Control of Locomotion in Annelids
Abstract and Keywords
This article reviews the status of research on locomotion in segmented worms. It focuses on three major groups (leeches, earthworms, and nereid polychaetes) that have attracted the most research attention. All three groups show two types of locomotion: crawling (moving over a solid substrate) and swimming (moving through a liquid). The adults of all three groups form a hydroskeleton by controlling the pressure within the segments, and they locomote by controlling the shapes of the individual segments in coordinated spatial and temporal patterns. Many annelid larvae use cilia to move through water. Four aspects of the locomotory patterns are considered: the kinematics (the movement patterns), biomechanics (how muscle contractions produce movement), the neuronal basis of the movement patterns, and efforts to produce robots that move like annelid worms.
Until recently, “annelid” was synonymous with “segmented worm.” Recent developments in molecular phylogeny, however, make a strong case for the inclusion of nonsegmented worms into the annelid clade (Struck et al., 2011, 2015). Most of the research on annelid locomotory mechanisms have centered on just a few segmented worms: oligochaetes (earthworms), hirudinids (leeches), and polychaetes (a diverse group that includes both sessile and free-swimming worms). These segmented annelids produce three major forms of locomotion: crawling, swimming, and ciliary gliding. All three behaviors are rhythmic (they repeat at a fairly regular frequency) and they are metachronal (whatever activity happens in one segment now will happen in an adjacent segment after a delay, producing a wave of activity that passes either back to front or front to back); this metachrony propels the worm forward or, less commonly, backward. In crawling, the worm pushes a part of its body against an unmoving substrate to make progress. Crawling movements in different annelids may be peristaltic (elongation and contraction of segments along the long axis of the body), undulatory (either left/right or up/down body waves), or “inch-worming” (leeches use the front and back suckers to gain traction on a solid substrate). Swimming is produced by undulating the body, out of contact with the substrate, in metachonal waves that propel the worm forward through water. These undulations, like those in crawling, are either left/right or up/down in a given species. Ciliary gliding is produced by the coordinated movements of cilia on the surface of a larval worm, which is usually used to move the larva through a water column.
Many of the issues about annelid locomotion were laid out beautifully in a remarkable series of studies by Sir James Gray and his colleagues in the late 1930s, in which they described the kinematics (the movements) of the locomotory behaviors of the earthworm (Gray & Lissman, 1938), the leech (Gray et al., 1938), and the polychaete worm, Nereis (p. 452) (Gray, 1939). Since then, the biomechanics (patterns of muscle contractions and their interactions with the animal’s solid and/or fluid environment) have been studied extensively in earthworms (Seymour, 1970; Quillin, 1999; Kier, 2012; Tanaka et al., 2012; Dorgan, 2010, 2015), leeches (Wadepuhl & Beyn, 1989; Skierczynski et al., 1996; Kristan et al., 2000), and free-swimming polychaetes of the genus Nereis (Taylor, 1952; Clark & Tritton, 1970; Clark & Hermans, 1976). The neuronal basis of the various behaviors has been investigated primarily in the medicinal leech (Kristan et al., 2005; Wagenaar, 2015), to some extent in the earthworm (Mizutani et al., 2002, 2003, 2004; Shimoi et al., 2014), and not at all in adult polychaetes, although a bit is known about the anatomical neuronal circuitry for ciliary gliding in a larval polychaete (Martin, 1978; Jékely et al., 2008; Randel et al., 2014). For convenience, this chapter is divided into three major parts, based upon the three major annelids (leech, earthworm, and Nereis) that have been used most extensively to study locomotion. For each behavior in each animal, the order of presentation is kinematics, then biomechanics, followed by the neuronal circuitry that produces the spatial and temporal patterns of muscle contractions that generate the behavior. Interestingly, several robots have been developed based upon the biomechanics of both earthworms and polychaetes; examples will be discussed, emphasizing how the robots inform our knowledge of the biological locomotion.
In general, all soft-bodied animals need to stiffen their bodies to be able to make locomotory movements. Segmented annelids have a linear array of repeating segments that stiffen by co-contracting antagonistic muscles—generally longitudinal and circular muscles—around the outside of each segment (Gray & Lissman, 1938; Taylor, 1952; Kristan et al., 2000; Kier, 2012), which form the bulk of the body wall (Fig. 19.1A). Many earthworms and polychaetes have intersegmental septa that wall off each segment from its neighboring segments, with the space enclosed by the body wall and the septa filled with fluid (Seymour, 1969; Brusca & Brusca, 2003); this arrangement is called a hydrostatic skeleton. Other annelids (such as leeches, polychaetes, and some earthworms) do not have septa separating the segments. In some of these worms, the space is filled with fluid that can flow between segments; this arrangement is called a hydraulic system. If the space has minimal fluid, the worm can still produce body stiffness by clamping down on tissue inside the segment; this is called a muscular hydrostat (Kier, 2012). In looking at a worm moving about, it is difficult to tell which kind of “temporary skeleton”—hydrostatic, hydraulic, or muscular hydrostat—it is using to produce body stiffness, and there does not appear to be a qualitative advantage of one type of skeleton over the others, even though the hydrostats—both fluid and muscular—probably produce finer control of movements.
Studies of the neuronal basis of leech1 behaviors began with identification and characterization of the major mechanosensory (Nicholls & Baylor, 1968) and motor neurons (Stuart, 1970) in the leech segmental ganglion, as well as many of the synaptic connections among them (Nicholls & Purves, 1970). Using this basic knowledge, and modifying the type of semi-intact preparations suggested by Gray et al. (1938), the neuronal basis of leech swimming was characterized (Stent et al., 1978).
