Dynamic construction of a neural network from multiple pattern generators in the lobster stomatogastric nervous system.
In the stomatogastric nervous system (STNS) of the lobster Homarus gammarus, the rhythmic discharge of a pair of identified modulatory neurons (PS cells) is able to construct de novo a functional network from neurons otherwise belonging to other functional networks. The PS interneurons are electrically coupled and possess endogenous oscillatory properties that can be activated synaptically by stimulation of an identified sensory pathway. PS neurons themselves project synaptically onto the three major neural networks (esophageal, gastric mill, and pyloric) of the STNS. When a PS is rhythmically active in vitro, either spontaneously (rarely) or in response to direct stimulation, it dramatically restructures the otherwise independent activity patterns of all three target networks. This functional reconfiguration elicited by a single cell does not rely on changes in neuronal allegiance to pre-existing circuits, or on a simple merger of these different circuits. Rather, PS is responsible for the creation of an entirely new motor rhythm in that, via its widespread synaptic connections, the interneuron is able to subjugate the ongoing activity of the three STNS circuits and selectively appropriate individual elements to its own intrinsic rhythm. In addition, PS excites motor neurons that innervate dilator muscles of a valve situated between the esophagus and the stomach. The reorganization of the regional foregut motor rhythms by the interneuron is therefore coordinated to the opening of this valve, which itself carries sensory receptors that have been found to activate bursting in PS. Our data suggest that the role of PS in massively restructuring stomatogastric output is to generate a unique motor pattern appropriate for swallowing-like behavior. In a wider context, moreover, the results demonstrate that a neural network may not exist as a predefined entity within the CNS, but may be dynamically assembled according to changing behavioral circumstances.
Meyrand
P
P
Laboratoire de Neurobiologie et Physiologie Comparées, Université de Bordeaux I, Arcachon, France.
Simmers
J
J
Moulins
M
M
D000818:Animals; D001370:Axonal Transport; D001369:Axons / Q000502:physiology; D004064:Digestive System / Q000294:innervation; D004558:Electric Stimulation; D066298:In Vitro Techniques; D008959:Models, Neurological; D009046:Motor Neurons / Q000502:physiology; D009130:Muscle, Smooth / Q000294:innervation; D008121:Nephropidae; D009415:Nerve Net / Q000502:physiology*; D009420:Nervous System / Q000033:anatomy & histology; D009424:Nervous System Physiological Phenomena; D009474:Neurons / Q000502:physiology*; D009475:Neurons, Afferent / Q000502:physiology