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The Fine Structure of Synapses

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The Fine Structure of Synapses

Citation: Peters, A (2008) The Fine Structure of Synapses IBRO History of Neuroscience [http://www.ibro.info/Pub/Pub_Main_Display.asp?LC_Docs_ID=3313]Accessed: date

Alan Peters

The word “synapse” was coined by Sir Charles Sherrington in 1897 to denote the normalanatomical relations between contiguous neurons (see Foster and Sherrington, 1897). The originof the word is explained in a footnote in Fulton’s Physiology of the Nervous System (Fulton, 1938,p. 55), and in the literature is it is quite clear that Sherrington recognized the synapse as adiscontinuous intercellular junction.

Although most scientists in the 1930s and afterwards accepted the neuron doctrine of Cajal,which postulates that each cell in the nervous system is a discrete entity that has no cytoplasmiccontinuity with other cells, it was not until synapses were examined by electron microscopists inthe 1950s that the last doubt about the existence of cytoplasmic continuity between cells waslaid to rest. In the 1950s it became evident that in both the invertebrate (Robertson, 1953) andvertebrate (Palade and Palay, 1954; Palay, 1956) nervous systems the pre- and postsynapticelements of a synapse are separated by a cleft. It also became evident that the presynapticelements contain vesicles, which were soon postulated to contain the chemicals released to allowconduction. From a morphological point of view, a chemical synapse can be described in term ofits parts (Figure 1).



Figure 1: Asymmetric synapses (S1 and S2) between two axon terminals (At1 and At2), whichcontain spherical vesicles, and the smooth surfaced dendrite (Den) of a non-pyramidal cell in

cerebral cortex. At the synaptic junctions the pre- and postsynaptic membranes are separated bya wide cleft and the postsynaptic membrane has a prominent dense coating on its cytoplasmic

surface. Rat auditory cortex. x100, 000.

The presynaptic component, which is most commonly an axon terminal, is characterized by itscontent of synaptic vesicles that often mingle with mitochondria; in the central nervous systemthe apposing postsynaptic element can have the features of any part of a neuron, and at aneuromuscular junction the postsynaptic component is a muscle cell (see Figure 2); the synapticcleft is the intercellular space between the pre- and postsynaptic components and is usuallybetween 20 and 30nm wide; the synaptic junction is formed by the plasma membranes of the pre-and postsynaptic components, the synaptic cleft, and the densities that occur both on thecytoplasmic faces of the pre- and postsynaptic components and within the synaptic cleft; at



some synaptic junctions vesicles accumulate against the presynaptic membrane at specificvesicles release sites, referred to as active zones (see Figure 2).


Figure 2: A motor end plate.

Passing down the middle of the field is the basal lamina (B), which occupies the synaptic cleftseparating the membranes of the axon terminal (At) and the striated muscle cell on the left. The

axon terminal contains synaptic vesicles (sv) that are concentrated at the active zones (*) of theaxolemma. Although no coated vesicles are evident in the axon terminal, the empty “shells” or“baskets” that form the coats of such vesicles are apparent in the axon terminal (arrowheads).

Rat diaphragm. x 75,000.

The following is a brief account of the different types of synapses found in the nervous system,with references to when some of the first descriptions of these synapses were made.

Types of chemical synapses

The study that had most influence on how chemical synapses are classified was that of Gray(1959). In tissue from cerebral cortex fixed by immersion in osmic acid, Gray (1959) encounteredtwo types of synapses, which he called type I and type II. In his account he states that type Isynapses, which involve dendritic spines and shafts, are formed by axon terminals that contain



round synaptic vesicles These synapses have a synaptic cleft that is abut 20nm wide and there isa prominent density on the cytoplasmic face of the postsynaptic membrane. Type II synapses onthe other hand involve neuronal perikarya and dendritic shafts, have a narrower synaptic cleft ofabout 12nm, and a less prominent density beneath the postsynaptic membrane. In addition, thesynaptic vesicles are smaller in the axon terminals forming type II synapses. Similar synapses havebeen found to occur in other parts of the central nervous system, and in the ventral cochlearnucleus Lenn and Reese (1966) found some axon terminals with synaptic vesicles having meandiameters of 45nm and other with mean diameters of 40nm. They deduced that terminals with thelarger vesicles are excitatory and the others inhibitory in function. Over the years it has beenshown that this deduction is correct.

