ABSTRACT Non‐spiking neurons use graded potentials for processing neural information, unlike spiking neurons. These non‐spiking neurons struggle to transmit signals distally due to membrane potential decay. Consequently, they possibly perform unique computations different from spiking neurons by using local processing with graded potential. Invertebrates, such as insects, possess both non‐spiking and spiking neurons in their central nervous system. However, how the subcellular local regions in non‐spiking neurons process sensory information remains unclear. We examined intracellular Ca 2+ dynamics in the wind‐sensitive non‐spiking neurons of crickets. Directional information about airflow is processed by a local circuit within the terminal abdominal ganglion, where several identified non‐spiking interneurons are involved. In this study, we measured the membrane potential and Ca 2+ responses to airflow from different angles in three local non‐spiking interneurons. These neurons exhibited spatial heterogeneities in their Ca 2+ responses. In two non‐spiking interneurons, the similarity in the time course of Ca 2+ responses between subcellular regions decreased with increasing intracellular distance. However, the similarity in directional selectivity was not always linked to the intracellular distance. In addition, the Ca 2+ signals induced by current injection did not necessarily couple with the membrane potential changes. The temporal dynamics of Ca 2+ signals were possibly influenced by partially uneven electrical propagation, and their directional selectivity, primarily determined by the spatial presynaptic arrangement, might depend less on intracellular distance. Therefore, local non‐spiking interneurons likely perform local processing affected by both presynaptic and postsynaptic factors, enabling a single neuron to substitute for functions otherwise distributed across multiple spiking neurons.