the ISI, with shorter intervals leading to greater adaptation. Specifically, we find that adaptation leads to decreased response duration, with a pronounced delayed response onset. We identified descending neurons that responded to looming stimuli either unilaterally or bilaterally and used this to show that most of the adaptation takes place within the neuron itself, rather than its pre-synaptic inputs. Finally, we found that the wing beat amplitude of tethered hoverflies did not appear to adapt to repetitive looming stimuli. Significance StatementRapidly expanding looming objects often signal approaching threats, and appropriate detection is therefore critical for survival across species. Adaptation to repetitive looming cues allows animals to filter out irrelevant information, ensuring they respond only to significant threats. While adaptation has been well studied in the brain, how descending neurons, which connect the brain with the body, adapt to looming stimuli remains poorly understood. Here, we investigate looming-sensitive descending neurons in the hoverfly Eristalis tenax and show that they adapt strongly when looming stimuli are repeated in quick succession. We show that most of the adaptation takes place within the descending neuron itself. Our research establishes a foundation for future exploration of the neural mechanisms underlying behavior in constantly changing environments.