Network Degeneracy and the Dynamics of Task Switching in the Feeding Circuit inAplysia

Abstract

The characteristics of a network are determined by parameters that describe the intrinsic properties of the component neurons and their synapses. Degeneracy occurs when more than one set of parameters produces the same (or very similar) output. It is not clear whether network degeneracy impacts network function or is simply a reflection of the fact that, although it is important for a network to be able to generate a particular output, it is not important how this is achieved. We address this issue in the feeding network of the mollusc Aplysia In this system, there are two stimulation paradigms that generate egestive motor programs: repetition priming and positive biasing. We demonstrate that circuit parameters differ in the 2 cases (e.g., egestive repetition priming requires activity in an interneuron, B20, which is not essential for positive biasing). We show that degeneracy has consequences for task switching. If egestive repetition priming is immediately followed by stimulation of an ingestive input to the feeding central pattern generator, the first few cycles of activity are egestive (not ingestive). In this situation, there is a task switch cost. This "cost" is in part due to the potentiating effect of egestive repetition priming on B20. In contrast, there is no switch cost after positive biasing. Stimulation of the ingestive central pattern generator input immediately triggers ingestive activity. Our results indicate that the mechanisms used to pattern activity can impact network function in that they can determine how readily a network can switch from one configuration to another.SIGNIFICANCE STATEMENT A particular pattern of neural activity can be generated by more than one set of circuit parameters. How or whether this impacts network function is unclear. We address this issue in the feeding network of Aplysia and demonstrate that degeneracy in network function can have consequences for task switching. Namely, we show that, when egestive activity is generated via one set of circuit modifications, an immediate switch to ingestive activity is not possible. In contrast, rapid transitions to ingestive activity are possible if egestive activity is generated via a different set of circuit modifications.