Neural circuit architecture and directional information processing of airflow stimuli in the cricket brain

Animals process spatial information of external stimuli and exhibit goal-directed behaviors based on this information. However, the neural circuits that link sensory inputs to motor outputs for directional control remain poorly understood. To clarify the entire picture of sensory-motor association underlying the goal-directed behavior, we examined the central nervous system of crickets, which exhibit wind-elicited escape behaviors. Crickets exhibit directed escape movements in response to a short air puff, moving precisely in the opposite direction to the stimulus. Directional control in escape behavior requires descending signals from the brain to the thoracic ganglia that include a motor center for the legs in insects. To clarify the brain neural circuit involved in directed escape behavior, we examined the firing activities of brain interneurons evoked by airflow stimuli applied from various directions by using intracellular recordings. Based on the morphology of the recorded cells, the wind-sensitive interneurons were classified into three types: ascending neurons (ANs, N = 27), local interneurons (LIs, N = 42), and descending neurons (DNs, N = 23). The ANs showed short-latency responses and directional preference toward the side ipsilateral to their ascending axon. LIs exhibited morphological diversity and variable directional tuning. DNs responded with longer latencies and displayed diverse directional preferences. Several DNs had dendritic arborizations in the lateral accessory lobe and showed strong directional selectivity. This study reveals the morphologies and response properties of brain interneurons that link mechanosensory processing to directional motor output, thereby contributing to a deeper understanding of the neural basis underlying goal-directed behaviors.NEW & NOTEWORTHY Although several cricket brain neurons have been well-studied for their morphology and sensory responses, no comprehensive research has quantitatively measured their response properties to airflow stimuli at the single-cell level. The present electrophysiological study of nearly 100 neurons significantly advances our understanding of the sensorimotor coupling that integrates spatial processing of stimulus source information with goal-directed movements, addressing a key issue in neuroscience.