THE QUESTION OF RELATIONSHIP BETWEEN GOLGI VESICLES AND SYNAPTIC VESICLES IN OCTOPUS NEURONS

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1 J. Cell Set. 7, 89- (97) Printed in Great Britain THE QUESTION OF RELATIONSHIP BETWEEN GOLGI VESICLES AND SYNAPTIC VESICLES IN OCTOPUS NEURONS E. G. GRAY Department of Anatomy, University College London, England SUMMARY Electron microscopy of the vertical lobe of octopus brain shows that the synaptic knobs of axons with penkarya in the median superior frontal lobe have synaptic vesicles, approximately 8 % of which are dense-cored (or granulated). In contrast, the endings of the amaenne neurons in the vertical lobe and the endings in the retina and optic lobe, both of which are derived from the retinal visual cells, have only agranular synaptic vesicles. The Golgi apparatuses of the median superior frontal penkarya have vesicles, approximately 4-3 % of which are granulated. The amaenne Golgi apparatuses have -5 % granulated vesicles. The visual cell Golgi apparatuses have virtually no dense-cored vesicles, only agranular ones. The question of the formation of dense-cored and agranular synaptic vesicles at the Golgi apparatus and their subsequent transport to the terminals are related to these observations. INTRODUCTION The division of the octopus brain into discrete lobes facilitates the recognition of ordered sets of neurons by light microscopy (see Young, 964, 97). This ordered arrangement is proving especially fruitful for electron microscopy, for to understand the synaptic connexions fully it is essential not only to see them, but also to know their precise location. At present we are establishing criteria for the recognition of the various types of synapse, and one striking feature of the octopus brain is the presence of numerous synapses with dense-cored synaptic vesicles in addition to synapses with only agranular vesicles. In the vertebrates there is evidence that the small (approximately 5 nm) dense-cored vesicles may contain catecholamines and that some at least may be formed at the Golgi apparatus in the perikaryon and then transported down the axon to the presynaptic knobs (see Hokfelt, 968, 969, for review and references). Possibly some of the clear (agranular) synaptic vesicles are similarly formed and transported, but evidence is lacking. Now in the octopus brain there are several sets of neurons of which cell bodies, trunks and endings can be located and identified with the electron microscope without difficulty. Three groups are considered here. First, there are the cell bodies of the median superior frontal (MSF) lobe. Their axons run into the outer zone of the medulla of the vertical lobe, where they form synaptic contacts on the trunks of the amacrine cells (see Gray & Young, 964). The MSF endings contain synaptic vesicles approximately 8 % of which have dense cores (see Gray, 976). Secondly, the

