An anticipatory circuit modification that modifies subsequent task switching

Abstract

Modulators are generally expected to establish a network configuration that is appropriate for the current circumstances. We characterize a situation where the opposite is apparently observed. A network effect of a peptide modulator is counterproductive in that it tends to impede rather than promote the creation of the configuration that is appropriate when the modulator is released. This raises a question, why does release occur? We present data that strongly suggest that it impacts task switching. Our experiments were conducted in an Aplysia feeding network that generates egestive and ingestive motor programs. Initial experiments focused on egestive activity and the neuron B8. As activity becomes egestive there is an increase in synaptic drive to B8 and its firing frequency increases (Wang et al., 2019). We show that as this occurs there is also a persistent current that develops in B8 that is outward rather than inward. Dynamic clamp introduction of this current decreases excitability. When there is an egestive-ingestive task switch in Aplysia negative biasing is observed, i.e., a bout of egestive activity has a negative impact on a subsequent attempt to initiate an ingestive response (Proekt et al., 2004). Using an in vitro analog of negative biasing we demonstrate that the outward current that develops during egestive priming plays an important role in establishing this phenomenon. Our data suggest that although the outward current induced as activity becomes egestive is counterproductive at the time; it plays an anticipatory role in that it subsequently impacts task switching.

SIGNIFICANCE STATEMENT:

In this study we identify a peptide-induced circuit modification (induction of an outward current) that does not immediately promote the establishment of a behaviorally appropriate network configuration. We ask why this might occur, and present data that strongly suggest that it plays an important role during task switching. Specifically, our data suggest that the outward current we characterize plays a role in the negative biasing that is seen in the mollusc Aplysia when there is a transition from egestive to ingestive activity. It is possible that the mechanism that we describe operates in other species. A negative effect of egestion on subsequent ingestion is observed throughout the animal kingdom.