Fenestration nodes and the wide submyelinic space form the basis for the unusually fast impulse conduction of shrimp myelinated axons

The great majority of nerve axons in various species are surrounded by a sheath of glial cells. The complexity of this glial sheath varies from a single layer to loose folds, and culminates in the formation of a compact multilayered sleeve of glial membranes known as the myelin sheath. Nerve axons surrounded by such a sheath are usually referred to as myelinated fibres. These have been found in all vertebrates with the exception of lamprey and hagfish (Bullock et al., 1984) and are considered to be exclusive to vertebrates, whereas all the other varieties of ensheathment occur in both vertebrates and invertebrates.

The myelin sheath covering the axon in vertebrates acts as an electrical insulator of high resistance and low capacitance. It is interrupted regularly by ‘nodes of Ranvier’, which are unmyelinated gaps 1–1.5 μm wide in the peripheral nervous system (PNS) and 1–10 μm or wider in the central nervous system (CNS) (see Roots, 1995). Voltage-gated Na⁺ and K⁺ channels are distributed unevenly on the axolemma: the nodal membrane is rich in Na⁺ channels but poor in K⁺ channels, whereas the internodal membrane is rich in K⁺ channels and has relatively few Na⁺ channels. Thus, the myelin sheath and node of Ranvier form the structural basis for the saltatory conduction of a nerve impulse from node to node. Myelination in vertebrates is considered as one of two strategies developed during evolution to increase impulse conduction velocity, the other being the enlargement of axon diameter (see Bullock et al., 1977; Schmidt-Nielsen, 1990; Kandel et al., 1995).

A sheath of multilayered membranes of glial cells devoid of cytoplasm has been reported in two species of earthworm, Eisenia foetida (Hama, 1959) and Lumbricus terrestris (Günther, 1973), in the tubificid worm Branchiura sowerbyi (Zoran et al., 1988), in two species of prawn, Macrobrachium niponensis (Yeh and Huang, 1962) and Palaemonetes vulgaris (Heuser and Doggenweiler, 1966), in the crab Cancer irroratus (McAlear et al., 1958) and in two species of shrimp, Penaeus orientalis (Huang et al., 1963) and P. japonicus (Kusano, 1966; Hama, 1966). However, among these species of invertebrate, saltatory conduction has only been demonstrated in pairs of medial giant fibres in P. orientalis (Hsu et al., 1964, 1975) and P. japonicus (Kusano and LaVail, 1971; Terakawa and Hsu, 1991) and in the median giant fibre of L. terrestris (Günther, 1976). Moreover, in the shrimp, both an unmyelinated branch of the giant fibres in each thoracic and abdominal ganglion and synapses between the medial giant fibre and every motor giant fibre serve as the functional nodes for saltatory conduction (Hsu et al., 1964, 1975; Kusano and LaVail, 1971; Terakawa and Hsu, 1991). In the earthworm, a few spot openings in the myelin sheath of the single median giant fibre serve as functional nodes in addition to several unmyelinated branches (Günther, 1976). To date, no common mode of saltatory conduction and no common structure similar to the node of Ranvier have been demonstrated in invertebrate nervous systems.

Recently, a novel common node for saltatory conduction, termed a ‘fenestration node’, has been found in myelinated fibres in the nervous systems of at least six species of shrimps from the Family Penaeus (Xu and Terakawa, 1993; Hsu and Terakawa, 1996). In addition, the myelinated nerve fibres of all six species of shrimp speed impulse conduction by broadening the gap between the axon and the myelin sheath rather than by enlarging the axon diameter as in other invertebrates. In this review, the fenestration node and some other functional and structural characteristics of the myelinated fibres of Penaeus shrimps are described and discussed with reference to their vertebrate counterparts.

The novel fenestration node has been demonstrated in the following six species of the Family Penaeus (Hsu and Terakawa, 1996): (1) genus Penaeus, P. orientalis Kishinouye (P. chinensis Osbeck, more specifically), P. japonicus Bate, P. monodon Fabricius, P. semisulcatus De Haan; (2) genus Trachypenaeus, T. curvirostris; (3) genus Metapenaeopsis, M. barbata.

