Multisensory enhancement of burst activity in an insect auditory neuron

Abstract

Detecting predators is crucial for survival. In insects, a few sensory interneurons receiving sensory input from a distinct receptive organ extract specific features informing the animal about approaching predators and mediate avoidance behaviors. Although integration of multiple sensory cues relevant to the predator enhances sensitivity and precision, it has not been established whether the sensory interneurons that act as predator detectors integrate multiple modalities of sensory inputs elicited by predators. Using intracellular recording techniques, we found that the cricket auditory neuron AN2, which is sensitive to the ultrasound-like echolocation calls of bats, responds to airflow stimuli transduced by the cercal organ, a mechanoreceptor in the abdomen. AN2 enhanced spike outputs in response to cross-modal stimuli combining sound with airflow, and the linearity of the summation of multisensory integration depended on the magnitude of the evoked response. The enhanced AN2 activity contained bursts, triggering avoidance behavior. Moreover, cross-modal stimuli elicited larger and longer lasting excitatory postsynaptic potentials (EPSP) than unimodal stimuli, which would result from a sublinear summation of EPSPs evoked respectively by sound or airflow. The persistence of EPSPs was correlated with the occurrence and structure of burst activity. Our findings indicate that AN2 integrates bimodal signals and that multisensory integration rather than unimodal stimulation alone more reliably generates bursting activity. NEW & NOTEWORTHY Crickets detect ultrasound with their tympanum and airflow with their cercal organ and process them as alert signals of predators. These sensory signals are integrated by auditory neuron AN2 in the early stages of sensory processing. Multisensory inputs from different sensory channels enhanced excitatory postsynaptic potentials to facilitate burst firing, which could trigger avoidance steering in flying crickets. Our results highlight the cellular basis of multisensory integration in AN2 and possible effects on escape behavior.