Opposing aminergic modulation of distinct spinal locomotor circuits and their functional coupling during amphibian metamorphosis.
The biogenic amines serotonin (5-HT) and noradrenaline (NA) are well known modulators of central pattern-generating networks responsible for vertebrate locomotion. Here we have explored monoaminergic modulation of the spinal circuits that generate two distinct modes of locomotion in the metamorphosing frog Xenopus laevis. At metamorphic climax when propulsion is achieved by undulatory larval tail movements and/or by kicking of the newly developed adult hindlimbs, the underlying motor networks remain spontaneously active in vitro, producing either separate fast axial and slow appendicular rhythms or a single combined rhythm that drives coordinated tail-based and limb-based swimming in vivo. In isolated spinal cords already expressing distinct axial and limb rhythms, bath-applied 5-HT induced coupled network activity through an opposite slowing of axial rhythmicity (by increasing motoneuron burst and cycle durations) and an acceleration of limb rhythmicity (by decreasing burst and cycle durations). In contrast, in preparations spontaneously expressing coordinated fictive locomotion, exogenous NA caused a dissociation of spinal activity into separate faster axial and slower appendicular rhythms by decreasing and increasing burst and cycle durations, respectively. Moreover, in preparations from premetamorphic and postmetamorphic animals that express exclusively axial-based or limb-based locomotion, 5-HT and NA modified the developmentally independent rhythms in a similar manner to the amines' opposing effects on the coexisting circuits at metamorphic climax. Thus, by exerting differential modulatory actions on one network that are opposite to their influences on a second adjacent circuit, these two amines are able to precisely regulate the functional relationship between different rhythmogenic networks in a developing vertebrate's spinal cord.
Rauscent
Aude
A
Université de Bordeaux, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5227, 33076 Bordeaux, France.
Einum
James
J
Le Ray
Didier
D
Simmers
John
J
Combes
Denis
D
D000818:Animals; D001522:Behavior, Animal; D001933:Brain Stem / Q000187:drug effects / Q000254:growth & development; D066298:In Vitro Techniques; D008124:Locomotion / Q000187:drug effects* / Q000502:physiology; D008675:Metamorphosis, Biological / Q000187:drug effects* / Q000502:physiology; D009415:Nerve Net / Q000187:drug effects* / Q000502:physiology; D009638:Norepinephrine / Q000494:pharmacology*; D012701:Serotonin / Q000494:pharmacology*; D013116:Spinal Cord / Q000187:drug effects* / Q000254:growth & development; D014982:Xenopus laevis / Q000033:anatomy & histology / Q000502:physiology*
D012701:Serotonin; D009638:Norepinephrine