The term Penaeus is used in this review to indicate these six species. Nerve fibres in several other species of the genus Penaeus, such as P. aztecus (brown shrimp), P. duorarum (pink shrimp) and P. setiferus (white shrimp), which are found in the Gulf of Mexico, generally share the same myelin characteristics and have a submyelinic space like that in the species mentioned above (Kusano and LaVail, 1971). It is likely that these shrimps also have fenestrated nodes in their myelinated fibres. Thus, these three species can be included in the group of Penaeus shrimps and are so considered in this review. Moreover, we expect most, if not all, decapod crustaceans of the Family Penaeus to share common characteristics in their myelinated nerve fibres, including the presence of fenestration nodes.

The CNS of the Penaeus shrimp is located close to the ventral surface of the body along the median line and is termed the ventral nerve cord. The anatomical structure of the ventral nerve cord of P. orientalis is shown schematically in Fig. 1. It consists of a head ganglion, a suboesophageal ganglion, five thoracic ganglia, five abdominal ganglia and a telson ganglion. A pair of circumoesophageal connectives links the head and the suboesophageal ganglia, and connectives lie between other adjacent ganglia. Two pairs of nerve branches (the first and second roots) originate directly from each thoracic and abdominal ganglion, and a pair of nerve branches (the third root) leaves the ventral nerve cord from the anterior part of every abdominal connective.

Neurons are located on the abdominal side of the thoracic and abdominal ganglia, and two pairs of giant nerve fibres pass through their dorsal region. The connectives contain nerve fibres and a large blood vessel. A cross section of the ventral nerve cord of P. chinensis at the level of an abdominal connective between the second and third roots is shown in Fig. 2A. Among numerous small- and middle-sized nerve fibres, there are five giant fibres: two pairs of giant fibres designated as medial and lateral giant fibres towards the dorsal side of the connectives, and a motor giant fibre running along the ventral nerve cord dorsal to the mid-line.

Conduction velocities greater than 200 m s⁻¹ have been measured in the medial giant fibres of P. chinensis and P. japonicus (Fan et al., 1961; Kusano, 1966). Giant fibre systems occur in the ventral nerve cord of most crustaceans that can swim by flapping their abdomen. They are considered to mediate rapid escape responses (Bullock, 1984).

In vertebrates, myelin sheaths surrounding peripheral nerve axons are formed by Schwann cells and those around central nerve axons are formed by oligodendrocytes, although in both cases their compacted laminae are arranged in a similar way. For invertebrates, the term CNS is used to describe aggregations of nervous tissue such as ganglia, i.e. the term refers to the gross neuronal organization (Hildebrand et al., 1993). Oligodendrocytes, which form the myelin sheath of nerve fibres in the CNS of vertebrates, have not been found in invertebrates (see Bunge, 1968), and the distinction between glial cell types in the CNS and the PNS, typical of vertebrate nervous systems, may not apply to invertebrates (Hildebrand et al., 1993). In this review, all the glial cells myelinating and ensheathing axons in the connectives are referred to as Schwann cells.

As in vertebrates, the myelin sheath of living nerve fibres of P. chinensis shows distinct birefringence when observed with a polarized light microscope. This property was used to make measurements of the relative thickness of the myelin sheath in 110 freshly dissected nerve fibres ranging in diameter from 10 to 230 μm. The ratio of internal diameter to external diameter of the myelin sheaths was constant at 0.69±0.10 (mean ± S.E.M.) (Hao and Hsu, 1965). A ratio of 0.7 is considered to be optimal for impulse conduction in vertebrate myelinated nerve fibres (see Hodgkin, 1964).