2 9 E. G. Gray amacrine cell bodies can easily be recognized in the cortex of the vertical lobe with their trunks running into the medulla of the vertical lobe. The trunks have dilatations containing synaptic vesicles, virtually all of which are agranular. (The amacrine trunks probably contact branches of the large cells of the vertical lobe and are themselves contacted by MSF fibres.) Thirdly, the visual cell bodies in the retina are readily identified (see Gray, 97a). These give rise to two sets of synaptic knobs: () the terminals on collateral branches which arise from their perikarya and contact neighbouring visual cells, and () the large carrot-shaped endings. The latter are formed at the extremities of the axons of these visual cells, which constitute the optic nerves (see Dilly, Gray & Young, 963). Both these types of endings of the visual cells contain only agranular synaptic vesicles. It may then be asked whether the Golgi apparatuses of the superior frontal lobe neurons contain dense-cored vesicles, and whether they are absent from the Golgi apparatuses of the amacrine and the visual cell neurons. For if so, it might perhaps be possible to predict whether a given neuron will or will not have dense-cored synaptic vesicles in its endings simply by a study of its Golgi apparatus, and thus aid our unravelling of the connexions of the octopus brain. METHODS The vertical and superior frontal lobes of the octopus were fixed by an injection technique (see Gray, 976) and the retina by an immersion technique (see Gray, 97a). The fixative used was % OsO 4 in saline buffered with veronal acetate at ph 7-3, and fixation was continued for 3 h. Ethanol and epoxypropane were used for dehydration and Araldite for embedding. All the material was block-stained with % uranyl acetate and the sections were further stained with lead citrate (see Gray, 976 for details). For counting, the first Golgi units to appear on the screen of the electron microscope were photographed from sections of each of the 3 different regions of the brain at a fixed magnification of x 8. The total number of vesicles appearing in each micrograph was counted and then the number of dense-cored vesicles; in this way a percentage was obtained. Using percentages obviates the need to take into account variations in section thickness of the different preparations. All round or oval vesicles less than 6 nm were counted, since this dimension represents the approximate upper limit of the diameters of dense-cored vesicles. RESULTS Observations on the Golgi apparatuses of the visual cells of the retina showed that dense-cored vesicles were virtually absent. In the micrographs (an example is shown in Fig. ) a total of 93 plain vesicles was counted. Each Golgi apparatus averaged 44 vesicles. Only in one picture was there one possible example of a densecored vesicle. The Golgi apparatuses of both the MSF (Fig. ) and the amacrine neurons (Fig. 3) showed dense-cored vesicles (Table ). Two out of the MSF Golgi apparatuses showed no dense-cored vesicles, as against 6 of the amacrine Golgi units. The mean percentage of granular vesicles in MSF Golgi apparatuses is 4-3% (s.d. = -69), compared with amacrine Golgi apparatuses which showed a mean of -5% granular vesicles (s.d. = -3). The percentage of granular vesicles in the Golgi apparatuses of

3 Golgi vesicles and synaptic vesicles 9 the MSF neurons is significantly greater than in those of the amacrine neurons (P = < o-ooi). A typical carrot-shaped ending in the optic lobe of a visual cell (Fig. 4 and see Dilly et al. 963) shows the numerous synaptic vesicles (3-5 nm in diameter), all of which are agranular (i.e. lacking dense cores). A smaller, neighbouring terminal, of undetermined source, does incidentally contain dense-cored vesicles, indicating Table. Comparison between the numbers of dense-cored and agranular vesicles in the Golgi apparatuses of neurons in the median superior frontal lobe and those in the Golgi apparatuses of amacrine neurons of the vertical lobe Total vesicles in MSF Totals 53 No. of dense-cored ones / /o ' '3 3-i i Total vesicles in amacrine cells i No of dense-cored ones /o i that the technique is adequate to demonstrate such vesicles. The visual cell collateral endings in the retina, with their agranular synaptic vesicles, are illustrated in the accompanying paper (Gray, 97a). An MSF ending with its mixture of dense-cored and agranular vesicles is shown in Fig. 5. It contacts an amacrine trunk, which has comparatively large (average diameter about 9 nm) agranular vesicles. With favourable planes of section these trunks can be seen to be presynaptic to other processes, so these amacrine vesicles may justifiably be termed synaptic vesicles (see Gray & Young, 964; Gray, 976, for details). DISCUSSION The above observations show that there is no clear-cut correlation between the presence or absence of dense-cored vesicles amongst the agranular vesicles of the Golgi apparatus and the presence or absence of dense-cored vesicles amongst the agranular

