Elsevier

Progress in Neurobiology

Volume 76, Issue 5, August 2005, Pages 279-327
Progress in Neurobiology

Neuronal control of leech behavior

https://doi.org/10.1016/j.pneurobio.2005.09.004Get rights and content

Abstract

The medicinal leech has served as an important experimental preparation for neuroscience research since the late 19th century. Initial anatomical and developmental studies dating back more than 100 years ago were followed by behavioral and electrophysiological investigations in the first half of the 20th century. More recently, intense studies of the neuronal mechanisms underlying leech movements have resulted in detailed descriptions of six behaviors described in this review; namely, heartbeat, local bending, shortening, swimming, crawling, and feeding. Neuroethological studies in leeches are particularly tractable because the CNS is distributed and metameric, with only 400 identifiable, mostly paired neurons in segmental ganglia. An interesting, yet limited, set of discrete movements allows students of leech behavior not only to describe the underlying neuronal circuits, but also interactions among circuits and behaviors. This review provides descriptions of six behaviors including their origins within neuronal circuits, their modification by feedback loops and neuromodulators, and interactions between circuits underlying with these behaviors.

Introduction

The major goal of neurobiology is to understand how the brain works: how it senses the external world and internal states, how it processes this sensory input, how it evaluates different inputs to select an appropriate motor act, and how it generates that behavior. One approach to studying these questions is to study the function of a particular neural structure (e.g. the superior colliculus or the habenular nucleus) in a complex brain and ask how it works. Another approach is to select a behavior and ask how the properties of neurons and their interconnections produce that behavior. The latter approach is the more direct, but is possible only in animals with relatively simple nervous systems, or in selected parts of complex nervous systems with neurons that are identifiable from animal to animal. For example, behavioral circuits have been described in a number of such animals: mollusks (Arshavsky et al., 1998, Satterlie et al., 2000, Brembs et al., 2002, Dembrow et al., 2003, Sakurai and Katz, 2003, Jing and Gillette, 2003, Staras et al., 1999, Bristol et al., 2004), crustaceans (Selverston et al., 2000, Teshiba et al., 2001, Prinz et al., 2003, Beenhakker et al., 2004), insects (Sasaki and Burrows, 2003, Wang et al., 2003, Riley et al., 2003, Wilson et al., 2004, Daly et al., 2004), amphibians (Roberts et al., 1999, Combes et al., 2004), fish (Higashijima et al., 2003, Grillner, 2003), and rodents (Sekirnjak et al., 2003, Kiehn and Butt, 2003, Yvert et al., 2004).

Rhythmic movements such as chewing, respiratory movements, locomotory movements, and, in some animals, heartbeat are of particular interest because of their combination of complex dynamics and relative stereotypy (Marder and Calabrese, 1996, Stein et al., 1997, Orlovsky et al., 1999). Oscillatory networks of central neurons are important components of most such motor pattern-generating networks. The anatomical wiring and synaptic connectivity within a network is the backbone on which intrinsic and synaptic properties of component neurons operate to produce network dynamics. The states of these intrinsic and synaptic properties are themselves dynamic, being subject to modulation through a multiplicity of sensory inputs provided by neurons extrinsic and intrinsic to the network (Katz, 1995, Harris-Warrick et al., 1997, Nusbaum et al., 1997).

A very useful animal for establishing the neuronal bases of behaviors has been the leech, particularly the European medicinal leech, Hirudo medicinalis. In this animal, more behaviors have been studied in neuronal terms than in any other. This review provides an overview of all the behaviors that have been studied, and an update of less comprehensive but more detailed reviews that have appeared elsewhere (Brodfuehrer et al., 1995b, Calabrese et al., 1995, Kristan et al., 1995). There is always the possibility that the neuronal mechanisms found in a particular animal will be unique to that animal, due to its specific evolutionary history and individual peculiarities of anatomy and biomechanics. We, however, believe the opposite: that there are general strategies for producing behaviors that will be found in all animals with a central nervous system (CNS).

There are many technical reasons why the medicinal leech is an auspicious animal for identifying behaviorally relevant neuronal systems. Some of the reasons are generally true of simple animals, and others are true of the leech in particular. It is worth enumerating the list to indicate why the medicinal leech has been so useful in studying the neuronal bases of behaviors:

  • 1.

    The leech nervous system is relatively simple (Fig. 1A) and readily accessible even while the animal is behaving in a variety of semi-intact preparations (Fig. 1B), making it possible to relate motor patterns directly to behaviors.