Medicinal leeches swim episodically, either when they are strongly stimulated or when they are out of contact with a solid substrate (Sawyer, 1981; Palmer et al., 2014). Typically, they swim until they run into something, which usually causes them to stop and attach to the object with their suckers (they have suckers at both ends). Agitated leeches will swim “spontaneously” in bouts (Willard, 1981). For instance, leeches put into a new tank will crawl and swim around the tank for tens of minutes before settling down (Bisson & Torre, 2011). Cutting the anterior brain away from the nerve cord produces much longer and more frequent episodes of swimming, a fact that is common knowledge among bass fisherman in the United States. This observation has both theoretical implications (the net effect of the anterior brain is inhibitory) and practical applications (cutting off the brain produces a semi-intact animal that readily swims [Gray et al., 1938; Kristan et al., 1974a]).
Kinematics of Leech Swimming
Leeches swim (Fig. 19.1B) by flattening dorsoventrally, then producing up-and-down undulations that start at the front end and progress smoothly backward along the animal, pushing backward on the water and thereby pushing the animal forward (Kristan et al., 1974a). The waves repeat at a frequency of 0.5 to 2 Hz, and there is always one peak and one trough in the body at all times, a body (p. 453) shape that optimizes the thrust produced by the metachronal waves (Taylor, 1952). The single body wave at all swimming frequencies means that the body wave passes through the 21 segments of the midbody from head-to-tail in nearly the same time that each up-and-down movement repeats (Kristan et al., 1974a). The thrust produced by this undulation is quite efficient: the stride length (the distance that the body moves forward per swim cycle) is about 40% of the body length per swim cycle (French et al., 2005).
Biomechanics of Leech Swimming
Gray et al. (1938) had postulated that alternating contractions of dorsal and ventral longitudinal muscles caused the up-and-down movements underlying the undulations. Using a semi-intact preparation (Fig. 19.1C) to record the tensions (p. 454) generated in these muscles during a swimming episode, Kristan et al. (1974b) showed that the Gray et al. postulations were correct: the dorsal and ventral longitudinal muscles do alternately generate tension during each cycle of the swimming movements (Fig. 19.1D). In addition, the motor neurons to these muscles produced burst of action potentials at just the times expected to produce the muscle contractions even if the nerves were disconnected from their muscles. Recording muscle contractions in several segments at once showed a normal front-to-back progression of the contractile waves, as did the motor neuronal bursts from cut ends of segmental nerves.
Neuronal Control of Leech Swimming
The neuronal basis of leech behaviors has been reviewed in detail in 2005 (Kristan et al., 2005), and with a later update on swimming (Friesen & Kristan, 2007). The following sections on leech locomotion provide a summary and updating of those reviews.
Gray et al. (1938) concluded, provisionally, that leech swimming undulations were produced by chained reflexes between the dorsal and ventral longitudinal muscle networks: dorsal contractions activated ventral muscle stretch receptors that led to ventral muscle contraction; the ventral muscle contractions dorsal muscle stretch receptors, leading to dorsal muscle contractions; and the cycle repeated. The alternative mechanism was that the nervous system could produce a neuronal activity pattern on its own, without any sensory feedback, a mechanism known as a central pattern generator (CPG). The ultimate test for this possibility was to obtain the swim motor activity pattern in an isolated nervous system, an experiment that Gray et al. (1938) tried but failed to obtain anything resembling the swim motor pattern. Slight modifications of both the dissection and the physiological saline produced an isolated leech nerve cord capable of producing a swimming motor pattern that is nearly identical to that seen in the semi-intact preparation (Kristan & Calabrese, 1976). This result both showed that leech swimming is generated by a CPG and provided a much more convenient preparation to search for the leech swimming circuitry. Using isolated leech nerve cords, the swimming pattern-generating neurons were found in all midbody segments (Friesen et al., 1976; Friesen et al., 1978; Poon et al., 1978) (Fig. 19.2A). Although their detailed interconnections are complex (Pearce & Friesen, 1985), the overall connections are relatively simple: CPG interneurons form three groups that (p. 455) are active at distinct phases, clustering around 0o, 120o, and 240o. As a whole, these three groups are mutually inhibitory: each group inhibits both of the other two groups and is inhibited by them (Kristan et al., 2005).
In seeking neurons that connected the CPG neurons from segment to segment to produce the metachronal coordination responsible for the undulation, there was a big surprise: many of the same CPG neurons sent an axon to the next ganglion (and maybe three or four beyond) to connect with the CPG interneurons in those ganglia (Friesen et al., 1978). The anteriorly projecting connections were homologous to the connections made in the neuron’s own ganglion, whereas the posteriorly projecting connections are more varied (Fig. 19.2B). This pattern of connections, in fact, assures that the swim pattern progresses in only one direction (front to back), so that leeches can swim only forward (Friesen et al., 1978; Cang & Friesen, 2002). Other animals can swim either forward or backward. Lamprey, for instance, also have segmentally repeating swim pattern generators, but the intersegmental connections between are symmetric anteriorly and posteriorly, allowing the lamprey to swim either forward or backward, depending upon whether they receive stimuli to the head or to the tail (Mullins et al., 2011a; Mullins et al., 2012).
