Spicule muscles: the retractors, protractors and anal depressor -Gubernacular muscles -Oblique muscles -The Sphincter muscle - Cell list - Muscle of the Male Part I -Back to Contents
The male copulatory spicules are associated with three sets of muscles (MaleMusFIG15A, 15B): (1) the dorsal and ventral spicule retractor muscles, dsrL/R and vsrL/R; (2) the spicule protractor muscles, dspL/R and vspL/R; (3) the anal depressor, adp. The retractor and protractor muscles are male-specific and are generated post-embryonically by the M lineage. The anal depressor is a sexually dimorphic muscle, present in both sexes but specialized in the male to function as an auxillary spicule muscle (Sulston et al., 1980; see MUSCLES OF THE MALE - Part I).
Two retractor muscles, one dorsal (dsrL/R) and one ventral (vsrL/R), attach to the base of each spicule. At their opposite ends the muscles attach to the sublateral body wall (MaleMusFIG15B, 16A, 16C ; Sulston et al., 1980). Each muscle contains a single sarcomere that occupies most of the cell. The myofilaments run A/P and so contraction of these muscles pulls the spicules inside the body.
At their body wall end (MaleMusFIG17A), dorsal and ventral retractors of a side are in direct contact for some distance along their length and are coupled by extensive gap junctions (MaleMusFIG17B, 17F). In addition the dorsal retractors form gap junctions with dorsal body wall muscles (dBWM, MaleMusFIG17C, 17F ; Sulston J.E., Albertson, D.G. and Thomson J. N., unpublished). The identity of neurons that innervate the spicule retractors is not yet known.
At the spicule end of the muscle (MaleMusFIG17D), muscle::spicule attachment sites appear analogous to those observed between non-striated muscles and body wall cuticle. Hemidesomosomes (Hds) connect the muscle to the basal lamina, which in turn is connected to proctodeal epithelium. Proctodeal epithelium is attached to spicule cuticle (Sulston J.E., Albertson, D.G. and Thomson J. N., unpublished). These retractor muscle::spicule attachments do not appear to be as numerous or as tightly localized as those observed between protractor muscle and spicule (compare MaleMusFIG17E with MaleMusFIG19B).
In addition to regulation of adult spicule behavior, the retractor muscles have a developmental role and are required for proper anterodorsal elongation of the proctodeum during development. In males that lack retractor muscles (or M) the proctodeum fails to elongate and its internal structures, the spicules and gubernaculum, are compressed (Sulston et al., 1980). During wild type larval development cells on the dorsal surface of the proctodeum insert "fingers" into the nearby retractor muscles. During male tail morphogenesis (late L4) anterior movement of the muscles (carried by the general forward movement of the body wall) draws out the proctodeum, the spicules and gubernaculum (Sulston et al., 1980).
2. Spicule protractor muscles
Two protractor muscles (one dorsal dspL/R; one ventral, vspL/R) are attached to the base of each spicule (MaleMusFIG18A, 18B; Sulston et al., 1980). These muscles, particularly the dorsal protractors, have large cell bodies. Each muscle contains a single sarcomere with myofilaments that run in the A/P orientation. The sarcomere is concentrated in the region of the muscle that overlaps with the spicules (MaleMusFIG18C). At their anterior edges, the dsp L/R are attached to the dorsal sublateral body wall and at their posterior edge to the anal depressor (adp). The vspL/R are attached to the ventral sublateral body wall (MaleMusFIG15B). Contraction of the protractors therefore has the opposite affect to retractor contraction and causes the spicules to extrude from the body.
The protractor muscles are connected to the spicules via a series of hemidesmosomes (Hds) that interconnect muscle, basal lamina, proctodeum and spicule cuticle (MaleMusFIG19A,19B; red arrows). Attachment plaques link spicule muscles to each other: dorsal protractors to ventral protractors and dorsal protractors to anal depressor (MaleMusFIG19B; yellow arrows).
