Latent Modulation: A Basis for Non-Disruptive Promotion of Two Incompatible Behaviors by a Single Network State

Abstract

Behavioral states often preferentially enhance specific classes of behavior and suppress incompatible behaviors. In the nervous system, this may involve upregulation of the efficacy of neural modules that mediate responses to one stimulus and suppression of modules that generate antagonistic or incompatible responses to another stimulus. In Aplysia, prestimulation of egestive inputs [esophageal nerve (EN)] facilitates subsequent EN-elicited egestive responses and weakens ingestive responses to ingestive inputs [Cerebral-Buccal Interneuron (CBI-2)]. However, a single state can also promote incompatible behaviors in response to different stimuli. This is the case in Aplysia, where prestimulation of CBI-2 inputs not only enhances subsequent CBI-2-elicited ingestive responses, but also strengthens EN-elicited egestive responses. We used the modularly organized feeding network of Aplysia to characterize the organizational principles that allow a single network state to promote two opposing behaviors, ingestion and egestion, without the two interfering with each other. We found that the CBI-2 prestimulation-induced state upregulates the excitability of neuron B65 which, as a member of the egestive module, increases the strength of egestive responses. Furthermore,we found that this upregulation is likely mediated by the actions of the neuropeptides FCAP (Feeding Circuit Activating Peptide) and CP2 (Cerebral Peptide 2). This increased excitability is mediated by a form of modulation that we refer to as “latent modulation” because it is established during stimulation of CBI-2, which does not activate B65. However, when B65 is recruited into EN-elicited egestive responses, the effects of the latent modulation are expressed as a higher B65 firing rate and a resultant strengthening of the egestive response.

Memory of recent oxygen experience switches pheromone valence in Caenorhabditis elegans

“…This arrangement suggests that information can be integrated across the circuit (36 We see parallels between our observations and a Drosophila study showing that repeated presentation of an aversive shadow cue leads to a persistent change in behavioral state that scales with the number and frequency of the presentations (55,56). Our findings are also reminiscent of "latent modulation" in the feeding network of Aplysia, where the history of activation in some circuit elements has a lasting effect on subsequent responses, most likely by changing neuronal excitability through peptidergic modulation (57,58).…”

Consequences of degeneracy in network function

“…A second method of inducing egestive activity involves a switch to EN stimulation after repeated stimulation of the ingestive input to the feeding CPG [48]**. A priori it might be expected that the induction of ingestive activity would either negatively impact the subsequent generation of egestive activity, or that it would have no effect.…”

“…A priori it might be expected that the induction of ingestive activity would either negatively impact the subsequent generation of egestive activity, or that it would have no effect. Surprisingly there is a ‘positive’ effect [48]**. Thus, if the EN is stimulated after ingestive repetition priming, fully egestive motor programs are immediately triggered (repeated EN stimulation is not necessary) [48,49]**.…”

“…Surprisingly there is a ‘positive’ effect [48]**. Thus, if the EN is stimulated after ingestive repetition priming, fully egestive motor programs are immediately triggered (repeated EN stimulation is not necessary) [48,49]**. This has been referred to as ‘positive biasing’.…”

“…Positive biasing induces persistent increases in the excitability of the egestive interneuron B65 (Fig. 2A1 left ) [48,50]. In contrast, during egestive repetition priming there is a persistent increase in the excitability of a second egestive interneuron (B20) [51–53], and use dependent potentiation of synaptic transmission between B20 and follower motor neurons (Fig.…”