Despite the fact that swimming is produced by a CPG, the leech has stretch receptors in the dorsal and ventral longitudinal muscles (Blackshaw & Thompson, 1988; Blackshaw, 1993) that have strong effects on the swimming pattern (Kristan & Stent, 1976; Cang & Friesen, 2000; Cang et al., 2001). Removing the stretch receptors has little effect on the swimming rate (intact swimming occurs at the same rate as the swimming motor patterns in an appropriated stimulated isolated nerve cord; Kristan & Calabrese, 1976), but the intersegmental coordination differs greatly in the two conditions: the intersegmental delays in the isolated nerve cord are shorter than in the intact animal (Yu et al., 1999). In addition, the intersegmental delays are constant in the isolated nerve cord, unlike the longer and variable delays in the intact animal, which serve to maintain a single wave in the animal at all swim frequencies (Cang & Friesen, 2002), a body form that is biomechanically optimal for producing maximal thrust with minimal upward/downward movement (Taylor, 1952; Humphrey et al., 2010; Chen et al., 2011a, 2011b). In addition, the stretch receptors have such strong effects on the segmental CPGs that they can coordinate the swim rhythm, as is most convincing evidenced by experiments in which the nerve cord was severed in the midbody. If one half of the leech was induced to swim, the swimming half usually did not induce the other half to swim, but if both halves were stimulated to swim, the two halves would synchronize so that the undulatory wave would pass smoothly from front to back (Yu et al., 1999; Yu & Friesen, 2004). These kinds of experiments showed that the pull exerted by the contractions in one segment can coordinate—but not initiate—the swim rhythm between the two halves of a leech.
Activation of Swimming
The normal stimulus to elicit leech swimming is mechanical stimulation of the posterior end (Palmer et al., 2014) that is sufficient to activate mechanosensory neurons responsive to touch (T cells) and pressure (P cells) (Kristan et al. 1982). Stimulating individual or pairs of T, P, or N mechanosensory neurons in an isolated nerve cord can elicit the swimming motor pattern (Debski & Friesen, 1987). Stimulating individual interneurons in midbody ganglia can also elicit swimming in an isolated nerve cord, a type of neuron that has been termed a command neuron (Kupfermann & Weiss, 1978). Two types of such neurons have been identified, distinguished by whether a short burst of their action potentials can initiate a swim (in which case, they are called trigger neurons; Brodfuehrer & Friesen, 1986a), or whether instead, the neuron must be activated continuously to maintain the swimming pattern (Weeks & Kristan, 1978; Weeks, 1981); these are called gating neurons (Brodfuehrer & Friesen, 1986a). Trigger neurons are found in the head brain, with axons that reach to all the segmental ganglia (Brodfuehrer & Friesen, 1986b), whereas the gating neurons are found in segmental ganglia, making connections to neurons in their own and other segmental ganglia (Weeks & Kristan, 1978). Trigger neurons connect to gating neurons (Nusbaum et al., 1987), as well as to pattern-generating and motor neurons (Brodfuehrer et al., 1995), whereas gating neurons connect only to pattern-generating neurons (Nusbaum et al., 1987) (Fig. 19.2C). Note that the only feedback connection is excitatory, from CPG neurons onto gating neurons, effectively a positive feedback that helps to maintain swimming once it begins (Friesen et al., 2011). In addition to the gating and trigger neurons in the anterior brain, there are other neurons in both the anterior and posterior brains that initiate, terminate, or otherwise affect the swimming (p. 456) motor program in isolated nerve cords (O’Gara & Friesen, 1995; Mullins et al., 2011b; Mullins & Friesen, 2012).
Modulation of Swimming
Leech swimming is strongly activated by serotonin, both when serotonin is injected into an intact animal or when it is applied to the saline bathing the isolated nerve cord (Willard, 1981). Serotonin is found in a small number of neurons in both the brains and the segmental ganglia of leeches (Lent, 1985; Nusbaum & Kristan, 1986). Some of the segmental serotonergic neurons make synaptic connections onto neurons of the central pattern generator (Nusbaum et al., 1987), but others release their serotonin into the extracellular space, and hence into the blood (Kristan & Nusbaum, 1983; DeMiguel & Trueta, 2005) to exert its effects hormonally. The effects of serotonin on the synapses both between motor neurons (Mangan et al, 1994a), between pattern-generating neurons (Mangan et al., 1994b), and on the electrical properties of a gating neuron (Angstadt & Friesen, 1993a,b) are consistent with making the segmental ganglia more likely to produce a robust swimming motor pattern. Interestingly, focal application of serotonin on the anterior brain makes swimming less likely (Crisp & Mesce, 2003), showing that serotonin is likely to affect circuitry in the anterior brain differently than in the segmental ganglia. This difference may be related to feeding behavior, because the segmental Retzius neurons are inhibited when the animal starts to feed (Wilson et al., 1996a; Zhang et al., 2000), and serotonin serves to presynaptically inhibit tactile stimuli from reaching their ganglionic targets during the time that the leech is feeding (Gaudry & Kristan, 2009). In contrast, octopamine activates swimming (Hashemzadeh-Gargari & Friesen, 1989; Crisp & Mesce, 2003), although the combination of the two swim-inducing modulators—serotonin plus octopamine—inhibits swimming (Mesce et al., 2001). On the other hand, dopamine application onto an isolated nerve cord makes it impossible to elicit swimming from a nerve cord (Crisp & Mesce, 2003). These results strongly suggest that serotonin has a variety of effects on different neurons in different behaviors, so that more focused delivery of serotonin will be required to sort out its specific effects.
Leeches crawl when they are searching—for food, for a mate, or for a place to hide—and in response to a mild touch to their posterior end (Sawyer, 1981; Palmer et al., 2016). Crawling is primarily a searching behavior, with many pauses, that makes forward progress more slowly than swimming (Stern-Tomlinson et al., 1986). Crawling is a universal behavior of leeches: every leech species crawls, but fewer than 30% of the species is capable of swimming (Sawyer, 1981).