At the turn of the century, reports of light microscopy studies suggested that many nerve fibres in decapods such as shrimps, prawns and crabs possessed a sheath that resembled the myelin sheath of vertebrates (see Holmes, 1942). Electron microscopy later showed that the myelin sheath of the vertebrate nerve fibres has multilayered laminae that repeat concentrically and regularly with a period of approximately 11 nm. Electron micrographs of the fibres of two prawn species, Macrobrachium niponensis (Yeh and Huang, 1962) and Palaemonetes vulgaris (Heuser and Doggenweiler, 1966), showed that their sheaths differ from those of vertebrates. In particular, the period of lamination in the sheath of the prawns is more than 20 nm, which is much wider than that in vertebrates. However, Huang et al. (1963) found using electron microscopy that most of the larger nerve fibres greater than 5 μm in diameter in the ventral nerve cord of P. chinensis possess a compact multilayered myelin sheath. Later, similar results were also obtained from P. japonicus (Kusano, 1966). The period of lamination in these sheaths was 8 nm for P. chinensis and 9 nm for P. japonicus.

The segment of myelin sheath between two neighbouring nodes in vertebrates is formed by closely apposed sheets of Schwann cell plasma membrane which form a spiral wrapping around the axon. The spiral is reported to be formed by a progressive advance of the inner lip of the Schwann cell over the axon surface rather than by an advance of the outer lip of the spiralling Schwann cell cytoplasm over its outer surface (Bunge et al., 1989). The spiral of laminated membranes starts from the internal mesaxon, where the outer faces of the plasma membranes come together to form an interperiod line, and ends outside the sheath at the outer mesaxon. The major dense line in the lamination is formed by apposition of the cytoplasmic faces of the membrane. It has been established that both the major dense line and the interperiod line in the myelin sheath of P. chinensis (Huang et al., 1963) and P. japonicus (Kusano, 1966) are also formed by apposition of the cytoplasmic and outer faces of the Schwann cell membrane. However, there is a clear difference in the fine structure of the myelin sheath between shrimps and vertebrates: the compact laminae of the shrimp sheath are not formed by a spiral wrapping of glial cell membrane. Instead, a number of laminae extend from a single Schwann cell to enwrap the axon from both sides, leaving a wide gap between the laminated sheath and the axon. Each lamina completely or partially encircles the axon just once by extending its ends from both sides and by connecting them each with other or with those of laminae from other Schwann cells to form a seam (Xu and Sung, 1980; Xu et al., 1994). In the seam region, the slightly swollen tips of the laminae form terminal loops, which contain a few microtubules. The junctions between the two tips of each lamina are arranged more or less regularly along a line radial to the axon (Fig. 3A,B, arrows). These junctions are frequently associated with an attachment zone (see Fig. 3A, arrowhead), which closely links the adjacent laminae and thus reinforces the sheath. Usually, only one seam line can be seen in a cross section of small-sized myelinated fibres, while two to three seam lines can be observed in cross sections of larger fibres, indicating that each stack of laminae originates from two or three Schwann cells. The seam line can also be observed in longitudinal sections of the fibres, showing that the laminae from adjacent Schwann cells are connected by the terminal loop structure. This tip-to-tip connection of the terminal loops to form a seam may provide some flexibility to the compact multilayered myelin sheath.

Another difference between the myelin sheath of vertebrates and that of the Penaeus shrimp is that in vertebrates the Schwann cell nucleus is located on the outer edge of a segment of the sheath, while in the shrimp the nucleus is randomly located between the sheath laminae (Fig. 3A). The differences in fine structure between the myelin sheaths of vertebrates and of the shrimp are shown schematically in Fig. 4.

From these observations in Penaeus shrimp, it is evident that a compact multilayered myelin sheath has evolved in the nervous system of at least some invertebrates, although the sheath is formed in a different manner from that of vertebrates. The fine structure of the Penaeus shrimp myelin sheath is, however, also quite distinct from that of the myelin enveloping the giant axon of earthworms, where there is a mixture of uncompacted, compacted and spirally arranged myelin lamellae (Hama, 1959; Günther, 1976; Zoran et al., 1988).