Asymmetric and symmetric synapses

As in tissue fixed primarily in osmic acid, both the large and the smaller synaptic vesicles appearspherical in the freeze- fractures studies that were abundant in the 1970s (e.g. Akert et al.,1972; Sandri et al., 1977). However, the images of synapses changed when glutaraldehyde wasintroduced as a primary fixative (Sabatini et al., 1963). Prior to the advent of glutaraldehyde,preservation of central nervous system tissue was generally poor, but this changed in the late1970s, when central nervous tissue began to be fixed by perfusion with mixtures of glutaraldehydeand formaldehyde, followed by osmication before embedding. This procedure greatly improvedpreservation, and while the vesicles within some terminals (Gray type I) retained their sphericalshapes in glutaraldehyde fixed tissue, in other terminals some of the vesicles appear elongate(Gray type II). And studying cerebral cortex after glutaraldehyde fixation, Colonnier (1968)concluded that the two types of synapses described by Gray (1959) really represent the extremesof a continuum of morphology. Colonnier suggested that the two extremes should be referred to asasymmetric and symmetric synapses, on the basis of the prominence of the density on thecytoplasmic faces of the postsynaptic components. Asymmetric synapses are those with sphericalsynaptic vesicles and a prominent postsynaptic density, and in general such synapses areexcitatory in function. Symmetric synapses lack a prominent postsynaptic density, and havepleomorphic vesicles, that is some vesicles have round profiles and others are elongate (Figures 3and 4).

Figure 3. Synapses in the cerebellum.In the upper half of the figure are two axon terminals (At1 and At2) from granule cells and theyare making asymmetric synapses with the spines (sp1 and sp2) of Purkinje cells. In the spines arecisternae of smooth endoplasmic reticulum (SR). The synapses are surrounded by processes ofastrocytes (As). The rest of the field is occupied by axons (Ax) of granule cells. Rhesus monkey.x60,000.In the lower half of the figure is a terminal (At) from a basket cell, and it is forming a symmetricsynapse (arrow) with the perikaryon of a Purkinje cell (N). Note the neurofilaments (nf) andmitochondria (mit) in the axonal cytoplasm. Rhesus monkey. x35,000.

In general asymmetric synapses are excitatory in function, and use transmitters such as glutamateand aspartate, although in some locations such as the spinal cord, substantia nigra, striatum andglobus pallidus, superior colliculus and inferior olive, some asymmetric synapses are GABAergic (seelower Fig. 4, and Peters et al. 1991).

Figure 4. Symmetric and asymmetric synapses.In the upper picture are two different axon terminals (At1 and At2) forming symmetric synapticjunctions (arrows) with the cell body (N) of pyramidal cell in cerebral cortex. The different packingdensities and shapes of the synaptic vesicles in the two terminals suggest that they are fromdifferent types of presynaptic neurons. Note the punctum adhaerens (triangle) at one of thejunctions. Cerebral cortex of rat. x80,000.In the lower picture is the axon terminal (At) of a basket cell in cerebellum. It is recognized by thepresence of neurofilaments (nf) and pleomorphic vesicles (sv) in its cytoplasm. These inhibitoryterminals are unusual in that they form asymmetric synapses with dendritic spines of Purkinje cells(sp1 and sp2). Rhesus monkey. x50,000.



In general, however, symmetric synapses are inhibitory in function. Attempts have been made tofit synapses in all parts of the nervous system into these two basic categories, and while therehas been some success, a number of variations have been encountered, even in cerebral cortex inwhich Peters and Harriman (1990) distinguished at least three types of axon terminals formingsymmetric synapses. Nevertheless, this number pales in the light of studies on spinal cord, inwhich Bodian (1972; 1975), Conradi (1969) and McLaughlin (1972) have described as many as sixtypes of axon terminals that can be distinguished from each other on the sizes and shapes of theirsynaptic vesicles. An example of the kinds of variation that can occur is shown in Figure 5, whichis from the cochlear nucleus.

Figure 5. A variety of synapses.Occupying the center of the field is a protrusion from the cell body of a neuron in ventral cochlearnucleus. It is surrounded by a number of axon terminals. Two of the terminals (At1 and At2)contain small, spherical vesicles, but two other terminals (At3 and At4) contain larger sphericalvesicles. The other axon terminals (At5 to At9) contain some elongate vesicles. The synapticjunction formed by axon terminal At5 is noteworthy since it has a regular array of presynapticdensities of the presynaptic grid (arrows). Adult rat. x44.000.