Leeches crawl in one of two ways that have been termed “vermiform” (i.e., worm-like) and “inch-worming” (Sawyer, 1981; Stern-Tomlinson et al., 1986). Vermiform crawls begin—if the animal is on a smooth, hard surface—with both suckers attached and the body at nearly its minimal length (Fig. 19.3A). The anterior sucker releases its attachment and a wave of circular muscle contractions starts in the most anterior segments and then progresses posteriorly. When fully extended, the front sucker attaches and a wave of longitudinal muscle contractions ensue that also start at the front end and progress posteriorly. As the contraction wave nears the back end, the posterior sucker releases its hold on the substrate and then reattaches when the body is fully contracted, completing a single step. The stride length (the distance advanced in a single step) is the difference between the fully contracted and fully extended length, which is about 60% of the fully extended length. Leeches can, in fact, crawl along soft substrates like mud or sand, surfaces to which the suckers cannot attach. In such circumstances, the extended leech lays its front end on the surface and then starts the contraction wave from the front end, just as it would if the sucker had attached, using the front end as its point of contact, effectively its foot. As the contraction wave moves posteriorly, progressively more of the front end is contracted and lies on the surface, thereby providing more frictional surface area to keep the front end from sliding backward as the back end is pulled forward. In fact, as the longitudinal muscles contract, the annuli (the hundred or so circular bands around the leech’s body) are thrown into ridges by annulus erector muscles in the body wall, making the contracted part of the body even more resistant to sliding. As will be seen in the next section, crawling in earthworms is essentially identical to this nonsucker version of leech vermiform crawling.
The second mode of leech crawling, inch-worming (Fig. 19.3A), shows the same two phases of waves of circular muscle contractions (the extension phase) alternating with longitudinal muscle (p. 457) contraction (the contraction phase), but during the extension phase the body is lifted off the substrate and forms an inverted U-shape, with the back sucker brought up just behind the front sucker (Stern-Tomlinson et al., 1986). These steps are produced entirely by a sucker-to-sucker alternation, without a frictional contact between the midbody and the substrate. This form of crawling produces a significantly longer stride length—about 90% of the extended body length—but it repeats more slowly than vermiform steps so that the mean speed (measured in body lengths of progress per second) is not significantly different in the two crawling modes. In addition, the annuli do not erect during an inchworm step.
Left to itself in a water-filled chamber, particularly in a new one, a leech will often show “searching behavior”: with their posterior sucker attached, they extend their body and move the front end in an arc back and forth, to the right and to (p. 458) the left, mixed in with shortenings, in a seemingly random pattern (Garcia-Perez et al., 2005, 2007). Often, after performing several searching extensions in many directions, the leech will attach its front sucker and perform a single crawl step, and then start to search once again. It might perform several repetitions of the search/step/search sequence before it settles down, typically with both suckers attached to the substrate. In fact, a crawling episode is effectively a sequential series of these search/step/search combinations in which there is a single extension to search in each step. Interestingly, a leech can be diverted from crawling by a variety of stimuli. For example, they will retract vigorously to a touch delivered to the anterior end; they often swim in response to touching the posterior end (Palmer et al., 2014); and they are attracted to food-like chemicals (Gaudry & Kristan, 2012). Each of these distractions must, however, occur during the extension phase of the crawl cycle; the same stimuli delivered during the contraction phase of a step simply speeds up the contraction (Cacciatore et al., 2000). Leeches—particularly very hungry leeches—will crawl toward a disturbance in shallow water, using both mechanosensory and visual cues (Carlton & McVean, 1993; Harley et al., 2011; Harley & Wagenaar, 2014). The variety of effects caused by different sensory stimuli, as well as the kinds of crawl coordination produced after cutting away different numbers of segments in different parts of the leech (Baader & Kristan, 1995; Cacciatore et al., 2000), suggested strongly that crawling—particularly the extension phase of each crawl step—is generated by movement-initiated sensory feedback, without a CPG. This hypothesis turned out to be incorrect, as discussed next.
The contraction phase of crawling is caused by activation of all the longitudinal muscles in a segment—both dorsal and ventral (Gray et al., 1938)—and the elongation phase is caused by contraction of the circular muscles (Eisenhart et al., 2000; Kristan et al., 2000). Both sets of contractions begin at the anterior end of the body and sweep backward at a rate proportional to the step cycle period. Recordings of pressures from the body cavity of a crawling leech showed that the pressure in one segment can be quite different from that in nearby segments (Wilson et al., 1996c), which, together with the fact that there are no rigid septa separating leech segments, implies that the tensing of the body that allows whole-body movements is caused by a muscular hydrostat (Kristan et al., 2000; Kier, 2012). The pressures generated by the circular and longitudinal muscles, therefore, act on the mechanical properties of muscles, both static (Wilson et al., 1996b; Tian et al., 2007) and dynamic (Chen et al., 2012). The major difference between vermiform and inchworm crawling is that the ventral longitudinal muscles are active during the extension phase of crawling in inchworm crawling, which produces the inverted-U shape.
