Functional differentiation of adult neural circuits from a single embryonic network

Abstract

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.

Animal-to-Animal Variability in Motor Pattern Production in Adults and during Growth

“…Receptor and channel density regulation must be appropriately matched to the increase in membrane surface area, and synaptic function must be altered in accordance with changes in input resistance in the postsynaptic cells (Edwards et al, 1994b). The STG has the same number of neurons in embryos and adults (Casasnovas and Meyrand, 1995), and the characteristic triphasic pattern and the regularity of the pyloric rhythm emerge over the course of larval development (Richards et al, 1999). We show here that the STG grows substantially from juvenile to adult animal.…”

Ontogeny of Modulatory Inputs to Motor Networks: Early Established Projection and Progressive Neurotransmitter Acquisition

“…The embryonic STNS can be visualized very early in development (Casasnovas and Meyrand, 1995) and can be dissected out as early as 65% of development (Fig. 1 B2).…”

“…Indeed, bath application of neuromodulatory substances (Harris-Warrick et al, 1992;Marder and Weimann, 1992;Blitz et al, 1995;Richards and Marder, 2000) or stimulation of identified modulatory neurons (Meyrand et al, , 1994(Meyrand et al, , 2000Nagy et al, 1994;Norris et al, 1996;Blitz et al, 1999;Combes et al, 1999) elicits a wide variety of motor outputs from the same neuronal circuitry. Although the embryonic STNS generates a motor output different from the adult one (Casasnovas and Meyrand, 1995), it has been shown recently that embryo can generate adult-like activity patterns (Le Feuvre et al, 1999), suggesting that basic network architecture is similar in the embryo and adult. Moreover, as in the adult, the expression of embryonic circuitry depends strictly on the presence of projection neurons (Le Feuvre et al, 1999) and can be altered by neuromodulatory substances Richards and Marder, 2000).…”

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

“…Thirty neurons located in the stomatogastric ganglion (STG) (Fenelon et al, 1998) are organized into a single motor network in embryos and premetamorphic larvae but form three distinct motor networks in postmetamorphic animals (Casasnovas and Meyrand, 1995). The expression of these different networks is controlled by the same group of modulatory neurons located in more rostral ganglia in embryos and adults (Le Feuvre et al, 1999.…”