1 General Information
A C. elegans male has 385 neurons
compared to 302 in the hermaphrodite. The majority of male-specific neurons are associated with the male tail and are involved in the complex mating behavior. The male mating circuitry contains 170 neurons (81 male-specific and 89 shared neurons) and 64 muscles. There are five modules in this circuitry; one involved in the response to hermaphrodite contact, one for locomotion, two for posture and one for insemination (Jarrell et al., 2012). The specific function of most male-specific neurons is still unknown. Adding to the complexity is that a lot of the male-specific neurons are polymodal and also two thirds of shared neurons show sexually dimorphic wiring pattern. In addition to the ganglia found in hermaphrodite tail (2 lumbar, 1 dorsorectal and 1 pre-anal), the mail tail contains a cloacal ganglion (MaleNeuroFIG 1).
MaleNeuroFIG 1: Mail tail ganglia. Left Panel: Male C. elegans has two male-specific ganglia (CG) in addition to the shared ganglia with the hermaphrodite. CG: cloacal ganglion; DNC: dorsal nerve cord; DRG: dorsal root ganglion; LG: lumbar ganglion; PAG: preanal ganglion; VNC: ventral nerve cord. Right panel: Placement of the ganglia in relation to the tail muscles. Bottom panel: TEM showing cross sections of lumbar ganglia (LG), cloacal ganglia (CG) and preanal ganglion (PAG). Inset indicates section level along the tail of the male (Image source: N2Y [MRC] N2YLP41-print 119)(for muscle nomenclature refer to MaleMusTABLE 1)
Four extra male-specific sensory neurons in the head (CEMs) are born in the embryo, and may provide some, yet unknown, male-specific behaviors during larval life. These cells undergo programmed cell death in the hermaphrodite embryo.
Most male-specific neurons, however, are born during the L3 and L4 stages during which time they also grow out axons and dendrites (Sulston et al., 1980; also refer to Individual Neurons). Two extra male-specific neurons (MCMs) are born in the head in the L4 stage and are daughters of the AMso glial cells. These two glial cells re-enter the cell cycle during early L4 stage to each produce an extra daughter cell that immediately transdifferentiates into an MCM neuron, while the other daughter retains the AMso cell function. These two interneurons have recently been shown to be essential for a sex-specific behavior, which is operational only in the adult male, called associative sexual conditioning (Sakai et al., 2013; Sammut et al., 2015). Most male-specific behaviors only begin to emerge at the beginning of the adult stage, after a major re-wiring of the nervous system during the late L4 stage. In particular, the male tail sensors and sex muscles are first activated just after the 4th larval molt. The young adult male’s ability to mate may improve over the first day of adulthood as its adult wiring becomes perfected. Whether those changes involve trial and error, perhaps to reinforce the most useful synaptic connectivity, has not yet been demonstrated.
Besides male mating behavior (MaleNeuroFIG 2; MaleNeuroFIG 3), which is controlled by the specialized cells and circuits of the male tail, the adult male also demonstrates a few other sex-specific behaviors, such as “leaving behavior” by which the animal can follow pheromone signals to find a potential mate (Lipton et al., 2004; Kleemann et al., 2008; Barrios et al., 2008). The male adult will choose to “leave” a food source to follow a pheromone signal only when the animal is well nourished. Control of this behavior is likely governed principally by the nerve ring, including the male-specific circuits there. Perception of the hermaphrodite’s secreted pheromones is accomplished by several sensory neurons in the male head, including the CEMs (Sakai et al., 2013; White et al., 2007; Chasnov et al., 2007; Srinivasan et al., 2008). During this behavior, animal generally moves forward to track the pheromone signal using forward locomotion circuitry. The MCM interneurons operate just downstream from these sense cells in the male head, with all synaptic interactions in the nerve ring and anterior ventral cord (Sammut et al., 2015). However, once the male finds a potential mate, all subsequent steps in mating are likely controlled by the synaptic connectivity involving the specialized neurons and muscles in the male tail; when the male makes a close approach to a mate going forwards, it halts and switches to moving backwards while attempting to mate (Emmons, 2006; Barrios et al., 2008; Jarrell et al., 2012). These backwards motions utilize synaptic connectivity that is concentrated in the pre-anal and lumbar ganglia of the male tail.
2 Support Cells of the Male Sensilla
Sensory structures that differ in the male can be divided into two types: male-specific and sexually dimorphic. Male-specific sensory organs have no homologs in the hermaphrodite and are formed by cell types generated only in the male. Sexually dimorphic sense organs contain at least some cells that have the same lineal origin in both sexes. These sensilla are considered sexually dimorphic because they express distinct differentiated characteristics in the two sexes, reflected in cell morphology, cell contacts or organization.
Four types of male-specific sensory organs are located in the copulatory apparatus of the tail: the sensory rays, the hook, the post-cloacal sensilla (PCS) and the spicules (MaleNeuroFIG 2). These sensilla have been shown to function in specific steps of male mating behavior (MaleNeuroFIG 3; Sulston et al., 1980; Loer and Kenyon, 1993; Liu and Sternberg, 1995; Barr and Sternberg, 1999; Garcia et al, 2001).
MaleNeuroFIG 2: Mating modules and male-specific sensilla of the tail. Left panel: neuronal modules for each step of mating behavior. Right panel: SEM of adult male tail, oblique view. (Image source: SEM [Hall] 434 H07_22.)
MaleNeuroFIG 3: Roles of sensilla in male mating behavior. (Based on Loer and Kenyon, 1993; Liu and Sternberg, 1995.)
With the exception of the rays, male sensilla contain interfacial cells of two types: sheath cells and socket cells (MaleNeuroFIG 4). In contrast to the sensilla of the head, which are common to both sexes, the number of non-neuronal cells can be between 1 and 3 (in the head there are invariably 2) (Sulston et al., 1980). Sheath cells wrap around the neuron ending forming a protective pocket and are linked to the neuron by adherens junctions (AJ). Its close proximity to the neuron, together with the the presence of numerous secretory vesicles, suggest that sheath cells are functionally analogous to glial cells in other organisms. The neurons, as in sense organs elsewhere in the animal, are ciliated. In many the axoneme of the cilia is associated with a transition zone (TZ) and some cilia also contain a striated rootlet (SR) extending proximally. The socket cell acts as a transitional cell that is linked both to the sheath and to the adjacent hyp by adherens junctions. Sheath and socket cells are often connected by gap junctions indicating that there is cell-cell communication between these cell types.
MaleNeuroFIG 4: Post-cloacal sensillum. Diagram showing typical organization of sensory organ cells, longitudinal view. (SR) Striated rootlet; (TZ) transition zone; (AJ) adherens junction; (Hd) hemidesmosomes. (Based on Sulston et al., 1980.)
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