Neuronal Basis of Crawling
A semi-intact preparation was used to monitor the motor neuronal activity in the exposed nerve cord as the animal crawled, with both the front and back suckers sewn shut to keep the animal from pulling itself free from its restraints (Fig. 19.1C, 19.3B) (Eisenhart et al., 2000). As predicted by Gray et al. (1938), bursts of impulses in the longitudinal muscle motor neurons produce the shortening (contraction) phase of each step, and circular muscle contractions produce the elongations. Such recordings had previously been reported from crawling, semi-intact leeches (Baader & Kristan, 1995), but Eisenhart et al. (2000) also reported, for the first time, that an isolated nerve cord would produce a variant of the crawling motor pattern. The crawling motor pattern in the isolated nerve cord is typically an order of magnitude slower in the isolated nerve cord than in the intact leech (a step period lasts 10–30 seconds in the isolated nerve cord (Eisenhart et al., 2000) and 2–10 seconds in the intact leech (Stern-Tomlinson et al., 1986)), but the pattern is clearly crawling because the motor neuron pattern shows a regular alternation between burst of impulses in the longitudinal and circular motor neurons (Eisenhart et al., 2000). The crawl pattern produced by the isolated nerve cord is almost certainly vermiform because the annulus erector motor neurons, which would produce ridges in the skin of an intact leech, produce bursts of impulses during longitudinal muscle contraction, exactly the phase that they are active during vermiform (but not inchworm) crawling steps. In fact, this same motor neuronal coordination of longitudinal circular, and annulus erector motor bursts, can be elicited from an isolated single ganglion that is bathed with a leech saline containing a moderate dose of dopamine (Puhl & Mesce, 2008), showing that there is a crawling CPG in each segmental ganglion capable. Except for one pair of neurons found in a survey of leech neurons that are active during both swimming and crawling (Briggman & Kristan, (p. 459) 2006), very little is known about the neurons that constitute the crawling CPG.
As in the intact leech, the crawling motor pattern in the isolated nervous system begins at the anterior end and progresses backward in both the extension and contraction phases during each crawl step (Eisenhart et al., 2000). The progression of the front-to-back wave slows when the duration of the steps increases, with the elongation phase slowing more than the contraction phase (Cacciatore et al., 2000; Puhl & Mesce, 2010). This intersegmental progression requires activity of cells R3b1, a pair of neurons in the anterior brain, to produce an appropriately phased motor program in an isolated nerve cord (Puhl et al., 2012).
Initiation of Crawling
The same R3b1neurons have an unusual property: they can initiate either swimming or crawling. In an isolated nervous system, activating just one of them will turn on either swimming or crawling, and sometimes both behaviors on successive activations (Esch et al., 2002). In a semi-intact preparation, they produce swimming when the intact part of the leech (the posterior 80% of the animal) is in deep water. If it is in shallow water, stimulating R3b1 produces only crawling. Hence, this pair of neurons, each of which has an axon that runs the length of the nerve cord, produces a state-dependent effect on behavior: it always initiates locomotion, but which of the two locomotory responses is produced depends upon the kinds of sensory input the animal is receiving. (If R3b1 gets no sensory input, as in an isolated nervous system, its activation appears to randomly produce one behavior or the other.) Interestingly, one of the previously described swim trigger neurons (cell Tr1) in the leech anterior brain can also activate crawling (Brodfuehrer et al., 2008). Other identified neurons (R3b2 and R3b3) whose somata lie near R3b1 in the anterior brain modify the posture of the animal as it produces crawling (Mesce et al., 2008). Hence, the brain appears to initiate and modify whole-body responses, whereas the segmental ganglia produce the rhythmic contractions and elongations of their own segment, the movements that underlie the crawling movements.
The leech nervous system devotes a small number of neurons to neuromodulation. In addition to peptide modulators, the leech nervous system contains specific neurons that contain and release the biogenic amines serotonin, dopamine, and octopamine (used by many invertebrates in place of epinephrine or norepinephrine (David & Coulon, 1985; Gallo et al., 2016). Dopamine (DA) both inhibits swimming (Crisp & Mesce 2004) and initiates crawling in the whole animal, in the isolated nerve cord, and in single ganglia (Puhl & Mesce 2008). These results show that not only is there a CPG for leech crawling but also that a complete crawling CPG is present in each segmental ganglion. DA has an effect on motor neurons (Crisp et al., 2012), and activation of R3b1 (the brain neuron that activates either swimming or crawling) always produces the crawling motor pattern in an isolated nerve cord exposed to DA, thus biasing leech behavior toward crawling and away from swimming (Puhl et al., 2012). Interestingly, one of the effects of activity in cell R3b1 is to facilitate the intersegmental coordination of the crawl motor pattern (Crisp & Mesce, 2006). Transection of the nerve cord disrupts crawling posterior to the cut in an otherwise intact leech (Harley et al., 2015). Over the course of weeks, transected leeches regain their ability to produce coordinated crawling, with the ganglion just posterior to the transection apparently taking over some of the control mechanisms normally performed by the anterior brain.
Leech Swimming Versus Crawling to Tactile Stimulation
Leeches either crawl or swim in response to mechanosensory stimuli applied to the posterior third of the body (Palmer et al., 2014). Which behavior occurs depends upon the depth of the water (e.g., leeches never attempt to swim if the water level is shallower than their body thickness), the state of hunger (e.g., well-fed leeches never swim), and their neuromodulatory status (Willard, 1981; Hashemzadeh-Gargari & Friesen, 1989; Crisp & Mesce, 2003, 2006). A similar regional difference in response is seen in isolated nerve cords in response to stimulation of peripheral nerves (Briggman et al., 2005). Stimulating a single nerve containing just one neuron responsive to touch (T cell) and one responsive to pressure (P cell) produced either swimming or crawling, each about 50% of the time. Using voltage-sensitive dyes to record simultaneously from most of the neurons in one ganglion in such a preparation, it was possible to show that the earliest detectable signal that indicated which behavioral pattern the nerve cord would produce was a small change in the activity of many of the neurons in the ganglion, rather than a large change in the response (p. 460) of just one or a few neurons. Remarkably, it was possible to bias the behavior toward either swimming or crawling by depolarizing or hyperpolarizing just a single neuron. Similar kinds of multicellular signaling of behavioral choice has since been detected in monkeys (Mante et al., 2013; Shenoy et al., 2013) and in the nematode worm, C. elegans (Roberts et al., 2016). In fact, most of the neurons active in phase with the swimming motor pattern arealso active in phase with crawling (Briggman & Kristan, 2006), suggesting that the swimming circuit evolved from the crawling circuitry, which might explain why all leech species crawl but only about 30% of them swim (Sawyer, 1981).
