Evolutionary Mechanisms and Neural Adaptation: Selective Versus Constructive Strategies in the Development and Plasticity of the Nervous System

The correct function of the nervous system requires complex neural networks bearing precise connections. In principle, the high structural specificity of neural circuits could be achieved by genetically-determined processes, selected and refined during evolution. Highly conserved gene networks regulate some crucial steps of neural development, such as the regionalization of the neural tube and the initial phases of neurogenesis and synaptogenesis. A totally hardwired nervous system may meet the requirements of adaptation and natural selection at the population level. Nevertheless, it would be inadequate to allow individual organisms to cope with rapid changes of environmental conditions. Neural adaptation to external constraints can be partly achieved by introducing selective mechanisms in neural development. Accordingly, neurons are generated in excess and then partially eliminated to match the actual extension of innervation territories. Such mechanisms, however, are restricted to a set of potentialities, which must be predetermined in the ontogenetic program. On the other hand, constructive mechanisms, in which external stimuli directly influence structural modifications of neural circuits to produce adaptive responses, may allow individual organisms to cope with a wide variety of unprecedented situations. Thus, in the last ontogenetic period as well as in the adult, when the organism actively interacts with the external milieu, experience exerts a strong growth-promoting effect on neural circuits and connections inducing the emergence of specific functional properties. By this mechanism, which requires strict inhibitory control to prevent aberrant growth and dysfunction, the nervous system exploits external stimuli to create adaptive responses to unexpected situations.