Parallel Peptide Actions Underlie Recruitment and Coordination of a Dual-Network Neuron

Abstract

AbstractOscillatory networks underlying rhythmic motor behaviors, and sensory and complex neural processing, are flexible, even in their neuronal composition. Neuromodulatory inputs elicit neuronal switching, whereby neurons switch participation between networks, or into multiple networks simultaneously. In most examples of neuronal switching, recruitment and coordination occur via the same mechanism, neuromodulation of internetwork synapses. However, separate mechanisms could enable additional flexibility. Here we explored whether modulation of synaptic properties occurs for a neuron recruited into dual-network activity via modulation of intrinsic properties. The isolated stomatogastric nervous system of the crab,Cancer borealis,contains two well-defined feeding-related networks (pyloric, food filtering, ∼1 Hz; gastric mill, food chewing, ∼0.1 Hz). The projection neuron MCN5 uses the neuropeptide Gly1-SIFamide to recruit the typically pyloric-only LPG neuron into dual pyloric plus gastric mill-timed bursting via modulation of LPG intrinsic properties. However, modulation of LPG intrinsic properties is insufficient for coordinating LPG with the gastric mill network, because synapses between LPG and gastric mill neurons are not effective under baseline conditions. Here, we show that LPG and gastric mill neurons IC, LG, and DG entrain each other during Gly1-SIFamide application, indicating bidirectional, functional connectivity. Further, in two-electrode voltage clamp recordings, Gly1-SIFamide enhanced bidirectional graded inhibitory synaptic currents between LPG and LG, IC, and DG. Thus, a neuropeptide that recruits a switching neuron into dual-frequency oscillations also modulates synapses that enable network coordination. These parallel modulatory actions provide the possibility of independent regulation of recruitment and coordination for neuronal switching.Significance StatementNeurons can exhibit activity that is simultaneously coordinated with separate networks. In previous examples where such a neuron was recruited into a second network, the recruitment occurred via modulation of internetwork synapses, which also coordinated activity of the switching neuron with the second network. In an alternative scenario where recruitment occurs via peptidergic modulation of intrinsic ionic currents instead of internetwork synapses, we find that peptidergic modulation of synapses between the recruited neuron and members of the second network also occurs for coordination of the switching neuron with the second network activity pattern. Thus, we determine that recruiting a neuron into a second network and coordinating its activity with the new network can occur via independent modulatory actions.