Earthworm crawling behavior share many kinematic and biomechanical features with leech crawling (Gray & Lissman, 1938; Gray, 1939), but much less is known about the underlying neuronal basis of earthworm crawling.
Earthworm crawling is similar to leech vermiform crawling: waves of contraction and elongation begin in anterior segments and pass backward along the body that is in contact with a substrate (Fig. 19.4) (Gray & Lissman, 1938; Gardner, (p. 461) 1976; Quillin, 1999; Kier, 2012). The contracted region—typically three to eight segments—effectively forms a transient “foot” that is in contact with the substrate (Fig. 19.4a, b, c). The friction of the body-to-substrate contact is enhanced by chaetae, stiff hair-like bristles on the ventral surface of each segment. Tunnel-dwelling oligochaetes have chaetae all around each segment, whereas surface-dwellers tend to have chaetae only on their ventral surface.2 As more posterior segments contract, the anterior segments elongate, lifting those segments from the substrate and pushing the anterior end forward (Fig. 19.4d–f). As the first “foot” moves to more posterior segments, the anterior segments begin to contract, forming a second “foot” that itself progresses posteriorly (Fig. 19.4–i). In effect, each three-to-eight-segment-long “foot” moves backward along the body, pushing the body forward. There may be several (usually two or three) regions of contracted “feet” along the length of an earthworm at any given time. The forward progress made with each contraction-extension cycle is called the stride length, the duration of one stride is the stride period, and the rate at which new “feet” form (the inverse of the stride period) is the stride rate. The stride rate in earthworms (about 0.5 to 0.2 Hz on a favorable substrate) is about the same as in leeches (Stern-Tomlinson et al., 1986), but the stride length is much less: about 15% of the body length for earthworms (Quillin, 1999; Alexander, 2003) versus 60%–90% for leeches (Stern-Tomlinson et al., 1986). The wavelength (λ) is the number of segments between successive repeats of the same segmental behavior. In Figure 19.4, λ is 14 segments, but λ varies considerably with the stride rate (Gray & Lissman, 1938; Gardner, 1976).
Despite the similarities, earthworm and leech crawling have significant differences. Leeches do not have chaetae, for instance, but they do erect the annuli into ridges (Eisenhart et al., 2000) that serve the same friction-increasing function as do chaetae in earthworms. Another difference is that leeches never form more than one “foot” at a time, the way that earthworms do; instead, the contracted leech segments remain contracted until the leech body is fully contracted and a new elongation wave begins at the front end (Cacciatore et al., 2000). In general, compared to leeches, earthworms show a more local autonomy: the coordination of different regions of an earthworm can be quite variable (Gray & Lissman, 1938; Quillin, 1998; Kier, 2012), whereas both crawling and swimming in leeches are tightly coupled, whole-body behaviors (Kristan et al., 1974a; Kristan & Calabrese, 1976; Cacciatore et al., 2000). These differences may be related to the differences in numbers of segments between earthworms and leeches. All leeches species have 32 segments: 4 that form the head (including the anterior sucker), 7 that form the tail (mostly the tail sucker), and 21 repeated midbody segments. The head and tail ends of earthworms are not nearly as specialized as leeches (earthworms have no suckers, for instance), earthworms have a variable number of segments (they add segments throughout life), and they can regenerate segments (which leeches cannot). In a sense, the price that leeches pay for having the complex sucker structures at each end is a lack of the flexibility in being able to add and to regenerate new segments.
Not surprisingly, the muscle contraction patterns used by earthworms to crawl are similar to those used by leeches: the contractions are produced by longitudinal muscles around the circumference of the body wall, and elongation movements are produced by contractions of the circular muscles around the outside of the longitudinal muscle band (Gray & Lissman, 1938; Seymour, 1971; Quillin, 1999; Kier, 2012). Movements of earthworm segments are more localized than leech segments: many species of earthworms have septa separating each segment from the ones anterior and posterior to it, and each segmental cavity is filled with fluid that cannot move past the septa (Seymour, 1970; Chapman, 1975). This structural arrangement means that, when one set of muscles in a segment contracts, the other set is lengthened by pressure conveyed through the fluid within the segment, with very little effect on movements in neighboring segments. This type of interaction is called a hydrostatic skeleton (as opposed to a muscular hydrostat in leeches), because the stiffening of the segment and antagonistic movements within the segment depend upon pressure conveyed by the fluid within that segment (Kier, 2012).
Neuronal Basis of Earthworm Crawling
The nervous system of the earthworm is much harder to record than that of the leech because the neuronal somata in the earthworm are neither as large nor as reproducibly located as those of the leech (Gardner, 1976), and earthworm tissue is not as robust as those of the leech, so that semi-intact earthworm preparations are much more fragile. Studies, mostly on night crawler earthworms (Lumbricus terrestris), have characterized the (p. 462) anatomy (Mulloney, 1970), the inputs to (Günther, 1972; Gardner, 1976) and outputs from (Drewes, 1984) the giant fiber system (two lateral giant fibers [LGFs] and a single medial giant fiber [MGF]), which runs the length of the earthworm nerve cord and mediate fast shortening responses to touch and to light (Mill, 1982). In addition, the neuromuscular synaptic connections from motor neurons onto longitudinal muscles have been identified in Lumbricus (Drewes & Pax, 1974) and a Brazilian species, Amynthas hawayanus (Chang et al., 1998). The giant fibers, both MGF and LGF, are activated irregularly and infrequently during locomotion—not at a sufficiently high frequency to elicit a shortening response—suggesting that they are activated by sensory input generated by the crawling movements rather than helping to generate the crawling behavior (Drewes et al., 1978).
