Modulation of swimming rhythmicity by 5-hydroxytryptamine during post-embryonic development in Xenopus laevis

The maturation and operation of neural networks are known to depend on modulatory neurons. However, whether similar mechanisms may control both adult and developmental plasticity remains poorly investigated. To examine this issue, we have used the lobster stomatogastric nervous system (STNS) to investigate the ontogeny and role of GABAergic modulatory neurons projecting to small pattern generating networks. Using immunocytochemistry, we found that modulatory input neurons to the stomatogastric ganglion (STG) express GABA only after metamorphosis, a time that coincides with the developmental switch from a single to multiple pattern generating networks within the STNS. We demonstrate that blocking GABA synthesis with 3-mercapto-propionic acid within the adult modulatory neurons results in the reconfiguration of the distinct STG networks into a single network that generates a unified embryoniclike motor pattern. Using dye-coupling experiments, we also found that gap-junctional coupling is greater in embryos and GABAdeprived adults exhibiting the unified motor pattern compared with control adults. Furthermore, GABA was found to diminish directly the extent and strength of electrical coupling within adult STG networks. Together, these observations suggest the acquisition of a GABAergic phenotype by modulatory neurons after metamorphosis may induce the reconfiguration of the single embryonic network into multiple adult networks by directly decreasing electrical coupling. The findings also suggest that adult neural networks retain the ability to express typical embryonic characteristics, indicating that network ontogeny can be reversed and that changes in electrical coupling during development may allow the segregation of multiple distinct functional networks from a single large embryonic network.

Section: Neuromodulation and The Development Of Neural Networkmentioning

confidence: 38%

Removal of GABA within Adult Modulatory Systems Alters Electrical Coupling and Allows Expression of an Embryonic-Like Network

Ducret¹,

Feuvre²,

Meyrand³

et al. 2007

“…Such differences between the behavior of identified STG neurons in embryo and in adult could be due to two main reasons. First, neuronal membrane properties may themselves undergo developmental changes as has been demonstrated in other systems (McCobb et al, 1990;Hayashi and Levine, 1992;Sillar et al, 1992b). Alternatively or in parallel, developmental changes in the STNS networks might instead derive from the modifications in the descending inputs that control the adult STNS networks.…”

Section: Discussionmentioning

confidence: 99%

Functional differentiation of adult neural circuits from a single embryonic network

Casasnovas¹,

Meyrand²

1995

The stomatogastric nervous system (STNS) of adult lobsters and crabs generates a number of different rhythmic motor patterns which control different regional movements of the foregut. Since these output patterns are generated by discrete neural networks that, in the adult, are well characterized in terms of synaptic and cellular properties, this system constitutes an ideal model for exploring the mechanisms underlying the ontogeny of neural network organization. The foregut and its rhythmic motor patterns were studied in in vitro STNS nerve-muscle preparations of the embryo and different larval stages of the lobster Homarus gammarus. The development of Homarus comprises a long embryonic stage in ovo followed by three pelagic larval stages prior to the onset of benthic life. During these stages the foregut itself develops slowly from a simple ectodermal invagination that occurs in the embryo. During successive larval stages it progressively acquires all the specialized structures and shape of the adult foregut. In contrast, the STNS is morphologically recognizable at early embryonic stages. In all recorded stages the STNS spontaneously expresses rhythmic motor activity. During development, this activity is progressively restructured, beginning with a single rhythmic motor pattern in the embryo where all the stomodeal muscles are strongly coordinated. In subsequent stages, however, this single pattern is progressively subdivided to give rise eventually to the three discrete rhythmic motor patterns characteristic of the adult STNS. Our data suggest that rather than a dismantling of redundant embryonic and larval neural networks, the different adult networks emerge as a progressive partitioning of discrete circuits from a single embryonic network.

“…Serotonin (5-HT, 10 M) and noradrenaline (NA, 5 M) (Sigma-RBI) were prepared from stock solutions dissolved in distilled water and used at final concentrations that were similar to those used in previous studies on postembryonic Xenopus larvae (Sillar et al, 1992;Fischer et al, 2001;Merrywest et al, 2001;Sillar, 2003, 2004). The saline containing either amine was supplied to the recording chamber at 2-5 ml ⅐ min Ϫ1 , and each application was followed by a replacement with circulating fresh saline for at least 30 min.…”

Section: Methodsmentioning

confidence: 99%

“…In the latter, 5-HT and NA exert opposing modulatory influences on the period and duration of motoneuron bursts that drive swimming (Sillar et al, 1992(Sillar et al, , 1998 because of their differential actions on common synaptic targets within the larval axial network (McDearmid et al, 1997;McLean et al, 2000). We therefore asked whether such opposing aminergic modulation might also serve during later metamorphic development to control the motor output of coexisting axial and appendicular circuitry.…”

Section: Introductionmentioning

confidence: 99%

“…In the latter, whereas exogenously applied 5-HT increases the duration of axial motoneuron bursts with little effect on cycle periods (Sillar et al, 1992), at later premetamorphic stages, this amine increases both burst and cycle durations. In contrast, NA lengthens the cycle periods of embryonic swimming without altering motor burst durations (McDearmid et al, 1997), whereas at premetamorphosis, axial burst durations are increased but without significant changes in cycle periods (Fig.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Opposing Aminergic Modulation of Distinct Spinal Locomotor Circuits and Their Functional Coupling during Amphibian Metamorphosis

Rauscent¹,

Einum²,

Ray³

et al. 2009

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.