4 9 E. G. Gray synaptic vesicles in the corresponding nerve ending of a given neuron. A relationship holds for the MSF neuron endings with dense-cored vesicles in both their Golgi apparatuses and endings, and for the visual cells where dense-cored vesicles are absent in both sites. However, the amacrine cells with agranular synaptic vesicles in their knobs showed a proportion of dense-cored vesicles at their Golgi apparatuses although only -5% compared with 4'5% in the MSF Golgi apparatus. Thus, as a clue to unravelling the connexions in octopus brain, it may turn out that neurons with only agranular Golgi vesicles can be predicted to have only agranular vesicles at their endings, but that neurons with some dense-cored vesicles at their Golgi apparatuses may not necessarily have dense-cored vesicles mixed with the agranular synaptic vesicles at their endings. More extensive observations are needed to decide whether or not the difference of 4-3% and -5% in the Golgi apparatus may be a sufficient guide to the nature of the vesicle content in the related synaptic knobs when a population of neurons is considered. Another possibility is that amongst the small cell perikarya in the vertical lobe, which were all counted as amacrine cells, there is in fact another type of small neuron, which has dense-cored vesicles both in its Golgi apparatus and its endings. However, detailed investigations (Gray, 976) have so far revealed only one sort of small neuron, the amacrine cell, in the vertical lobe, in agreement with Young (964). The other sort have much larger perikarya and in addition their location and other features make them easily distinguishable from the amacrines (Young, 964, 97; Gray, 976). These large cells were avoided when the counts were made. If the synaptic vesicles are formed at the Golgi apparatus, they should be detected with the electron microscope in transit down the axons. In the vertebrates there is evidence consistent with this proposition, especially where the monoamine-containing dense-cored vesicles are concerned (see, for example, Dahlstrom, 966; Kapeller & Mayor, 967, 969a, b\ Mayor & Kappeller, 967; Zelena, Lubinska & Gutmann, 968; Hdkfelt, 968, 969; Geffen & Ostberg, 969; Geffen, Livett & Rush, 969). Possibly only some of the vesicles become charged with detectable monoamine at the Golgi apparatus, while others remain agranular and become charged only during transit or after arrival at the ending. Also, some vesicles may be formed locally at the ending. Also, agranular vesicles can often be seen with the electron microscope as if in transport, in the axons of non-adrenergic neurons (A. R. Lieberman, personal communication). However, a variety of size ranges of membrane-bound bodies is often apparent and one can never be quite sure which is destined to become a synaptic vesicle and which is just a piece of spherical agranular endoplasmic reticulum (the dense-core label being absent). In the octopus brain observations are consistent with the transport theory. Fig. 6 shows both dense-cored and agranular vesicles, apparently in transport in the initial portions of two axons of MSF neurons. Agranular vesicles are common in all regions of the amacrine cells between the Golgi apparatuses and the synaptic knobs (Gray, 976). Similarly, agranular vesicles can be detected along the length of the collaterals of the retinal visual cells and in the various regions of their axons (Dilly et al. 963; Gray, 97 a).

5 Golgi vesicles and synaptic vesicles 93 Both noradrenaline and dopamine are detectable in homogenates of the vertical lobe (A. V. Juorio, personal communication), but it is not yet known whether these substances are concentrated in the dense-cored vesicles of the MSF endings. These dense-cored vesicles have a mean diameter of about 7 nm, whereas mammalian monoamine-containing dense-cored vesicles are about 5 nm (see Hokfelt, 968). (However, the size of the MSF dense-cored vesicles may vary under different osmotic conditions; see Gray, 976). Nor can the dense cores be clearly seen in vesicles in permanganate-fixed preparations of the median superior frontal lobe (either at the Golgi apparatus or in the neuropil), although this fixative is best for displaying the monoamine dense cores (Richardson, 966). However, Richardson used a 3% concentration of potassium permanganate, and so far I have used only a % solution. In a gastropod mollusc, Rogers (968) has described large (approximately nm) dense-cored vesicles in synaptic bags of nerve tissue where there is evidence for catecholamines (see also Gerschenfeld, 963). I am indebted to Mr S. Waterman for photography and Miss H. Pease for technical assistance. REFERENCES DAHLSTROM, A. (966). The Jntraneuronal Distribution of Noradrenaline and tlie Transport and Life Span of Avune Storage Granules in the Sympathetic Adrenergic Neurons. M.D. Thesis, Stockholm. DILLY, P. N, GRAY, E H. & YOUNG, J. Z. (963). Electron microscopy of optic nerves and optic lobes of Octopus and Eledone. Proc. R. Soc. B 58, GEFFEN, L. B., LIVETT, B. G. & RUSH, T. A. (969). Immuno-histochemical localization of protein components of catecholamine storage vesicles. J. Physiol., Lond. 4, GEFFEN, L. B. & OSTBERG, A. (969). Distribution of granular vesicles in normal and constricted sympathetic neurons. J. Physiol., Lond. 4, GERSCHENFELD, H M. (963). Observations on the ultrastructure of synapses in some pulmonate molluscs. Z. Zellforsch. mikrosk. Anat. 6, GRAY, E. G. (97a). A note on synaptic structure of the retina of Octopus vulgans. J Cell Sci. 7, 3-5. GRAY, E. G. (976). The fine structure of the vertical lobe of Octopus Phil. Trans R Soc. Ser. B (in the Press). GRAY, E. G. & YOUNG, J Z. (964). Electron microscopy of synaptic structure of Octopus brain. J. Cell Biol., H5KFELT, T. (968). In vitro studies on central and peripheral monoamine neurons at the ultrastructural level. Z Zellforsch mikrosk. Anat. 9, -74. H5KFELT, T. (969) Distribution of noradrenahne in storing particles in peripheral adrenergic neurons as revealed by electron microscopy Ada physiol scand. 76, KAPELLER, K. & MAYOR, D. (967). The accumulation of noradrenaline in constricted sympathetic nerves as studied by fluorescence and electron microscopy Proc. R. Soc. B 67, 8-9. KAPELLER, K. & MAYOR, D. (969a). An electron microscopic study of the early changes proximal to a constriction in sympathetic nerves. Proc. R Soc B 7, KAPELLER, K. & MAYOR, D. (9696). An electron microscopic study of the early changes distal to a constriction in sympathetic nerves Proc. R. Soc. B 7, MAYOR, D & KAPPELLER, K. (967). Fluorescence microscopy and electron microscopy of adrenergic nerves after constriction at two points. Jl R. microsc. Soc. 87, RICHARDSON, K. C. (966). Electron microscopic identification of autonomic nerve endings. Nature, Lond., CEL 7

