The Origin of the Integrative Systems: A Change in View Derived from Research on Coelenterates and Sponges

THE ORIGIN OF THE INTEGRATIVE SYSTEMS: A CHANGE IN VIEW DERIVED FROM RESEARCH ON COELENTERATES AND SPONGES MAX PAVANS DE CECCATTY* Can speculation about the evolutionary origin of the nervous system have any valile? That we may never know exactly by what route the beliaviour machinery ofthefirst Metazoa was derived L· only too probable, and the past hutory ofsuch speculations does not encourage one to suppose that today will be enduring. But so long as we are careful not to confuse that which is speculative with that which is true, they can have a real if limited value. They encourage usfrom lime to time to reconsider the capabilities ofsimple systems in the light of contemporary knowledge. [Pantin 1956] Cajal [1] and Parker [2] were led by the contemporary knowledge to conceive a theoretical model of a primitive animal to bridge the gap between the sponges and the coelenterates, the former "without" and the latter "with" a nervous system. They proposed an ideal invertebrate in which independent neurons are scattered in the teguments and are—each one of them—both sensory and motor. We can ask ourselves why these scientists, and so many after them, elaborated a model for which there was no living evidence. (The evidences for sensory-motor neurons have been only recently reported in a mollusc [3], in Hydra [4], and in Ctenophora [5], that is, in animals in which the nervous system is well developed.) Neurology was, at that time, the scene of a dispute which greatly divided anatomists into "reticularists" and "neuronists." When the neuronists, led by Cajal, had to consider the most primitive stage of nervous organization, how could they but follow the logical conclusion of their ideas which reduced the origin of the nervous system to that of one nerve cell? Besides, for the majority of biologists at that period, and ?Laboratory of Histology and Tissue Biology, University Claude Bernard (Lyon-I), 43 Boulevard du 1 1 Novembre, 69621 Villeurbanne, France. These studies are supported by the Centre National de la Recherche Scientifique (ERA-183 and RCP 248), France. 1 . dedicate this article to the memory of C. F. A. Pantin and thank P. R. Bergquist, W. C. Jones, J. Kennedy, G. O. Mackie, and E. A. Robson for their advices or revisions of the manuscript. Perspectives in Biology and Medicine · Spring 1974 | 379 indeed for many of our contemporaries, the basic functional unit of the nervous system is the reflex. This concept involves a conclusion as logical as the previous one and reduces the origin of nervous integration to that of the reflex. Thus, the founders of the modern neurology came to propose a rigourous theory, placing the origin of the nervous system in its most elementary form as a characteristic mononeuronal reflex arc. All the facts which supported this theory remain unchallenged today: low reactivity of sponges, the true nervous system of coelenterates, the discontinuous synaptic nature of all nervous networks, the generality of the reflex arc, and also the ectodermal origin ofthe nervous cord during the embryonic development of higher animals. But, for the last 20 years, new discoveries—also indisputable—have increased our knowledge. And, according to a well-known process in the history of science, the accumulation of new data often makes previous theories out of date, not because they are false, but because they are not sufficiently true to continue to be totally operative. The Lesson of Coelenterates Improvements in the analysis of primitive nervous systems came from many anatomical and physiological works dealing with coelenterates in which the structural and functional features of the nervous system are simpler but not fundamentally different from those of higher metazoans [6]. But, with regard to our topic, a new point of view was provided chiefly by the research on behavioural physiology [7-13]. Pantin pointed out the necessity for a total (and not only local) integration of the multicellular organism with respect to signals from the environment—an integration which cannot be achieved by one or several elementary reflex arcs. What does it matter if a given muscle cell responds to a particular stimulation transmitted by a neuron? What does matter is the reaction of the muscle field as a...