Regulation and Restoration of Motoneuronal Synaptic Transmission During Neuromuscular Regeneration in the Pulmonate Snail Helisoma trivolvis

Abstract

Regeneration of motor systems involves reestablishment of central control networks, reinnervation of muscle targets by motoneurons, and reconnection of neuromodulatory circuits. Still, how these processes are integrated as motor function is restored during regeneration remains ill defined. Here, we examined the mechanisms underlying motoneuronal regeneration of neuromuscular synapses related to feeding movements in the pulmonate snail Helisoma trivolvis. Neurons B19 and B110, although activated during different phases of the feeding pattern, innervate similar sets of muscles. However, the percentage of muscle fibers innervated, the efficacy of excitatory junction potentials, and the strength of muscle contractions were different for each cell’s specific connections. After peripheral nerve crush, a sequence of transient electrical and chemical connections formed centrally within the buccal ganglia. Neuromuscular synapse regeneration involved a three-phase process: the emergence of spontaneous synaptic transmission (P1), the acquisition of evoked potentials of weak efficacy (P2), and the establishment of functional reinnervation (P3). Differential synaptic efficacy at muscle contacts was recapitulated in cell culture. Differences in motoneuronal presynaptic properties (i.e., quantal content) were the basis of disparate neuromuscular synapse function, suggesting a role for retrograde target influences. We propose a homeostatic model of molluscan motor system regeneration. This model has three restoration events: (1) transient central synaptogenesis during axonal outgrowth, (2) intermotoneuronal inhibitory synaptogenesis during initial neuromuscular synapse formation, and (3) target-dependent regulation of neuromuscular junction formation.

Nitric Oxide Regulates Neuronal Activity via Calcium-Activated Potassium Channels

“…Inside the buccal ganglion, motor neuron B19 is active during the hyper-retraction phase (S3) of the feeding motor pattern in Helisoma and activates several muscle groups in the radula [26] , [27] . Physiological release of NO, either through nitrergic neurons projecting into the buccal ganglion, or from neurons located within the ganglion [12] , [50] , are expected to depolarize B19 neurons, resulting in an increase in their firing frequency and membrane excitability.…”

“…Gastropod feeding is driven by central pattern generators [25] , [26] , and NO has been implicated in regulating the feeding motor program [22] – [24] . Buccal neuron B19 in Helisoma is a bilaterally symmetric motor neuron that innervates muscle groups in the radula [26] , [27] . The somata of B19 neurons are located in the vicinity of NO-producing neurons [12] , [28] , suggesting that NO might affect B19 neurons by volume transmission.…”

Anatomical and physiological background permitting spatial odor sensation in stylommatophoran molluscs

“…Most invertebrate muscle fibers, receive synaptic inputs from multiple motoneurons and in addition from modulatory neurons, such that significant motor plasticity can be generated at the periphery [33,42,67,81,91]. Innervation of muscles of different molluscan species is usually reduced to a single naked axon contacting the muscle fiber.…”