Neuronal Control of Leech Behavior William B

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Neuronal Control of Leech Behavior William B Progress in Neurobiology 76 (2005) 279–327 www.elsevier.com/locate/pneurobio Neuronal control of leech behavior William B. Kristan Jr.a, Ronald L. Calabrese b, W. Otto Friesen c,* a Section of Neurobiology, Division of Biological Sciences, 9500 Gilman Dr., University of California, San Diego, La Jolla, CA 92093-0357, USA b Department of Biology, Emory University, 1510 Clifton Road, Atlanta, GA 30322, USA c Department of Biology, Gilmer Hall, University of Virginia, P.O. Box 400328, Charlottesville, VA 22904-4328, USA Received 7 April 2005; received in revised form 23 August 2005; accepted 26 September 2005 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. # 2005 Elsevier Ltd. All rights reserved. Keywords: Elemental oscillators; Interneurons; Serotonin Contents 1. Introduction . ................................................................................ 280 1.1. Anatomy and electrophysiology ............................................................... 282 1.2. The hydroskeleton and behaviors . ........................................................... 284 2. Circulation and heartbeat ........................................................................ 285 2.1. The heartbeat neural control system of the leech ................................................... 286 2.2. The elemental oscillators. ................................................................... 286 2.3. Mechanisms of oscillation in an elemental half-center oscillator . ...................................... 286 2.4. Coordination in the beat timing network . ....................................................... 287 2.5. Heartbeat motor pattern switching by switch interneurons . .......................................... 288 2.6. Gaps in our current knowledge ............................................................... 290 3. Overt behaviors . ............................................................................ 290 3.1. Introduction . ............................................................................ 290 3.2. Local bending . ........................................................................ 290 3.2.1. Motor neurons . ................................................................... 290 3.2.2. Mechanosensory neurons that produce local bending .......................................... 293 3.2.3. Local bend interneurons . ........................................................... 293 3.2.4. The local bend response as a directed behavior .............................................. 295 3.2.5. Gaps in our current knowledge . ....................................................... 295 * Corresponding author. Tel.: +1 434 982 5493; fax: +1 434 982 5626. E-mail address: [email protected] (W.O. Friesen). 0301-0082/$ – see front matter # 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.pneurobio.2005.09.004 280 W.B. Kristan Jr. et al. / Progress in Neurobiology 76 (2005) 279–327 3.3. Shortening .............................................................................. 296 3.3.1. Whole-body shortening . ............................................................. 296 3.3.2. Local shortening. ................................................................. 296 3.3.3. Gaps in our knowledge . ............................................................. 297 3.4. Swimming .............................................................................. 298 3.4.1. History: reflex chain versus central pattern generator . ........................................ 298 3.4.2. Swimming behavior and motor control . ................................................. 298 3.4.3. Central oscillator circuits. ............................................................. 300 3.4.4. Control of swimming activity . ......................................................... 300 3.4.5. Neuromodulatory control: serotonin and other biogenic amines . ................................ 302 3.4.6. Role of sensory feedback ............................................................. 304 3.4.7. Functional aspects of the central oscillator ................................................. 306 3.4.8. Gaps in our current knowledge ......................................................... 308 3.5. Vermiform crawling . ..................................................................... 308 3.5.1. Behavior ......................................................................... 308 3.5.2. Kinematics . ..................................................................... 309 3.5.3. Motor neuron activity . ............................................................. 309 3.5.4. Sensory input. ..................................................................... 309 3.5.5. Models .......................................................................... 311 3.5.6. Initiation of crawling . ............................................................. 312 3.5.7. Gaps in our current knowledge ......................................................... 313 3.6. Feeding . .............................................................................. 313 3.6.1. Behavior ......................................................................... 313 3.6.2. Chemosensation . ................................................................. 314 3.6.3. Motor patterns ..................................................................... 314 3.6.4. Regulation and plasticity . ............................................................. 314 3.6.5. Gaps in our knowledge . ............................................................. 314 3.7. Interactions among behaviors................................................................. 315 3.8. Methodologies and approaches for further research ................................................. 316 3.8.1. Functional indicator dyes ............................................................. 316 3.8.2. Modeling......................................................................... 318 3.8.3. Plasticity ......................................................................... 318 3.8.4. Development . ..................................................................... 319 4. Conclusion .................................................................................. 319 Acknowledgements . .......................................................................... 320 References .................................................................................. 320 1. Introduction Teshiba et al., 2001; Prinz et al., 2003; Beenhakker et al., 2004), insects (Sasaki and Burrows, 2003; Wang et al., 2003; The major goal of neurobiology is to understand how Riley et al., 2003; Wilson et al., 2004; Daly et al., 2004), the brain works: how it senses the external world and internal amphibians (Roberts et al., 1999; Combes et al., 2004), fish states, how it processes this sensory input, how it evaluates (Higashijima et al., 2003; Grillner, 2003), and rodents different inputs to select an appropriate motor act, and how it (Sekirnjak et al., 2003; Kiehn and Butt, 2003; Yvert et al., generates that behavior. Oneapproachtostudyingthese 2004). questions is to study the function of a particular neural Rhythmic movements such as chewing, respiratory structure (e.g. the superior colliculus or the habenular movements, locomotory movements, and, in some animals, nucleus) in a complex brain and ask how it works. Another heartbeat are of particular interest because of their approach is to select a behavior and ask how the properties combination of complex dynamics and relative stereotypy of neurons and their interconnections produce that behavior. (Marder and Calabrese, 1996; Stein et al., 1997; Orlovsky The latter approach is the more direct, but is possible only et al., 1999). Oscillatory networks of central neurons in animals with relatively simple nervous systems, or in are important components of most such motor pattern- selected parts of complex nervous systems with neurons that generating networks. The anatomical wiring and synaptic are identifiable from animal to animal. For example, connectivity within a network is the backbone on which behavioral circuits have been described in a number of such intrinsic and synaptic properties of component neurons animals: mollusks (Arshavsky et al., 1998; Satterlie et al., operate to produce network dynamics. The states of these 2000; Brembs et al., 2002; Dembrow et al., 2003; Sakurai intrinsic and synaptic
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