  • 2.

    Quite accurate representations of all the behaviors, or at least their rudiments, can be elicited in isolated nerve cords (Fig. 1B), where intracellular and optical recording is more favorable.

  • 3.

    The neurons are easily seen and readily identified, based on the location of their somata (Fig. 1C), morphology (Fig. 1D), and physiological properties.

  • 4.

    Intracellular neuronal activity can be recorded readily because the somata are relatively large (10–80 μm) and every soma is visible in segmental ganglia. These properties also make optical recording feasible.

  • 5.

    Long, easily accessible peripheral nerves allow for stimulation of selected neurons and monitoring of neuronal activity with extracellular electrodes.

  • 6.

    Most relevant electrical parameters can be measured. Intracellular recordings from somata reveal relatively large, individual synaptic potentials, which are not greatly attenuated from their origins in the neuropil, and attenuated action potentials.

  • 7.

    The nervous system is iterated, with homologous neurons found in most, if not all, 21 segmental ganglia (Fig. 1). So despite having more than 10,000 neurons, the functional unit (i.e. the number of different kinds of neurons) of the leech CNS is relatively small. For instance, there are only 400 neurons per segmental ganglion (Macagno, 1980), and most of these are paired. Thus, in essence, the segmental nerve cord (roughly corresponding to the spinal cord in vertebrates) consists of 42 copies (one on each side of 21 segments) of a basic unit of 200 neurons.

  • 8.

    Most neurons in the CNS are unique rather than members of functionally identical clusters, hence activating or ablating single neurons (irreversibly by killing or reversibly by hyperpolarization) often has behaviorally detectable consequences.

Because of these favorable features, it is possible, in principle, to identify every neuron that contributes substantially to any leech behavior. In practice, this task is far from trivial, so that no single behavior has yet been completely characterized. In no other system, however, have so many behaviors been investigated and described at the neuronal circuit level. This review is intended to provide a brief overview of the state of what is known, and what remains to be known about the most completely described behaviors. To understand these descriptions, background information concerning basic leech anatomy and electrophysiology is essential. After this introduction, the neuronal circuits underlying six different behaviors are discussed individually, followed by a discussion of how these circuits interact. A final section provides a vision of how the leech may prove useful for future research.

Leeches are annelids, all of which are segmented worms (Fig. 1A). Unlike most other annelids, leeches have a fixed number of segments – 32 – plus an anterior non-segmental region called the prostomium. The segments form as a repeated iteration of divisions of the same stem cells, whereas the prostomium is derived from a different set of stem cells (Stent et al., 1992). The prostomium and the most anterior four segments form the head and the most posterior seven segments form the tail. There are a variety of specializations in the head and tail, the most striking of which are the suckers. The mouth is in the middle of the front sucker, whereas the anus is located in the body wall anterior and dorsal to the posterior sucker. At rest, the posterior sucker is usually attached to the substrate. The anterior end is used to explore the environment, so that the anterior sucker is typically attached only when the leech is crawling or feeding. The body is a tube formed by epidermis and muscles, which encases the internal organs: the gut and intestines, the nephridia and urinary sacs, the reproductive organs, and the blood vessels (Fig. 2A). The circulatory system of a leech is closed, with four major longitudinal blood vessels that run the length of the leech and a mesh of circumferentially directed vessels connecting them. The dorsal and ventral longitudinal vessels are passive (they function as veins) and the lateral tubes are contractile (they function as hearts).

The leech CNS consists of a ventral nerve cord with a brain at each end (Fig. 1A). Each segment contains a single ganglion, which communicates with the adjacent anterior and posterior ganglia via three connectives (a pair of large lateral connectives and a smaller medial connective, known as Faivre's Nerve). The four anterior ganglia fuse during embryogenesis to form a subesophageal ganglion, and a supraesophageal ganglion forms within the prostomium. The borders of these individual ganglia are visible in the adult. The neuronal compartments of the four ganglia are called neuromeres. Together, the supraesophageal and subesophageal ganglia form the anterior brain (sometimes called the head brain). Similarly, the last seven ganglia in the chain fuse embryonically to form the posterior brain (also called the tail brain). The neuromeres in the anterior brain are denoted as R1–4 (rostral neuromeres 1–4), those in the posterior brain are C1–7 (caudal neuromeres 1–7), and the individual, mid-body ganglia are labeled M1–M21.

