Identified neurons B4/B5 function as sensory neurons, motor neurons, and interneurons in Aplysia

Adaptive behavior is critical for animals' survival. A multifunctional nervous system is crucial to generate behaviors that respond effectively to the changing environment. Multiple mechanisms behind a multifunctional neural circuit have been found in vertebrate and invertebrate systems: the change in the nervous system can occur at the cellular level, the synaptic level and at the circuitry level. Aplysia's feeding circuit is a multifunctional system capable of producing different modes of behavior. In Aplysia, B4/B5 are two electrically coupled multiaction neurons that have wide inhibitory synaptic outputs to multiple key motor neurons, mediating an important component of rejection behavior. However, B4/B5 also fire at a lower frequency during ingestion, generating a limited inhibitory effect on their synaptic followers. To further understand the role of B4/B5 in different behaviors, we investigated the functions of B4/B5 and their firing patterns in freely feeding animals. As previous studies suggested that B4/B5 have sensory and motor functions, we further characterized the sensory response and the motor effect of B4/B5 and related these functions to different behaviors. We found that B4/B5 receive direct sensory inputs from different receptive fields within the feeding apparatus, and they innervate and alter forces in the retractor muscles and reduce forces induced by a motor neuron (B3) for the retractor muscles. Their sensory signaling may be related to contact with food during ingestion. Studies on the B4/B5 neurons demonstrated how a neural circuit can be influenced by multifunctional neurons, suggesting another way that adaptive behaviors can be generated.NEW & NOTEWORTHY The B4/B5 neurons in Aplysia californica have multiple functions. In this study, we further characterized B4/B5's sensory responses to mechanical stimuli at different locations in the feeding apparatus and identified their direct motor effect on the muscles. The bidirectional signaling of B4/B5, which was also observed in freely feeding animals, suggests that these neurons may play a role in detecting nociceptive or proprioceptive information and regulating the movements that facilitate particular feeding behaviors.