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Aspects of the Organization of Central Nervous Pathways in Aplysia Depilans

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Aspects of the Organization of Central Nervous Pathways in Aplysia Depilans '. Exp. Biol. (196a), 39, 45-69 45 ith 13 text-figures Printed in Great Britain ASPECTS OF THE ORGANIZATION OF CENTRAL NERVOUS PATHWAYS IN APLYSIA DEPILANS BY G. M. HUGHES* AND L. TAUC Centre d'£tudes de Physiologic nerveuse du Centre National de la Recherche Scientifique, Paris, and Institut de Biologie marine d'Arcachon, France {Received 22 November 1961) There has been little recent work on the relationship between the behaviour of gastropod molluscs and the activity of their nervous systems. Older workers (e.g. ten Cate, 1928), studied the effects of electrical stimulation of different nerves on the movements of parts of the animal. More recently observations on the spontaneous activity and electrical properties of individual cells in isolated ganglion preparations have been extensively carried out (Arvanitaki, 1942; Tauc, 1955, 1957a, b, 1958, 1960a; Hagiwara & Saito, 1959), but little attention has been paid to the importance of these phenomena in the life of the animal. Furthermore, deductions concerning the behaviour of gastropods based on observations of the activity in isolated ganglia are necessarily tentative (Hughes & Kerkut, 1956). The most recent study of neuronal pathways is that of Turner & Nevius (1951) on Ariolimax columbianus. They used external electrodes in stimulation and recording experiments and made tentative proposals concerning the layout of some of the typical neuronal connexions. As they point out, little is known of the connexions between neurones, and anatomical methods are unable to provide sufficient information about the nature of neuronal connexions over long distances. Nisbet (1961) has recently recorded impulses in the pallial nerves of Archachatina in response to tactile stimulation and has studied conduction in the nerves and across ganglia. Techniques similar to those of Turner & Nevius have been used in the present work but in addition intra- cellular micro-electrodes have been employed for recording the activity of individual cells in whole animal preparations. This technique is extremely valuable as the pattern of activity of single units, now well known from such cells in isolated preparations (Tauc, 1960a), gives additional information about the paths of single neurones over quite large distances. A preliminary account of results of such investigations on the so-called giant cells of Aplysia has already been published (Hughes & Tauc, 1961). In the present paper special attention is given to the general nature of pathways within the central nervous system and to the activity of cells in the abdominal ganglion while this retains its connexion with the rest of the animal. This preparation enables a study to be made of the influence of peripheral stimulation on the spontaneously active cells. Studies have also been made in isolated preparations of the different type3 of activity found in cells of the pleural ganglion and these are compared with what is already known about abdominal ganglion cells. • Department of Zoology, Cambridge, England. 46 G. M. HUGHES AND L. TAUC MATERIAL AND METHODS During the months of September and October many individuals of Aplysia depilans are found in the Bassin d'Arcachon where they feed on the Zostera and lay their eggs. The animals were freshly caught and kept in well-aerated sea water at the marine station. The specimens used were about 10 in. long and before any incisions were made the animals were stimulated mechanically to exude most of their purple and white secretions. The animal was then pinned out in a dissecting dish and the foot main- tained in a fairly elongated position. The parapodia (or wings) were also pinned out on the two sides. An incision was first made from the base of the reduced mantle cavity anteriorly to the head. The viscera were thus revealed and the alimentary canal was quickly removed to prevent any of the gastric juices coming into contact with the nervous system during the isolating procedure. The dissection was well washed in sea water and the nervous system dissected according to the particular experiment. Isolation of the abdominal ganglia alone was readily accomplished in the usual way (Tauc, 1955). In other experiments the whole central nervous system with the pleural, pedal, cerebral and abdominal ganglia was carefully dissected with all their connectives and more important nerves intact. The isolated ganglia were then spread out in a waxed Petri dish and pinned through the sheath surrounding the ganglia. If micro-electrode recording was to be done this sheath was cut under the microscope by means of a micro-scalpel. The sheath immediately retracts from the cut and reveals the orange-coloured ganglion cells. In whole animal preparations only the first incision was made and the body wall pinned on both sides. Micro-electrode studies were then only possible on the abdominal ganglia because of the difficulty of pinning any others to a firm base, which was