6 94 E. G. Gray ROGERS, S. C. (968). Fine structure of smooth muscle and neuromuscular junctions in the optic tentacles of Helix aspersa and Limax flavus. Z. Zellforsch. mikrosk. Anat 89, 8 94 YOUNG, J. Z (964) A Model of the Brain. Oxford: Oxford University Press. YOUNG, J.Z. (97). The Anatomy ofthe Nervous System of Octopus vulgaris. Oxford: Clarendon Press. ZELENA, J., LUBINSKA, L. & GUTMANN, E. (968). Accumulation of organelles at the ends of interrupted axons. Z. Zellforsch. vnkrosk. A-nat. 9, -9. {Received 3 October 969) REV am av dcv in msf mt nf IATIONS ON PLATES amacnne trunk agranular vesicle dense-cored vesicle mitochondrion terminal of axon from median superior frontal lobe microtubule neurofilament nuc r s sc sv t V nucleus ribosome spinous post-synaptic invagination synaptic cleft agranular synaptic vesicle small terminal with dense-cored vesicles Golgi agranular vesicle Fig. Golgi apparatus of a retinal visual cell. No dense-cored vesicles are present in the section. Fig.. Golgi apparatus of a median superior frontal neuron. Two dense-cored vesicles are seen; two others (not shown) were present in another part of the field. Fig. 3 Golgi apparatus of an amacrine cell of the vertical lobe. Two dense-cored vesicles are present in the section.

7 Golgi vesicles and synaptic vesicles

8 96 E. G. Gray Fig. 4. A carrot-shaped ending in the optic lobe of a retinal visual cell. The ending is packed with agranular vesicles. Mitochondria occur in the superficial part of the ending and numerous spinous invaginations in the deep part constitute the post-synaptic elements An adjacent ending, of unknown origin, contains dense-cored vesicles.

9 Golgi vesicles and synaptic vesicles

10 98 E. G. Gray Fig. 5. Vertical lobe' ending of median superior frontal cell with (in this example) 5 % granulated vesicles. It contacts a dilated region of an amacnne trunk, which has synaptic vesicles only of the agranular variety.

11 Golgi vesicles and synaptic vesicles

12 oo E. G. Gray Fig. 6. Two initial portions of axons of median superior frontal neurons cut in longitudinal sections. Dense-cored and agranular vesicles are present.

13 Golgi vesicles and synaptic vesicles

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