The protractor muscles are directly innverated by neurons SPCL/R (MaleMusFIG20A, 20C; Sulston et al., 1980). The SPCL/R neurons have both sensory (proprioceptive/mechanosensory) and motor neuron function. Their sensory endings are directly attached to the dorsal protractor muscles via hemidesmosomes (MaleMusFIG19B, 20A,20B; Male Wiring Project). SPCL/R form numerous neuromuscular junctions (NMJs) with both dorsal and ventral muscles and a few with the anal depressor (Male Wiring Project). Interestingly, these synapses are not on muscle arms but on the main body of the muscle that contains the sarcomere (MaleMusFIG20C). Muscle activity is also regulated by the post-cloacal sensilla (PCS) neurons although this may be indirect as PCS neurons do not appear to synapse with spicule muscles (Male Wiring Project). SPCL/R and PCS neurons control different aspects of spicule behavior: PCS neurons, detecting the presence of the vulva, induce periodic contraction of the muscles which causes the spicules to prod the hermaphrodite surface for the vulval opening; SPCL/R stimulate prolonged contraction which causes the spicules to extrude fully and insert into the vulva once the opening is located. Both the PCS neurons and SPCL/R regulate muscle activity through release of acetylcholine. The gonad also influences the behavior of these muscles as its presence is required for maintaining prolonged muscle contraction so that spicules remain fully inserted during sperm transfer (Garcia et al., 2001; see MOVIE of spicule behavior below by L. Rene Garcia)
The protractors and anal depressor are not only physically connected to each other and regulated by common neurons, they are also coupled electrically. The dspL/R and vspL/R muscles of each side are connected by gap junctions (MaleMusFIG20B,20C); dspL and dspR, in turn, are electrically coupled to the anal depressor (MaleMusFIG20B,20D; Sulston J.E., Albertson, D.G. and Thomson J. N., unpublished). Electrical coupling in this way likely facilitates coordinated contraction of the spicule muscle.
Click to view MOVIE of Periodic vs Prolonged Spicule Muscle Contraction (by L. Rene Garcia)
3. The anal depressor muscle
As described in MUSCLES OF THE MALE - Part I, the anal depressor muscle (adp) is a sexually dimorphic muscle. In males, instead of participating in defecation, it functions as an auxillary spicule protractor muscle (MaleMusFIG20A, 20D; Sulston et al., 1980; Garcia et al., 2001). The muscle contains a single sarcomere with myofilaments oriented the same direction as the dspL/R i.e. A/P. Along its ventral edges the adp is attached to the proctodeum/gubernaculum and to the ventral body wall. Dorsally it retains some connections sublaterally to the dorsal roof (MaleMusFIG20A). Where adp and the dspL/R overlap there are extensive regions of gap junctions (MaleMusFIG20D; Sulston J.E., Albertson, D.G. and Thomson J. N., unpublished).
Two bilateral pairs of sex-specific muscles are attached to the gubernaculum: (1) the gubernacular erectors (gecL/R) and (2) the gubernacular retractors (grtL/R) (MaleMusFIG21A,21B; Sulston et al., 1980). The gubernaculum is a thick sclerotic strip of cuticle that lines the roof of the cloaca and is thought to guide the movement of spicules ventrally through the anus (described in detail in THE PROCTODEUM - EPITHELIAL SYSTEM OF THE MALE, PARTIII; Sulston et al., 1980). Both muscle types contain a single sarcomere with myofilaments oriented dorsoventrally.
1. Gubernacular erector muscles
The gubernacular erectors (gecR/L) attach at their ventral edges to the gubernaculum and cloacal roof (MaleMusFIG22). At their dorsal edge these muscles attach to the dorsal sublateral body wall.
The gubernacular erectors (gecL/R) are innervated on their muscle arms by 2 of the PCS (post-cloacal sensilla) neurons, PCAL/R and the left PCB neuron, PCBL (MaleMusFIG23A,23B; Male Wiring Project). After the PCS and/or hook detect the approximate location of the vulva, PCS neurons trigger spicule prodding behavior which is used to pinpoint the vulval opening (Liu and Sternberg, 1995; Garcia et al., 2001). At this time the gubernaculum twitches possibly due to PCS neuron-stimulated contraction of the gec muscles.
2. Gubernacular retractor muscles
The gubernacular retractor (grtL/R) muscles attach at their ventral edges to the gubernaculum and overlying proctodeal epithelium. At their dorsal edges the muscles attach to the sublateral dorsal body wall, immediately below the lateral seam (called the set cell in this region in the male) (MaleMusFIG24A, 24B). The neurons that innervate the gubernacular retractors have not yet been identified.