necessary if the electrode was to main- tain its position during the limited movements of the animal. The great length of the connectives between the abdominal ganglia and the circumoesophageal ring made it possible to pin the abdominal ganglia to a waxed Perspex stage which was rigidly fixed to the dissecting dish. Conventional electrical recording methods were used. Pairs of silver-silver chloride electrodes were placed on several nerves of the preparation and by means of a bi- polar switching arrangement each pair of electrodes could be connected either to a stimulator or to a Grass pre-amplifier. In the case of whole animal preparations as many as four or five pairs of electrodes were placed in position at various places. The glass capillary micro-electrodes were filled with a 2-5 molar potassium chloride and connected to a cathode follower. The amplifiers fed into a double-beam oscillo- scope and simultaneously to a four-channel pen recorder. The indifferent electrode was a coil of chlorided silver wire placed in sea water bathing the preparation. Changes in the polarization of the cell were achieved through the same electrode as was being used for recording by means of a bridge circuit (Araki & Otani, 1955). Movements of the parapodia were recorded by means of an RCA 5734 mechano- transducer valve and a light lever hooked to the parapodium. Central nervous pathways in Aplysia depilans 47 RESULTS (i) Gross morphology of the nervous system The descriptions of Mazzarelli (1893), McFarland (1909), and Eales (1921) give very complete accounts of the gross structure of the central nervous system and de- scribe in some detail the nerves from various ganglia, but each is based on a different species of Aplysia. The three species are compared by Hoffmann (1939) who experi- enced difficulty in homologizing the nerves, partly because of differences in the com- pleteness of these accounts. The description of Mazzarelli, based upon Aplysia depi- lans, is less complete concerning the precise innervation of periphral structures and in the present work most use was made of Eale's account of A. punctate It is apparent, Cerebral ganglia Right C-pi. Pleural •^ ganglion Branchial nerve Abdominal ganglia Fig. 1. Diagram of the chief ganglia and connectives of the central nervous system of A. depi- lans. The main nerves leaving the pedal and abdominal ganglia which were used in recording and stimulating experiments are shown, but their branches and many finer nerves have been omitted. however, that A. depilans differs in several respects from A. punctata and some of these may be related to the greater use which A. depilans makes of its parapodia during swimming. For instance, the third pedal nerve of A. punctata does not inner- vate the parapodia, whereas it does in A. depilans. Confirmation of this was obtained from both stimulating and recording experiments which showed that both sensory and motor fibres innervating the posterior portion of the wing were present in this large nerve, which in the present paper will be called the posterior parapodial nerve. The other nerves which arise from the pedal ganglia were also studied by recording and stimulating techniques. Two of them which innervate respectively the middle and anterior region of the parapodia were usually identifiable and are referred to as the middle and anterior parapodial nerves. A nerve which arises from the medial 48 G. M. HUGHES AND L. TAUC and ventral aspect of the pedal ganglia and quite definitely innervates the foot alone is described below as the pedal nerve. These four nerves are the most important in the present work and their position is shown diagrammatically in Fig. 1. where the con- nectives of the different ganglia are also indicated. The two cerebral ganglia are joined to the pleural ganglia by the cerebro-pleural connectives (C-pl.) and to the pedal ganglia by the cerebro-pedal connectives (C-pe). The pedal commissure (Pe.- pe.) joins the two pedal ganglia. The pleuro-pedal connectives are extremely short and it has not been possible to record from them in the present work. As described above, many nerves radiate from the pedal ganglia to innervate the foot and parapodia on both sides. Few nerves arise from the pleural ganglia, but passing backwards on both sides to the abdominal ganglion is a very long connective. These are referred to in the present work as the right and left (or sometimes pleuro-visceral) connectives. Their precise homologies are doubtful and depend upon the interpretation of the posterior ganglionic mass, which is described here as the abdominal ganglion. Primitively, the visceral loop has along its length a parietal ganglion on each side and a posterior single or paired visceral ganglion. In Aplysia there seems to be general agreement that the right parietal ganglion has fused with the visceral ganglion and is represented by the right half of the abdominal ganglion. The fate of the left parietal ganglion is not so certain, though most authorities suppose that it is fused with the original visceral ganglion and together they form the left half of the final composite ganglion.
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