Applying micromolar concentrations of octopamine (OA) initiates a bursting motor pattern in the isolated nerve cord of the red wiggler earthworm, Eisenia fetida (Oka et al., 1994). This bursting pattern resembles the crawling motor pattern, both in its cycle period (Shimoi et al., 2014) and in its front-to-back progression (Mizutani et al., 2002), indicating that there is a CPG for crawling in the earthworm nerve cord. The body wall in a semi-intact earthworm provides sensory feedback onto the crawling pattern generator (Mizutani et al. 2004). A series of studies using fluorescent dyes, both voltage-sensitive (Oka et al., 1994) and synaptic activity-specific (Shimizu et al., 1999), have identified synapses (Mizutani et al., 2003) as well as some neurons that oscillate in phase with the crawling motor pattern (Shimoi et al., 2014). These studies hold promise that the neuronal circuitry for earthworm crawling can be determined using a combination of electrophysiological and optical imaging techniques.
It is likely that earthworm burrowing behaviors use the same motor patterns as crawling, although there are differences depending upon the size of the worm (Kurth & Kier, 2014) and the nature of the burrow that is produced (Quillin, 2000; Kurth & Kier, 2015). For instance, night crawlers (Lumbricus terrestris) make extensive, rigid tunnels deep into hard-packed soil, whereas red wiggler worms (Eisenia foetida) crawl through leaf litter and loose soil near the surface of the ground. Burrowing earthworms produce their tunnels by greatly elongating their anterior end, which they push into small chinks in the structure of the soil, and then expand their diameter greatly by producing a strong circular-muscle contraction, comparable to forming a “foot” (Dorgan, 2010, 2015; Dorgan et al., 2016). Surface-dwelling earthworms produce much longer body shapes and weaker contractions as they move through their more compliant substrate.
Most earthworms do not swim, but there are some exceptions. One of these is Dero digitata, a small (less than 1 inch long) freshwater oligochaete that makes remarkable helical swimming movements when suspended in water and touched on its posterior end (Drewes & Fourtner, 1993). D. digitata forms a helical coil in its front end by coordinated contractions of muscles in the front-most segments (Fig. 19.5) and then moves the coil metachronally backward through successive body segments, pushing back against the water to move the animal forward. The stride length is a moderate 30%–50% of the body length, and these worms move through the water quite fast because the strides (p. 463) repeat at 6–12 per second. The helix can begin as either right-handed or left-handed, but it strictly alternates with each successive cycle. From the kinematics, the muscle contraction patterns are inferred (a coordinated pattern of ventral, dorsal, and lateral longitudinal muscle contractions), but no electrophysiological recordings have been performed on these small worms.
Several versions of segmented, worm-like robots have been fabricated that can be used to test theories of the biomechanics of individual segments (Daltorio et al., 2013; Kim et al., 2013) as well as the optimal intersegmental phase patterns to produce forward progress (Fang et al., 2015). An added feature of studying robots is that their fabrication can uncover functional explanations for animal movements that were unexpected. For instance, a biomechanical model of a crawling earthworm misestimated the total energy needed to move an earthworm forward because it assumed that the entire ventral surface of the animal remained in contact with the substrate, producing a large frictional impediment to forward movement (Alexander, 2003). A robotic version of an earthworm (Daltorio et al., 2013) found that the elongated segments between the “feet” were not in touch with the substrate and produced very little resistance to movement. Earthworm-like robots are being developed to be able to move through such varied—and inacessible—places as underwater environments (Vaidyanathan et al., 2000), pipes of varying diameter (Daltorio et al., 2013), and even in the human colon (Wang et al., 2009). Hence, building biologically inspired robots can both address basic conceptual ideas and potentially produce practical applications.
Polychaetes are a diverse, paraphyletic group of mostly aquatic worms, largely marine: fewer than 200 of the estimated 10,000 species live in fresh water. Many species are sedentary as adults, dwelling in tubes or tunnels, so they do not locomote, per se, although they do move around in their tubes. Other species, such as Nereis (Fig. 19.6A), roam widely as adults. Although they can swim—albeit poorly (Brusca & Brusca, 2003)—these adults mostly locomote by crawling (Gray, 1939). Very few electrophysiological recordings have been obtained in polychaetes, and none since the 1960s. Those early studies were concerned with the giant fiber system (Horridge, 1959), neuromuscular summation (Wilson, 1960), and visual processing (Gwilliam, 1969).
Nereis Crawling and Swimming
The family of nereid worms (Nereidida) contains some 500 species that have many segments (up to 200), most of which bear a pair of fleshy lateral parapodia with bristles (chaetae) extending from them (Fig. 19.6A). Nereid worms crawl and swim using the same basic activity pattern: a metachronal wave of lateral contractions that—unlike leeches and earthworms—begins at the back end and moves forward along the body, using both the ventral surface and the parapodia as resistive anchors to push the body forward (Gray, 1939) (Fig. 19.6B). Because the intersegmental progress is slow relative to the cycle period, there are several waves in the body at once. At faster step speeds, a distinct lateral bend is apparent at the sites of the anchors. These bends are caused by contractions of longitudinal muscles on the short side of the active segment and relaxation on the long side. If sufficiently provoked, the crawling speeds up, the progression of the waves through the body speeds up even more, so that there are fewer waves in the body at any given time, and the waves become larger in amplitude (Fig. 19.6C). Enough thrust is produced by these more vigorous body movements that these worms, if in sufficiently deep water, can lift off the solid substrate and swim.
