Maturation of rhythmic neural network: role of central modulatory inputs

J Physiol Paris. 2003 Jan;97(1):59-68. doi: 10.1016/j.jphysparis.2003.10.007.

Abstract

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.

Publication types

  • Comparative Study
  • Review

MeSH terms

  • Action Potentials / physiology
  • Aging / physiology*
  • Animals
  • Embryo, Nonmammalian
  • Ganglia, Invertebrate / cytology
  • Ganglia, Invertebrate / physiology
  • Models, Neurological*
  • Nephropidae
  • Nerve Net / embryology
  • Nerve Net / physiology*
  • Nervous System / cytology*
  • Neural Pathways / embryology
  • Neural Pathways / physiology
  • Neuronal Plasticity
  • Neurons / classification
  • Neurons / physiology*
  • Periodicity*
  • Synapses / physiology