Neural Analog of Arousal: Persistent Conditional Activation of a Feeding Modulator by Serotonergic Initiators of Locomotion

Abstract

We investigated how a neural analog of a form of arousal induced by a mildly noxious stimulus can promote two antagonistic responses, locomotion and feeding. Two pairs of cerebral serotonergic interneurons in Aplysia, CC9 and CC10, were persistently activated by transient noxious stimuli. Direct stimulation of CC9 -10 activated locomotor activity that outlasted the stimulation and enhanced subsequent nerve-evoked locomotor programs. Thus, CC9 -10 function both as initiators and as modulators of the locomotor network. CC9 -10 also interacted with the feeding circuit but in a fundamentally different manner. CC9 -10 did not directly trigger feeding activity or activate feeding command or pattern generating interneurons. CC9 -10 did, however, elicit slow EPSPs in serotonergic cells that modulate feeding responses, the metacerebral cells (MCCs). CC9 -10 persistently enhanced MCC excitability, but did not activate the MCCs directly. Previous work has demonstrated that the MCCs are activated during food ingestion via a sensory neuron C2. Interestingly, we found that CC9 -10 stimulation converted subthreshold C2 mediated excitation of the MCC into suprathreshold excitation. Transient noxious stimuli also enhanced MCC excitability, and this was largely mediated by CC9 -10. To summarize, CC9 -10 exert actions on the feeding network, but their functional effects appear to be conditional on the presence of food-related inputs to the MCCs. A potential advantage of this arrangement is that it may prevent conflicting responses from being directly evoked by noxious stimuli while also facilitating the ability of food-related stimuli to generate feeding responses in the aftermath of noxious stimulation.

Gastric and pyloric motor pattern control by a modulatory projection neuron in the intact crabCancer pagurus

“…While the CBIs release different types of neuromodulators, their common feature is that these neurons are not spontaneously active, but rather are only activated by external stimuli (such as food). The same is true for the C-PR neuron and the serotonergic CC9/10 neurons, which are activated by food stimuli and influence locomotion (Teyke et al , 1997Jing et al 2008). …”

Evolving Concepts of Arousal: Insights from Simple Model Systems

“…The serotonergic arousal system of gastropods appears to be highly conserved across the class Gastropoda (cf. 730, 33,54,56,114,1467) (see below), and, indeed, may be recognizable in both form and function in other molluscs like the cephalopods. A basic reason, we argue, is that evolutionary changes in the nervous system are basically more conservative than those that occur in the periphery, and that natural selection tends to operate more drastically on the periphery than on the basic structure of the CNS.…”

Characterization of GdFFD, a d-Amino Acid-containing Neuropeptide That Functions as an Extrinsic Modulator of the Aplysia Feeding Circuit

“…apNPY, SCP, and FRF-amide/FMRF-amide, that promote egestive programs and may serve to interrupt ingestion of food when animals become satiated. Although we do not yet know under what circumstances GdFFD-positive neurons would be activated, it is attractive to speculate that GdFFD may function to interrupt ingestion when locomotion is active because the pedal ganglion is involved in the control of locomotion (83). In this sense, in contrast to the actions of intrinsic modulators apNPY and SCP, the extrinsic modulator GdFFD might provide a new context in which a modulator may bias the feeding programs toward egestion in the Aplysia feeding system (41,47).…”