Neuronal somata within the CNS are roughly spherical, and are located on the surface of segmental ganglia and terminal brains. In midbody ganglia, somata are in 10 clusters – four on the dorsal surface and six on the ventral surface – delineated by giant glial cells that effectively engulf the somata of dozens of neurons. In fact, modern-day characterization of the function of leech neurons began with a series of elegant studies by Stephen Kuffler and his colleagues using these giant glial cells to study the electrical properties and potential functions of glia (Kuffler and Potter, 1964, Nicholls and Kuffler, 1964). They concluded that the membranes of these glial cells are nearly perfect K+ electrodes, and that their contributions to the electrical function of the nervous system is to sequester K+ ions released by active neurons in order to buffer the effects of local release of the K+. These giant glial cells, therefore, gather the neuronal somata into packets, with the lateral edges serving as packet margins that provide useful markers for identifying neurons. The ventral surface of a typical midbody ganglion is shown in Fig. 1C. Most or all of the leech central neurons are identifiable from animal-to-animal and segment-to-segment on the bases of the size and location of their somata within a cluster, as well as their characteristic electrophysiological properties and morphological features (Muller et al., 1981).

All neurons in the leech CNS are monopolar: a single process extends from each soma. Typically, this process gives rise to one or more axons that leave the ganglion, via nerves to the periphery in the case of sensory and motor neurons (MNs), and via the connectives in the case of interneurons (INs) and some sensory and secretory neurons. Secondary branches emerge from the main process; these side branches may subdivide to generate many orders of branching (Fig. 1D). Synaptic connections are made primarily on these fine branches.

All the ganglionic MNs that send axons via segmental nerves to muscles in the body wall (Stuart, 1970, Ort et al., 1974, Norris and Calabrese, 1987) and to the lateral heart tubes (Thompson and Stent, 1976a) are located within the CNS. The muscles used by the leech to make overt movements are of four types: longitudinal, circular, oblique, and dorsoventral (Fig. 2B). Contractions of each of these muscles produce characteristic types of movements: longitudinal muscle contractions produce shortening, circular muscle contractions produce a reduction in cross-section and elongation, oblique muscle contractions cause stiffening at an intermediate body length, and dorsoventral muscle contractions cause a flattening of the body and contribute to elongation. Each MN connects to a single muscle type, and only to muscle fibers on either the left or right side of its own segment, and then only to a regional subset of muscle fibers. For instance, MNs – both excitatory and inhibitory – that project to longitudinal muscles, innervate either dorsal, dorsolateral, lateral, ventrolateral, ventral, or dorsolateroventral regions (Stuart, 1970). The excitatory neuromuscular transmitter is ACh (Sargent, 1977) and the inhibitory transmitter is GABA (Cline, 1986). Activity of various combinations of these MNs in different temporal patterns produce the behaviors described in subsequent sections.

Leeches have a variety of sensory receptors. For instance, there are light-sensitive receptors in the sensilla located in each segment and in the eyes (a pair of expanded sensilla located on the lateral edge of each of the first five segments) (Kretz et al., 1976); chemoreceptors, in placodes on the upper lip (Elliott, 1987); stretch receptors, embedded in the dorsal, lateral, and ventral body wall of each segment (Blackshaw et al., 1982, Blackshaw and Thompson, 1988, Blackshaw, 1993, Cang et al., 2001); and mechanoreceptors of different sorts. There are ciliated mechano-receptive neurons whose somata are in the sensilla (DeRosa and Friesen, 1981, Phillips and Friesen, 1982) and respond to movements of the water (Brodfuehrer and Friesen, 1984). There are also mechanoreceptors with somata in the CNS (Nicholls and Baylor, 1968) that have free nerve endings in the skin (Blackshaw, 1981) and respond to different intensities of stimulation to the skin: light touch (T cells), pressure (P cells), and noxious stimuli (N cells). These neurons have primary receptive fields within their own segment, and secondary ones (via axons through connectives) in the adjacent ganglia both anterior and posterior. There are three pairs of T cells and two pairs of P cells. The receptive fields of these cells divide up the body wall into roughly equal, overlapping receptive fields around the circumference of the animal. There are two pairs of N cells in each ganglion, each of which innervates half the ipsilateral body wall. All the N cells respond to noxious mechanical stimuli, but the two on each side differ in their responses to other stimuli, such as heat and low pH (Pastor et al., 1996).

