Neural analog of arousal: persistent conditional activation of a feeding modulator by serotonergic initiators of locomotion.
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.
Jing
Jian
J
Department of Neuroscience, Mount Sinai School of Medicine, New York, New York 10029, USA. jingj01@gmail.com
Vilim
Ferdinand S
FS
Cropper
Elizabeth C
EC
Weiss
Klaudiusz R
KR
D000200:Action Potentials / Q000502:physiology / Q000528:radiation effects; D000818:Animals; D001048:Aplysia; D001143:Arousal / Q000502:physiology*; D001522:Behavior, Animal; D002540:Cerebral Cortex / Q000166:cytology; D019706:Excitatory Postsynaptic Potentials / Q000502:physiology / Q000528:radiation effects; D005247:Feeding Behavior / Q000523:psychology*; D017952:Ganglia, Invertebrate / Q000166:cytology; D066298:In Vitro Techniques; D053444:Inhibitory Postsynaptic Potentials / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D008124:Locomotion / Q000502:physiology*; D008297:Male; D009415:Nerve Net / Q000166:cytology / Q000502:physiology; D009474:Neurons / Q000187:drug effects / Q000502:physiology* / Q000528:radiation effects; D018408:Patch-Clamp Techniques / Q000379:methods; D010812:Physical Stimulation / Q000009:adverse effects; D051381:Rats; D017207:Rats, Sprague-Dawley; D012701:Serotonin / Q000378:metabolism*
D012701:Serotonin