A distinctive feature of Penaeus shrimp myelinated fibres is that the axon diameter is much smaller than the fibre diameter. This unusual relationship between the axon and the myelin sheath is depicted in Fig. 2B. In a pair of medial giant fibres dissected from the ventral nerve cord of P. chinensis, one fibre (the lower one) was kept intact, whereas the other (the upper one) was partly desheathed to expose the axon. A thin straight axon is visible in both giant fibres (Fig. 2B). The same structural characteristic is also evident in the middle- and small-sized myelinated fibres of the shrimp (Fig. 2A). In most cases, the axon is as little as one-eighth to one-tenth of the diameter of the host fibre. Although some motor fibres have thicker axons, the axon:fibre diameter ratio is less than 1:4 (Fig. 2A; GMF and M). Two structures unique to the Penaeus shrimp occupy the space between the axon and the myelin sheath: a microtubular sheath and a wide gap filled with a gel.

The axolemma of the myelinated fibres of P. chinensis (Yeh et al., 1963; Hsu et al., 1980) and P. japonicus (Hama, 1966) is closely surrounded by the microtubule-rich processes of a distinct type of Schwann cell. The innermost process is separated from the axon by a gap of just 20 nm. The microtubules in the processes of this Schwann cell are assembled in bundles, which lie more or less parallel to the longitudinal axis of the axon. Each process, flat in the radial direction and elongated longitudinally, is stacked up to other similar processes. This stack of cell processes forms an irregular spiral layer that encloses the axon and forms a unique wall around the axon designated the microtubular sheath (Fig. 3A,C). The nucleus of this Schwann cell has a random location along the sheath (Fig. 3A). The microtubular sheath is usually very thin but, in general, the larger the fibre size the thicker is the sheath. Thus, myelinated nerve fibres of the Penaeus shrimp have three subtypes of Schwann cell, one forming myelin, another ensheathing without myelinating and a third forming the microtubular sheath. The electrical resistance of the microtubular sheath should be low, since there is little difference in the amplitudes of action potentials recorded from the axon and from the submyelinic space (Fig. 5). The most likely function for the microtubular sheath is as a mechanical support for the axon.

The axon and its associated microtubular sheath are surrounded by a wide gap and then by the myelin sheath. This gap between the microtubular sheath and the myelin sheath is unique to the myelinated fibre of the Penaeus shrimp and is designated the submyelinic space (Fig. 3A). The submyelinic space is filled with an amorphous gel, into which a few cells extend numerous processes shaped like thin flaps. Some processes are attached to the outer layer of the microtubular sheath as well as to the inner layer of the myelin sheath. The processes tend to run parallel to the longitudinal axis of the fibre. In small fibres, the axon with its microtubular sheath usually attaches to the inner layer of the myelin sheath, whereas in middle-sized and giant fibres, the complex of axon and microtubular sheath is located asymmetrically in the submyelinic space and tends not to contact the myelin sheath.

The electrolyte composition of the submyelinic space is similar to that of sea water (K. Xu, unpublished results), and no difference in direct current potential is recorded when electrodes are placed in the external medium and in the submyelinic space in the giant fibres of P. chinensis and P. japonicus. The resting membrane potential of the axon measured by microelectrode insertion is −64.3 ±7.4 mV (mean ± S.E.M., N=7) (Xu and Terakawa, 1991). As shown in Fig. 5, it is interesting to note that a monophasic positive action potential is recorded intracellularly from the axon (approximately 75 mV in amplitude) and also extra-axonally from the submyelinic space (approximately 65 mV in amplitude) (Xu and Terakawa, 1993).

This fact indicates that no excitation takes place in the internodal axolemma during impulse conduction and that the submyelinic space is sufficiently well insulated to serve as a conductor that is equipotent to the axolemma so far as impulse conduction is concerned. Indeed, the internodal axolemma has proved to be experimentally inexcitable in the motor giant fibre of P. japonicus (Xu and Terakawa, 1991). The specific resistance of the gel within the submyelinic space of a fibre 120 μm diameter in P. japonicus has been estimated to be as low as 23 Ω cm (Kusano, 1966). The large submyelinic space is, in fact, a low-resistance pathway for the majority of the longitudinal internal current of shrimp nerve fibres. The pattern of local current flow during impulse conduction is shown schematically in Fig. 6.

It is worthwhile noting that, during ontogeny, the axon of the shrimp nerve fibre is first surrounded by the myelin sheath directly, and then the microtubular sheath and submyelinic space gradually develop between the axon and myelin sheath. A developing nerve fibre in the ventral nerve cord of an immature shrimp 5 mm in body length is shown in Fig. 3B. In this fibre, the microtubular sheath and submyelinic space have yet to appear.