The great majority of the neuronal somata within the leech CNS, as in other animals, are neither sensory nor MNs; rather they are INs without direct connection to the periphery. These INs were identified largely by methodically searching for neurons associated with specific behaviors. For example, specific neurons were identified when intracellular current injection evoked (or terminated) a behavior in either semi-intact preparations, or fictive behavior in the isolated CNS. Using this technique, INs were found that participate in seven behaviors: heartbeat (Thompson and Stent, 1976b), local bend (Lockery and Kristan, 1990b), shortening (Shaw and Kristan, 1995), swimming (Friesen et al., 1978, Weeks, 1982a, Weeks, 1982b, Weeks, 1982c, Friesen, 1985, Friesen, 1989b, Brodfuehrer and Friesen, 1986a, Brodfuehrer and Friesen, 1986b, Brodfuehrer and Friesen, 1986e), crawling (Eisenhart et al., 2000), reproduction (Zipser, 1979) and feeding (Zhang et al., 2000). It is largely true that homologs of each of the neurons found in one ganglion can be found in the remaining 20 segments. There are exceptions to this general rule, which are pointed out in the sections below. In addition, homologs of the Retzius neurons (Lent, 1977) and several mechanosensory neurons (Yau, 1976) have been found in the neuromeres of the subesophageal ganglion, although many of the INs in the subesophageal ganglion do not appear to have homologs in the segmental ganglia (Brodfuehrer and Friesen, 1986a, Brodfuehrer and Friesen, 1986b, Brodfuehrer and Friesen, 1986c, Brodfuehrer and Friesen, 1986e). This ability to identify a particular neuron in segment after segment and in animal after animal has greatly aided the characterization of neuronal circuits. In addition, this stereotypy has led to the notion that all neurons within the leech CNS are unique (with the possible exception of the PE cells (Baptista and Macagno, 1988), neurons that develop post-embryonically in the ganglia of segments 5 and 6, which are the reproductive segments of leeches).

The leech was developed as a neurophysiological preparation in the 1930's by Gray et al. (1938), who studied the neuronal bases of leech swimming and crawling. The first intracellular recordings were accomplished in the early 1960's, when Hagiwara and Morita (1962) and Eckert (1963) recorded intracellularly from the somata of the paired Retzius neurons in segmental ganglia of Hirudo. They both showed convincingly that these neurons are strongly electrically coupled. They also demonstrated that at least two of the neurons in each ganglion were identifiable by the location and size of their somata, as well as their electrophysiological properties. The identification and characterization of leech neurons advanced greatly when John Nicholls chose to identify neurons that had been used in the laboratory of Stephen Kuffler to characterize the electrophysiological properties of glial cells and their effects on the electrical function of neurons (Kuffler and Potter, 1964). The Nicholls lab identified mechanosensory neurons (Nicholls and Baylor, 1968) and MNs (Stuart, 1970) in stereotyped locations within each segmental ganglion. They showed that these sensory neurons made both electrical and chemical synaptic connections onto the MNs, and also established a number of physiological techniques to suggest strongly that these connections were direct, monosynaptic contacts, without any intervening INs (Nicholls and Purves, 1970). Subsequently, several other MNs have been identified (Ort et al., 1974, Thompson and Stent, 1976a; Sawada et al., 1976, Norris and Calabrese, 1987). Many of these MNs are inhibitory (Stuart, 1970, Sawada et al., 1976, Ort et al., 1974), releasing GABA onto muscle fibers to hyperpolarize them and cause their relaxation (Cline, 1986). Surprisingly, at least some of the inhibitory MNs also make strong central connections, with both excitatory and inhibitory MNs (Ort et al., 1974, Granzow et al., 1985, Granzow and Kristan, 1986, Friesen, 1989a), and with INs (Friesen, 1989b).

Leeches perform a variety of distinguishable behaviors by combinations of lengthening, shortening, and bending. Fig. 3 shows five of these behaviors: local bending, swimming, whole-body shortening, crawling, and feeding. Each behavior is produced by a characteristic temporal and spatial pattern of muscle contractions. The nature of these motor patterns is discussed below, in individual sections devoted to each of the behaviors.

