Sites of plasticity in the neural circuit mediating tentacle withdrawal in the snail Helix aspersa: implications for behavioral change and learning kinetics.
The tentacle withdrawal reflex of the snail Helix aspersa exhibits a complex combination of habituation and sensitization consistent with the dual-process theory of plasticity. Habituation, sensitization, or a combination of both were elicited by varying stimulation parameters and lesion condition. Analysis of response plasticity shows that the late phase of the response is selectively enhanced by sensitization, whereas all phases are decreased by habituation. Previous data have shown that tentacle withdrawal is mediated conjointly by parallel monosynaptic and polysynaptic pathways. The former mediates the early phase, whereas the latter mediates the late phase of the response. Plastic loci were identified by stimulating and recording at different points within the neural circuit, in combination with selective lesions. Results indicate that depression occurs at an upstream locus, before circuit divergence, and is therefore expressed in all pathways, whereas facilitation requires downstream facilitatory neurons and is selectively expressed in polysynaptic pathways. Differential expression of plasticity between pathways helps explain the behavioral manifestation of depression and facilitation. A simple mathematical model is used to show how serial positioning of depression and facilitation can explain the kinetics of dual-process learning. These results illustrate how the position of cellular plasticity in the network affects behavioral change and how forms of plasticity can interact to determine the kinetics of the net changes.
Prescott
S A
SA
Department of Biology, McGill University, Montreal, Quebec, Canada.
Chase
R
R
D000818:Animals; D001522:Behavior, Animal / Q000502:physiology; D002490:Central Nervous System / Q000502:physiology; D004558:Electric Stimulation; D015726:Giant Cells / Q000502:physiology; D006372:Helix, Snails / Q000502:physiology*; D007700:Kinetics; D007858:Learning / Q000502:physiology; D009046:Motor Neurons / Q000502:physiology; D009132:Muscles / Q000294:innervation* / Q000502:physiology*; D009434:Neural Pathways / Q000502:physiology; D009473:Neuronal Plasticity / Q000502:physiology*; D009832:Olfactory Nerve / Q000502:physiology; D012018:Reflex / Q000502:physiology*