Both medial and lateral giant fibres run the entire length of the ventral nerve cord of the Penaeus shrimp without noticeable interruption. Morphological studies have shown that, at each thoracic and abdominal ganglion, the four giant fibres give off unmyelinated branches to nerve cell bodies in the opposite side of the ganglion. Motor giant fibres originating from the last thoracic ganglion and each abdominal ganglion run posteriorly along the connective and divide into two branches. Each branch of the motor giant fibre forms giant synapses with both medial and lateral giant fibres on the ipsilateral side before leaving the connective. Then, through the third root, these branches innervate the abdominal muscles on the ipsilateral side. The anatomical locations for the giant fibres with their unmyelinated intraganglionic branches and giant synapses in the ventral nerve cord are shown schematically in the middle and lower enlarged drawings in Fig. 1.

The action current could only be recorded from the ganglionic and synaptic regions of the giant nerve fibres, and the unmyelinated intraganglionic branches and synaptic membranes were further proved to be the functional nodes for saltatory conduction (Hsu et al., 1964, 1975; Kusano and LaVail, 1971; Terakawa and Hsu, 1991). Moreover, voltage-clamp studies showed that the nodal current of the synaptic membrane consisted of a large Na⁺ current and a small K⁺ current, which is similar to the situation in the amphibian node of Ranvier. It is interesting to note that both activation and inactivation of the Na⁺ current of the functional nodal membrane in the shrimp are the fastest that have been recorded from any animal to date. The time from onset to maximum Na⁺ current in the presynaptic membrane was as short as 100 μs at 20 °C in the fastest case, whereas values measured at the nodes of Ranvier were approximately 150 μs in the frog and 180 μs in the rabbit at the same temperature. The fast rate constant of Na⁺ inactivation in the shrimp was 200 μs at 21 °C, compared with 462 μs in the frog and 513 μs at 20 °C in the rabbit. The rapid kinetics of the shrimp giant fibres is advantageous for fast impulse conduction over long internodal distances (see Terakawa and Hsu, 1991). Indeed, the internodal distances found in the medial giant fibres of adult P. chinensis and P. japonicus range from 3 mm to more than 10 mm.

The record high conduction speed of the shrimp giant fibres may not mean that the conduction efficiency is as high as that of warm-blooded vertebrates. The velocity/diameter relationship for myelinated fibres (Hursh, 1939) predicts that a mammalian myelinated fibre would have a conduction velocity of 600 m s⁻¹ at 37 °C, if the diameter of the fibre was 100 μm (see Terakawa and Hsu, 1991).

The medial and lateral giant fibres in the circumoesophageal connective and in the caudal half of the last abdominal connective do not have synapses or branches for a length that may exceed 20 mm in adult P. japonicus and P. chinensis. If the unmyelinated intraganglionic branches and synaptic membranes were the only source of local currents for saltatory conduction, the internodal distance for fibres in these connectives would appear to be too long for impulses to propagate. Moreover, neither synaptic structures nor unmyelinated branches were found in many middle- and small-sized myelinated fibres in the connectives of the ventral nerve cord of the shrimp. This led us to suspect the presence of an unknown type of node in shrimp myelinated fibres. No node-like structure was apparent in fixed or living preparations examined by conventional microscope. However, by scanning a single living nerve fibre preparation from P. japonicus using a differential interference contrast (DIC) microscope, we found a novel type of nodal structure. Using voltage-clamp procedures, we proved that the structure functions like the node of Ranvier in vertebrate myelinated fibres (Xu and Terakawa, 1993; Hsu and Terakawa, 1996).

With DIC microscopy, the myelin sheath of the nerve fibres of Penaeus shrimp can be clearly seen (Fig. 7). The distance between the axon and the myelin sheath, the submyelinic space, is quite uniform, the same separation being maintained over long distances. Along a whole single fibre preparation, a few regularly spaced spots are present where the smooth continuity of the myelin sheath is interrupted by many circular or ellipsoidal areas arranged concentrically. In the DIC microscope, these concentric circles appear to form a crater-like structure, shown in top view in Fig. 7A,B.