Finally, it must be mentioned that in addition to clear vesicles, other vesicles in some terminalscontain a dense granule. Such granular vesicles are associated with the presence ofcatecholamines (Figure 6, lower half).

Figure 6. Axoaxonic synapse and dense core vesicles.The upper picture shows an axo-axonal synapse between a pyramidal cell axon initial segment (Ax)and the axon terminal of a chandelier cell (At), which has pleomorphic synaptic vesicles. The axoninitial segment is characterized by the presence of fascicles of microtubules (m) in its cytoplasmand the dense undercoating (D) of the axolemma. The synaptic junction is symmetric andinhibitory. Rat cerebral cortex. x90,000.The lower picture shows two axon terminals (At1 and At2) synapsing with a dendrite in thedentate nucleus. One of the terminals (At2) contains agranular, or clear vesicles, while the otherone (At1) contains some granular vesicles with dark cores. Monkey. x90,000.

Disposition of synapses

In terms of their frequency, in all parts of the central nervous system, asymmetric synapsesoutnumber GABAergic symmeteric ones by a factor of about 4:1. And when the disposition ofsynapses on a postsynaptic neuron is examined, it is generally found that inhibitory synapses arepreferentially located on proximal dendrites, the cell body and axon initial segment of thepostsynaptic neuron; locations where inhibition can be most effectively applied. Asymmetricsynapses tend to be preferentially located on distal dendrites and dendritic spines, but it is notuncommon to find symmetric and asymmetric synapses existing side-by-side. For example incerebral cortex this occurs on the cell bodies of inhibitory neurons and on some dendritic spines.

Synaptic junctions

Presynaptic components. At asymmetric synapses there is usually only one synaptic junction. Atthe smallest synapses, this junction may have the form of a complete disc, but at larger synapsesthe junction may have on or two perforations (see Peters and Kaiserman-Abramof, 1969).Consequently, in thin sections taken at right angles to the plane of large junction, it often appearsthat two or three discontinuous densities are present. The reason for the perforations is notknown. However, the number of perforations has been shown to increase during development andto be enhanced by complex behavioral environments (see Greenough and Chang, 1988). It mightbe mentioned that at the neuromuscular junction of striated muscle (Figure 2), there are numerousjunctional zones or vesicle release sites, which consist of many strips arrange at right angles tothe length of the axon terminal (e.g., Dreyer et al., 1973; Heuser and Reese, 1973) since this type


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of synapse needs to fire in a predicable fashion. Multiple release sites also occur at excitatorysynapses between bulbs and Held and the neurons of the ventral cochlear nucleus (Gulley et al.,1978).

At symmetric synapses there may be multiple small synaptic junctional zones, or vesicle releasesites, where vesicles accumulate near the pre-synaptic membrane. In addition there may be anumber of puncta adhaerentia (Peters et al., 1990). The puncta are adhesion sites, and not activezones, since vesicles do not accumulate next to them (see Figure 4, upper picture; Figure 7, lowerpicture).

Gray (1963) found that when tissue is treated with phosphotungstic acid before it is embedded,some dense particles appear within the presynaptic density. These particles form an hexagonalgrid, which is referred to as the presynaptic grid. (see Figure 5; e.g., Akert et al., 1972). Suchgrids can be found at both asymmetric and symmetric synapses, and it seems that thedepressions in the grid are places where vesicle attachments sites are located (see Triller andKorn, 1985; Sur et al. 1995).

In other terminals the role of the presynaptic grid appears to be assumed by a presynaptic ribbon.Such ribbons occur in rods and cones of the retina, in the lateral lines of fishes and in hair cells ofthe cochlear, and their role appears to be to guide synaptic vesicles towards the presynapticmembrane (see Peters et al., 1991).

Postsynaptic components. Postsynaptic densities can be isolated and a number of studies haveexamined their composition (e.g., Carlin et al., 1983; Hunt et al., 1996). At some synapses there isa postsynaptic apparatus. Thus, as first shown by Taxi (1961) in sympathetic ganglia, in additionto the post synaptic density on the plasma membrane there may also be subsynaptic material thatconsists of two dense bars, or a row of dense particles beneath the postsynaptic membranedensity. Another postsynaptic element that is often encountered in the cerebral and cerebellarcortices is the spine apparatus, which consists either simple smooth endoplasmic cisternae, as inthe cerebellum, or of parallel smooth endoplasmic reticulum cisternae separated by sheets ofdense material, as in the cerebral cortex.

