Maturation of rhythmic neural network: Role of central modulatory inputs

Valérie Fénelon, Yves Le Feuvre, Tiaza Bem, Pierre Meyrand
Journal of Physiology-Paris. 2003-01-01; 97(1): 59-68
DOI: 10.1016/j.jphysparis.2003.10.007

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Modulatory systems are well known for their roles in tuning the cellular and
synaptic properties in the adult neuronal networks, and play a major role in the
control of the flexibility of functional outputs. However far less is known
concerning their role in the maturation of neural networks during the
development. In this review, using the stomatogastric nervous system of lobster,
we will show that the neuromodulatory system exerts a powerful influence on
developing neural networks. In the adult the number of both motor target neurons
and their modulatory neurons is restricted to tens of identifiable cells. They
are therefore well characterized in terms of cellular, synaptic and morphological
properties. In the embryo, these target cells and their neuromodulatory
population are already present from mid-embryonic life. However, the motor output
generated by the system is quite different: while in the embryo all the target
neurons are organized into a single network generating unique motor pattern, in
the adult this population splits into two distinct networks generating separate
patterns. This ontogenetic partitioning does not rely on progressive acquisition
of adult properties but rather on a switch between two possible network
operations. Indeed, adult networks are present early in the embryonic life but
their expression is repressed by central modulatory neurons. Moreover, embryonic
networks can be revealed in the adult system again by altering modulatory
influences. Therefore, independently of the developmental age, two potential
network phenotypes co-exist within the same neuronal architecture: when one is
expressed, the other one is hidden and vice versa. These transitions do not
necessarily need dramatic changes such as growth/retraction of processes,
acquisition of new intra-membrane proteins etc. but rather, as shown by modelling
studies, it may simply rely on a subtle tuning of pre-existing intercellular
electrical coupling. This in turn suggests that progressive ontogenetic
alteration may not take place at the level of the target network but rather at
the level of modulatory input neurons.

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