When viewed from the side, this structure is characterized by a lack of myelin, forming a round ‘window’ onto the axon. In this region, the thickness of the myelin sheath tapers, suggesting that the layers of myelin at the edge of the window gradually decrease in number so that the window resembles a crater on the axolemma. Hereafter, we refer to this structure as the fenestration node. In the fenestration node region, the axon is swollen and attached to the myelin sheath. Once the site of the fenestration node has been noted under the DIC microscope, it can be detected with a conventional bright-field microscope.

The fenestration node was first found in the circumoesophageal and telson segments of the medial and lateral giant fibres of P. japonicus. The number of fenestration nodes is variable, ranging from one to three in the circumoesophageal segment and from five to six in the telson segment (Hsu and Terakawa, 1996). The arrangement of the fenestration nodes as well as other excitable membranes that function as nodes (unmyelinated intraganglionic branches and synaptic membranes) is shown schematically in the enlarged drawings of Fig. 1. The fenestration node was later also found as a regularly spaced structure in numerous smaller myelinated fibres in the ventral nerve cord of the shrimp. The fenestration node has now been identified in the myelinated fibres of five other species of Penaeus shrimp, as described above.

The internodal distance is roughly proportional to the diameter of the fibre. For example, the internodal distance was 3 mm in nerve fibres with a diameter of approximately 40 μm, but was as long as 12 mm in the circumoesophageal segment of a medial giant fibre 170 μm in diameter. The diameter of the fenestration also depends on the diameter of the nerve fibre. For example, the largest diameter of the outermost ring of the myelin layer around the fenestration was 50 μm in a medial giant fibre 150 μm in diameter and approximately 5 μm in fibres 30–40 μm in diameter. In the region of the fenestration node, the axon is swollen and contains many vacuoles of different shapes and sizes (Figs 7, 8). This does not appear to be a sign of morphological damage, since the vacuoles were observed in fresh nerve fibre preparations showing normal impulse conduction (Hsu and Terakawa, 1996).

Preservation of the axolemma at the fenestration node was actually very difficult using conventional fixation, probably because of the thick myelin sheath and the many large vacuoles in the axon. Of the various methods tried, glutaraldehyde used together with paraformaldehyde or with intermittent microwave irradiation resulted in relatively good fixation. Electron microscopic studies revealed that both the myelin sheath and the microtubular sheath are absent in the fenestration region, and instead a few perineurial cells loosely cover the axolemma with digitated infoldings of various lengths (Fig. 8B). The opening in the myelin sheath is formed just over the swollen part of the axon (Fig. 7), and the myelin layers are seamed and fused together at the edge around the fenestration node (Fig. 8A,B). At this edge, the myelin sheath is tightly attached to the axolemma, presumably forming a close junction between them. The edge of the microtubular sheath is also tightly attached to the myelin sheath so that the submyelinic space is electrically insulated from the external space. The excitable nodal membrane (axolemma attached to the window) is located slightly above the narrowest part of the fenestration in the myelin. Many infoldings are formed by the axolemma at the nodal region, partly by perineurial cell processes but mainly by multiple processes of the microtubular sheath (Fig. 8B,C). These infoldings contribute to the total area of the excitable membrane in the node, which would help to increase the density of the local loop current for saltatory conduction.

To enable comparison of the fine structure of the fenestration node with that of the spot opening in the myelin sheath of the earthworm L. terrestris, two electron micrographs modified from Günther (1973, 1976) are shown in Fig. 9. The differences in fine structure between the fenestration node and the spot opening are evident. In the earthworm spot opening, the nodal membrane is extended towards the upper level of the myelin sheath and is connected directly with the collagenous capsule of the nerve cord. Neither infoldings of axolemma nor vacuoles within the axoplasm are present in the earthworm spot opening.