At the slowest crawling speeds, polychaetes may use mainly their parapodia to crawl (“slow crawl” in Fig. 19.6C), with waves of parapodial contraction moving from the back end to the front. The waves are well coordinated: several adjacent parapodia on a side are contracting at once, with the left and right parapodia in a segment contract out of phase with one another. At higher crawling speeds, larger side-to-side undulations are produced that are coordinated with the parapodial contractions (“fast crawl” in Fig. 19.6C). When stimulated mechanically while moving, crawling can blend smoothly into swimming movements, with the side-to-side undulations becoming larger and their number in the body becoming fewer (“swim” in Fig. 19.6C). In a few polychaete species, the side-to-side swimming movements start in the front and progress backward (front-to-back metachrony), which provides a more efficient means of locomotion than the more typical back-to-front coordination mode (Clark & Hermans, 1976).
The original kinematic analysis of nereid locomotion (Gray, 1939) pointed out that the back-to-front (p. 464) body wave would produce a backward movement in both crawling and swimming if these worms did not have parapodia. An early biomechanical analysis (Taylor, 1952) concluded that Nereis could make forward progress during swimming even with completely passive parapodia: having these appendages protruding from the sides could create a backward thrust of the parapodia against the water and propel the worm forward, however inefficiently. A later analysis showed that the species of Nereis analyzed in this early study was atypical: most nereid species would not make forward swimming progress unless the parapodia produced a backward thrust when they are at the peak of the lateral bend (Clark & Tritton, 1970). The parapodia do have flexor and extensor muscles (Brusca & Brusca, 2003) and the parapodia do—in kinematic studies—appear to contract (Gray, 1939; Merz & Edwards, 1998), but there have been no recordings from parapodial muscles or motor neurons to confirm this impression. Some of these species even have jointed chaetae that make the parapodial swimming strokes more efficient (Merz & Edwards, 1998).
Like earthworms, nereid worms use crawling movements to make burrows in both sand and mud (Dorgan, 2010), although the detailed dynamics differ in different species (Francoeur & Dorgan, 2014; Dorgan et al., 2016). The forces to both (p. 465) fracture the substrate and plastically deform it are generated by the same longitudinal and circular muscles, used in the same patterns as in locomotion. Additional behaviors used in burrowing (e.g., side-to-side movements of the head) are matched to the anatomy of the anterior end of the species, the strengths of their muscles, and the substrate being penetrated (Dorgan et al., 2016).
A robot that mimics basic polychaete anatomy (i.e., segments that can elongate and shorten, with laterally projecting parapodia that can generate force) provides an interesting way to test differences between earthworm and nereid locomotion (Sfakiotakis & Tsakiris, 2009). For instance, a robot worm without parapodia (earthworm-like) moves on a sandy surface best using a back-to-front coordination of segments, whereas a front-to-back coordination works best for a robot with parapodia on the same surface. These kinds of robotic studies, therefore, enable experiments that are impossible to do on biological animals.
Although many polychaetes are sessile as adults, they do have free-swimming larval stages. The larvae swim by coordinated beating of cilia, usually located in clusters of epithelial cells located in specific regions of the body (Jékely, 2011). The larva of the polychaete worm Platynereis dumerilii (Fig. 19.7) has become a favored animal for evolutionary and developmental studies (Tessmar-Raible et al., 2005; Raible & Tessmar-Raible, 2014). Because these larvae are so small, their nervous systems are not amenable to electrophysiological recording, but behavioral circuits have been determined using serial EM reconstruction (Randel et al., 2014); for instance, the circuitry responsible for swimming toward light has been characterized (Jékely et al., 2008; Randel et al., 2014, 2015). Larvae develop four eyes: a pair of larval eyespots, each with just a single photoreceptor, and a pair of adult eyes, each having two to seven photoreceptors (Randle et al., 2014).
Two rows of cilia around the larval head beat in synchrony to move the animal through the water. The photoreceptors connect both directly and through interneurons to ciliary effector cells that control the direction of the ciliary power stroke to produce movement either toward or away from light (phototaxis), the direction presumably determined by other sensory or modulatory factors. The cilia move the larval body in a spiral path, which modeling studies suggest is optimal for avoiding blind spots or nondirected movements (Jékely et al., 2008). These animals may serve as useful models for studying the functional and evolutionary mechanisms that control coordinated ciliary movements in other animals, including humans (Jékely, 2011). The feasibility of a ciliated robot of the approximate size of P. dumerilii (a few hundred microns) has been suggested (Ghanbari & Bahrami, 2011), but it has not been fabricated because the mechanism for driving the cilia is a major hurdle.
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(1.) Throughout, the animal will be called “the leech,” but most of the work discussed was performed on the European medicinal leech. Until 2007, the experimental subject was called Hirudo medicinalis, until Mark Siddall and his colleagues gave convincing evidence that most of these studies used the closely related species, Hirudo verbana (Siddall et al., 2007). In fact, most commercially supplied medicinal leeches from Europe are H. verbana, but some shipments do contain true H. medicinalis. The laboratories that work on the neuronal basis of leech locomotory behaviors have not found a difference between the two species, so fortunately, the previous research on the “European medicinal leech” is equally valid whichever species was actually used.
(2.) The terms “chaete” and “setae” are used synonymously for these bristles in annelids, but “chaetae” is the more preferred term for these structures in oligochaetes and polychaetes.