Presynaptic dendrites

In the early electron microscopic studies of the central nervous system it was assumed that onlyaxons could be presynaptic, and so synapses could be described as being axo-dendritic, axo-spinous, axo-somatic, or axo-axonic, but then in 1966 Rall and his colleagues (Rall, 1966)produced evidence that in the olfactory bulb there are dendro-dendritic synapses between mitralcell and granule cell dendrites. To cloud the field even further, it was found that not only are bothcomponents of these synapses dendrites, but they are also unusual in being reciprocal synapses:at the same interface both the mitral cell and the granule cell can be pre- and postsynaptic (seeFigure 7).

Figure 7. Dendro-dendritic and dendro-somatic synapses.The upper picture shows the dendrite (Den) of a mitral cell in olfactory bulb, synapsing with thegemmule (gem) of a granule cell dendrite. At the interface between the two there are reciprocalsynaptic junctions with opposite polarities. Where the mitral cell dendrite is presynaptic (left sidearrow) vesicles accumulate against its plasma membrane and the synapse is asymmetric, andexcitatory. When the gemmule is presynaptic (right side arrow) the synapse is symmetric, andinhibitory. Olfactory bulb of rhesus monkey. x80,000.The lower picture shows gemmules (gem) of granule cells synapsing with the cell body (N) of amitral cell. As in the upper picture, at the synapses where the mitral cell is presynaptic (arrows)the junctions are asymmetric. The other junction between the mitral cell and the gemmule on theright is a punctum adhaerens (triangle). Olfactory bulb of rhesus monkey x 60,000.

Where the mitral cell is presynaptic the junction is asymmetric (upper Figure 7, Den to gem) andthe vesicles are round, so that the synapse is excitatory. In contrast, at the granule cell–to-mitral



cell synapse, the junction is symmetric and the vesicles are pleomorphic, so that this synapse isinhibitory (Upper Figure 7, gem to Den). It is assumed that at these synapses the mitral cell-to-granule cell synapses are activated first, and that the excitation is then inhibited by the reciprocalsynapses.

Other examples of dendro-dendritic synapses are to be found in the synaptic glomeruli of thethalamus. These are aggregations of synapsing processes that are often surrounded by anastrocytic sheath. The most widely studied of these glomeruli are those in the lateral geniculatenucleus (e.g. Famiglietti and Peters, 1972; Wilson et al. 1984; Hamos et al., 1985). The mainelements in these glomeruli (see Figure 8) are the terminals from the optic tract (Ax1).

Figure 8. A glomerulus. Lateral geniculate nucleus.This large synaptic glomerulus has a prominent central axon terminal (Ax1), which is an optic nerveterminal. It is forming asymmetric synapses (arrows) both with the dendrite (Den1) of ageniculocortical relay neuron and with a vesicle-filled dendritic terminal from an interneuron(Den2). The vesicle filled dendritic terminals (Den2) also synapse (arrowhead), at inhibitorysynapses, with the dendrites (Den1) of the geniculocortical relay neuron, so that a synaptic triadis formed. A fourth type of profile (Ax2) with somewhat flatter vesicles is also present in theglomerulus. Cat. x40,000.

These are excitatory and form asymmetric synapses with two kinds of elements. One is a dendrite(Den1) belonging to the principal cell in the LGN, and the other is a vesicle-containing dendrite(Den2) of a local circuit GABAergic inhibitory neuron. These three components form triads in whichthe optic tract terminals excite both dendritic components, after which the vesicle-containingdendrites (Den2) one synapse delay later inhibit the dendrites (Den1) of the principal cells (e.g.see Fitzpatrick et al., 1984). Thus, as in the olfactory bulb there is excitation followed after onesynaptic delay by inhibition.

Other places where synaptic glomeruli are found are in the granular layer of the cerebellum (seePalay and Chan-Palay, 1974), the olfactory bulb (see Shepherd and Greer, 1990), and in the dorsalhorn of the spinal cord. And in addition to dendro-dendritic synapses, examples of dendro-somatic,and somato-somatic synapses have been found, as well as dendro-axonic and somato-axonicsynapses, although these latter are not very common (see Peters et al., 1991).