The nodal currents were recorded and analyzed using the sucrose-gap voltage-clamp method. The results showed that the action current largely arises from the activity of Na⁺ channels located in the nodal membrane. The current/voltage (I/V) curve of the nodal membrane is shown in Fig. 10. Although there is a small outward K⁺ current at the late phase of the clamping pulse, even in the voltage range 50–120 mV, this current would not be enough to terminate the excitation during the action potential. In fact, the fast kinetics of the Na⁺ channel per se is responsible for both the rapid termination and the rapid onset of the action potential (Hsu and Terakawa, 1996).

Roots (1995) suggested that a myelin sheath evolved independently in chordates, arthropods and annelids. The widespread distribution of fenestration nodes in the nerve fibres of various species of the Penaeus shrimp makes the position of their myelin sheath in the evolutionary tree significant. The differences in fine structure of the myelin sheath between vertebrates and invertebrates suggest that the ability to generate the myelin sheath and the different types of node were developed after an evolutionary separation between these two branches of animal (Hsu and Terakawa, 1996).

For most animals, rapid propagation of nerve impulses is of functional importance, and two distinct mechanisms have been developed to achieve this during evolution. One adaptive strategy is to increase the diameter of the axon core and the other is through myelination of axons (Kandel et al., 1995). A myelin sheath interrupted by nodes of Ranvier forms the structural basis for the rapid conduction of impulses from node to node in a saltatory manner. It is usually considered that the former method is largely available to invertebrates, and the latter only to vertebrates, since giant axons are most commonly found in invertebrates, whereas the compact multilayered myelin sheath together with the node of Ranvier have been exclusively observed in vertebrates (Bullock et al., 1977; Schmidt-Nielsen, 1990). In fact, however, a compact multilayered myelin sheath (Huang et al., 1963; Hama, 1966) with regular interruptions by a common node for saltatory conduction (Xu and Terakawa, 1993; Hsu and Terakawa, 1996) has also evolved in the nervous system of the Penaeus shrimp.

The myelinated fibres of the Penaeus shrimp have the following structural and functional characteristics. (1) The period of lamination in the myelin sheath is 8 nm (Huang et al., 1963) or 9 nm (Kusano, 1966), but each lamina is interrupted 1–3 times by a seam formed by the terminal loops, which contain a few microtubules meeting tip-to-tip. The sheath is formed by Schwann cells, which extend numerous laminae to enwrap the axon in a manner similar to a hug with two arms. The seams are arranged in a radial line and are typically accompanied by an attachment zone. The seam structure also serves as a connection between the myelin layers of adjacent Schwann cells along the nerve fibre (Xu et al., 1994). The tip-to-tip connected terminal loop structure is believed to provide some flexibility to the myelin sheath. (2) The compact myelin sheath is regularly spotted with fenestration nodes, which are characterized by a round window lacking myelin. Nodes of this type have been found in the nervous systems of six species of shrimp. (3) Two unique structures, the microtubular sheath and the submyelinic (gap) space, are located between the axon and the myelin sheath. The microtubular sheath may provide mechanical support for the axon. The wide submyelinic space, which is filled with gel, is tightly sealed at the nodal region and is electrically equivalent to an increase in axon diameter such as occurs in the giant axons of other invertebrates. The longitudinal axoplasmic resistance of shrimp nerve fibres is greatly lowered by the parallel conductance of the gel within the submyelinic space. This gel could provide the nerve fibres with some flexibility. A submyelinic space of this type has been found in nerve fibres of nine species of the Penaeus shrimp and is the third strategy adopted by nature for increasing the conduction velocity in nerve fibres. (4) The conduction velocities of the medial giant fibres were 80–200 m s⁻¹ in P. chinensis (Fan et al., 1961) and 90–210 m s⁻¹ in P. japonicus (Kusano, 1966). The values vary because of the wide range of sizes of shrimps used and because, once nerve fibres have been myelinated, the number of nodes becomes stabilized. The factors contributing to the extreme rapidity of impulse conduction are: (i) myelination with long internodal distances, (ii) a wide submyelinic space with low electrical resistance, and (iii) the rapid kinetics of activation and inactivation of the Na⁺ current. The efficiency of impulse conduction in the shrimp giant nerve fibres, however, may not be as high as in warm-blooded vertebrates.