Two bilateral pairs of sex-specific (M-derived) oblique muscles are located in the anal region of the adult male tail; an anterior pair (aobL/R) and a posterior pair (pobL/R) (MaleMusFIG25,26; Sulston et al., 1980). These muscles contain a single sarcomere oriented dorsoventrally. At their dorsal edge, the muscles attach to the body wall, immediately below the set cell; along their ventral edge the muscles attach ventral body wall.
Anterior and posterior oblique muscles on each side receive synaptic inputs from all three post-cloacal sensillum (PCS) neurons, namely PCAL/R, PCBL/R and PCCL/R (Male Wiring Project). Synapses are located on muscle arms that project from the muscle cell body and run with PCS neuron processes as they descend towards the left or right sensillum (MaleMusFIG28A,28B; Sulston J.E., Albertson, D.G. and Thomson J. N., unpublished). As mentioned above, the PCS neurons trigger spicule muscle contraction in response to a vulval cue (Liu and Sternberg, 1995; Garcia et al., 2001). PCS neuron-stimulated shortening of the oblique muscles possibly changes the posture of the tail during the execution of this and downstream steps in mating (spicule prodding, spicule insertion and sperm transfer).
As described in MUSCLES OF THE MALE - Part I, the sphincter (sph), like the anal depressor, is a sexually dimorphic muscle, common to both sexes but modified during male larval development.
In the adult male the alimentary tract and reproductive tract are joined to a common chamber, the cloaca, which opens to the environment at the anus (described in detail in THE PROCTODEUM - EPITHELIAL SYSTEM OF THE MALE, PARTIII). In contrast to the hermaphrodite anus, the male cloaca is constitutively open presumably to permit free movement of the spicules (housed within) and sperm during mating behavior. The principal seal for the male alimentary tract is instead at the sphincter.
The male sphincter is tonically contracted and must be relaxed (through inhibitory GABA transmission) during defecation. This response to GABA is opposite to that observed in larval males and in adult hermaphrodites and may reflect a change in receptor expression in the muscle (Reiner and Thomas, 1995). The male sphincter also differs morphologically from larval male and hermaphrodite sphincters. It is enlarged (hypertrophied) but still contains a single sarcomere. It has a dorsal process that attaches to the dorsal roof and that contains myofilaments. Thus hyper-contraction of the sphincter during ejaculation not only clamps off the intestine but also draw it away from the vas deferens, possibly allowing sperm to pass more freely (Sulston et al., 1980).
Diagonal (dgl) muscles of the adult:
Ventral longitudinal muscles of the adult
1- Outer longitudinal
SM3R.aap (polR, posterior outer longitudinal, right)
SM3R.aaa (aolR, anterior outer longitudinal, right)
SM3L.aap (polL, posterior outer longitudinal, left )
SM3L.aaa (aolL, anterior outer longitudinal, left)
2. Inner longitudinal
SM3R.app (pilR, posterior inner longitudinal, right)
SM3R.apa (ailR, anterior inner longitudinal, right)
SM3L.app (pilL, posterior inner longitudinal, left)
SM3L.apa (ailL, anterior inner longitudinal, left)
3. Caudal longitudinal
SM3R.pp (cdlR, right)
SM3L.pp (cdlL, left)
Spicule muscles of the adult
1. Spicule protractors
SM3R.pa (dspR, dorsal right)
SM1R.aaa (vspR, ventral right)
SM3L.pa (dspL, dorsal left)
SM1.aaa (vspL, ventral left)
2. Spicule retractors
SM2R.paa (dsrR, dorsal right)
SM1R.ppp (vsrR, ventral right)
SM1L.ppp (dsrL, dorsal left)
SM1L.ppa (vsrL, ventral left)
Gubernacular muscles of the adult
1. Gubernacular erectors
SM2R.pp (gecR, right)
SM2L.pap (gecL, left)
2. Gubernacular retractors
SM2R.apa (grtR, right)
SM2L.apa (grtL, left)
Oblique muscles of the adult
SM2R.pap (pobR, posterior right)
SM2R.app (aobR, anterior right)
SM2L.paa (pobL, posterior left)
SM2L.app (aobL, anterior left)
Anal Sphincter muscle
Anal depressor muscle
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