Electrotonic synapses

Not long after the separation had been shown between synapsing elements in the nervous system,intracellular recording showed that between some neurons, there are connections at which thereis no synaptic delay. These connections are electrotonic synapses. The first one to be examinedmorphologically was the electrotonic synapse at the motor junction of the crayfish (Robertson,1953), and this was also the first synapse of this kind to be examined electrophysiologically(Furshpan and Potter, 1969). Since then a number of these synapses have been examined in thenervous systems of fishes by Bennett and Pappas and their co-workers (see Bennett, 1977).Other electronic synapses occur in the retina, in which nearly all type of neurons participate inelectrotonic networks (see Vaney, 2002), as well as in locations such as the lateral vestibularnucleus, the inferior olive, the cerebellum, and the cerebral cortex. In all cases it has been shownthat these electrotonic synapses have the features of gap junctions. Thus, in thin sections takenat right angles to a junction, the outer faces of the apposed plasma membranes are separated bya distance of only 2nm (Fig. 9 lower half), and in freeze-fractured preparations arrays ofhexagonal particles are evident in the plasma membranes at the sites of the junctions (Figure 9;upper half).

Figure 9. Electrotonic synapses.At the upper left is a freeze fractured gap junction, or electrotonic synapse, between twoelements in the retina. The particles (arrows) are connexins and they are on the P face of onemembrane. Corresponding pits, or depressions, are apparent on the E face of the other membraneforming the junction. Inner plexiform layers of rhesus monkey retina. x150,000.



At the upper right is a ribbon-like gap junction between a rod and a cone. The particles of thejunction (arrow) are in a row. Outer plexiform layer of rhesus monkey. x120,000.In the lower picture is a gap junction or electrotonic junction between a presynaptic (pre) mossyfiber (At) and a postsynaptic (post) granule cell dendrite (Den). The gap between the two plasmamembranes is about 3nm. At each end of the junction are puncta adhaerentia (arrows).Cerebellum of viper. X 230,000.

These particles are connexins. Connexins are perforated by a hydrophilic channel, and when theplasma membranes become apposed, the connexins in each of them line up to provide channelsthrough which ions can pass from one cell to the other. The main features of electrotonicsynapses are that they are faster than chemical ones, and they are bidirectional, so that it issometimes difficult to establish which neuron is the functional presynaptic one.

In the 1970s it was thought that electrotonic junctions in the cerebral cortex were rare, andindeed such synapses do not commonly occur between excitatory neurons. But in the past 10years or so, it has been established that electrotonic junctions are common between fast spiking,inhibitory cortical neurons (see Galarretta and Hestrin, 2001, Connors and Long, 2004). Theelectrotonic junctions in cerebral cortex are mainly dendro-dendritic and they tend to be mostcommon between neurons of the same type, for example inhibitory neurons that are parvalbuminpositive, and these same neurons can also be interconnected by chemical synapses.

Finally it should be mentioned that there have been descriptions of mixed synapses, at whichthere is either morphological or physiological evidence for both chemical and electrotonictransmission at the same synaptic interface. But such synapses are not common, and for moreinformation consult Peters et al. 1991.

Summary

It is evident that there are many morphological varieties of synapses, and almost any part of aneuron can be presynaptic, or postsynaptic, to another. With the advent of antibodies, andtechniques for recording from neurons and then intracellular filling them, it has been possible toanalyze the physiology and morphology of some neurons in detail and to determine where theiraxon terminals form their synapses. However, detailed information about how many synapsesindividual neurons receive, and what are the sources of those synapses is still largely missing. Onlywhen that information becomes available will we be able to know how the central nervous systemreally functions. Some of the information about local neuronal circuits may eventually becomeavailable through making extensive three-dimensional reconstructions from serial thin sections, butdetermining the precise connections of neurons with long axonal projections presents much moreof a challenge.

Alan PetersWaterhouse ProfessorDepartment of Anatomy and NeurobiologyBoston University School of MedicineBoston, MA, USA

FiguresAll the figures are reproduced from Peters, Palay and Webster, The Fine Structure of the NervousSystem. Neurons and their Supporting Cells, 3rd edition. 1991. Oxford University Press. New York.

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