Leeches have no hard, fixed skeleton. Instead, they use a muscular arrangement that has been termed a “muscular-hydrostat” (Kier and Smith, 1985) or a “hydroskeleton” (Kristan et al., 2000). The leech body is a tube whose shape is controlled by muscles in each segment. To a first approximation, each segment is a cylinder with an ovoid cross-section (Fig. 2B); a segment maintains roughly the same volume during all behaviors. The muscles used to produce the behaviors shown in Fig. 3 are the longitudinal and circular layers in the body wall, plus the dorsoventral muscles that span the body cavity. Contraction of one muscle type changes the shape of the cylinder by increasing internal pressure, stretching the other muscle types. Hence, each of these three muscle types is potentially an antagonist for the other two sets of muscles. The body stiffness, which acts like a skeleton, is caused by co-contraction of antagonistic muscles or, for some behaviors, by contraction of a fourth set of muscles, the oblique muscles. These latter, thin muscles, which lie between the longitudinal and circular muscles, are oriented obliquely, so that their contraction stiffens the body at an intermediate body length – the posture seen in a leech at rest. In effect, leeches have a degree of freedom not available to skeletized animals: they can control the stiffness of their skeleton dynamically during a behavior. A single segment can perform four types of basic movements:

  • (1)

    bending, by contracting the longitudinal muscles on one side; the longitudinal muscles on the opposite side may also relax;

  • (2)

    shortening, by contracting all longitudinal muscles at the same time;

  • (3)

    elongation, by contracting the circular muscles and

  • (4)

    flattening, by contracting the dorsoventral muscles. (Note that flattening also produces elongation).

The first four behaviors illustrated in Fig. 3 are caused by different temporal and spatial patterns of these segmental movement units. Local bending (Fig. 3A) occurs in a small number of adjacent segments (1). Whole-body shortening (Fig. 3C) takes place in the whole animal almost simultaneously (2). In swimming (Fig. 3B), flattening of the whole body (4) is maintained throughout swimming episodes, and serves to stiffen the body and present a wide surface to the water. During swimming, each segment alternately bends dorsally and ventrally, with each segment producing the same movement as its more anterior neighbor at a phase delay of about 5%. This produces a repeated up-and-down undulation with about one peak and one trough in the body at any given time (Kristan et al., 1974a). Crawling (Fig. 3D) is also an oscillatory locomotory pattern, but in this case shortening (2) alternates with elongation (3) in each segment. Again, whatever occurs in a given segment is repeated in the next segment with a delay of about 5% of the cycle period. Compared to swimming, crawling cycles are slow: swim cycles are 0.4–2.0 s in duration (Kristan et al., 1974a, Kristan et al., 1974b, Kristan and Calabrese, 1976), whereas crawling cycles are 2–20 s in duration (Stern-Tomlinson et al., 1986, Cacciatore et al., 2000). The action of the suckers is important in shortening and crawling, but very little is known about their muscular or neuronal control. The typical feeding posture (Fig. 3E) is with one or both suckers attached. The jaws evert through the front sucker, rasp a hole in the skin of the prey, and blood is sucked through the oral opening in this sucker. Specialized internal muscles in the pharynx produce the suction that brings the blood into the body, but longitudinal muscles produce a peristalsis that moves blood into the various chamber of the gut (Wilson and Kleinhaus, 2000).

Section snippets

Circulation and heartbeat

Heartbeat is an autonomic function that is rhythmic and continuous in Hirudo medicinalis. The circulatory system is a closed network comprising four longitudinal vessels – one dorsal, one ventral, and two lateral – that run the length of the animal, communicating in every segment by a series of branched vessels (Fig. 2A). Rhythmic constrictions of the muscular lateral vessels (the heart tubes) drive the flow of blood through the closed circulatory system (Thompson and Stent, 1976a). The heart

Conclusion

This overview of the neuronal mechanisms underlying six distinct behaviors in the medicinal leech illuminates the utility of this animal for gaining insights into rhythmic movements, sensory feedback, neuromodulatory control, interactions among behaviors, and behavioral choice. The gaps in our understanding of the biophysical and developmental bases of these behaviors, in the face of so much existing information, make the leech a prime contender for further study. With the function of about

Acknowledgements

Funding was provided by NIH grants MH43396 and NS35336, and a grant from Microsoft Research Labs (to WBK); NSF grant IBN-0110607 and NIH grant NIMH-MH63855 (to WOF); and NIH grant NS24072 (to RLC). We express our deep gratitude to numerous students and colleagues who collaborated with us over a span of more than three decades. Without their expert and active participation in the research described here, this review would have been much shorter. We are especially grateful to Prof. Gunther Stent,

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