Abstract
The hindbrain and spinal cord can produce multiple forms of locomotion, escape, and withdrawal behaviors and (in limbed vertebrates) site-specific scratching. Until recently, the prevailing view was that the same classes of central nervous system neurons generate multiple kinds of movements, either through reconfiguration of a single, shared network or through an increase in the number of neurons recruited within each class. The mechanisms involved in selecting and generating different motor patterns have recently been explored in detail in some non-mammalian, vertebrate model systems. Work on the hatchling Xenopus tadpole, the larval zebrafish, and the adult turtle has now revealed that distinct kinds of motor patterns are actually selected and generated by combinations of multifunctional and specialized spinal interneurons. Multifunctional interneurons may form a core, multipurpose circuit that generates elements of coordinated motor output utilized in multiple behaviors, such as left-right alternation. But, in addition, specialized spinal interneurons including separate glutamatergic and glycinergic classes are selectively activated during specific patterns: escape-withdrawal, swimming and struggling in tadpoles and zebrafish, and limb withdrawal and scratching in turtles. These specialized neurons can contribute by changing the way central pattern generator (CPG) activity is initiated and by altering CPG composition and operation. The combined use of multifunctional and specialized neurons is now established as a principle of organization across a range of vertebrates. Future research may reveal common patterns of multifunctionality and specialization among interneurons controlling diverse movements and whether similar mechanisms exist in higher-order brain circuits that select among a wider array of complex movements.
Highlights
Cellular and network mechanisms of behavioral choice or motor pattern selection are best understood for several invertebrate model systems containing a relatively small number of individually identifiable neurons (Morton and Chiel, 1994; Marder and Calabrese, 1996; Kupfermann and Weiss, 2001; Marder and Bucher, 2001; Marder et al, 2005; Katz and Hooper, 2007; Briggman and Kristan, 2008)
Mechanisms of motor pattern selection have been explored in some detail in the hindbrain and/or spinal cord of primarily three model systems: hatchling Xenopus tadpoles, larval zebrafish, and adult turtles
The predominant view in the literature was that the same classes of vertebrate central nervous system (CNS) neurons can generate multiple, distinct kinds of movements, through either a reconfiguration of a single, shared circuit or through an increase in the number of neurons recruited within each identifiable class of neurons (Jankowska et al, 1967; Berkinblit et al, 1978; Lundberg, 1979; Grillner, 1981, 1985; Robertson et al, 1985; Carter and Smith, 1986; Bekoff et al, 1987; Gelfand et al, 1988; Pearson, 1993; Soffe, 1993, 1996; Berkowitz and Stein, 1994b; Green and Soffe, 1996; Johnston and Bekoff, 1996; Svoboda and Fetcho, 1996; Earhart and Stein, 2000a; Juranek and Currie, 2000; Lieske et al, 2000; Marder, 2000; Berkowitz, 2001b; Marder and Bucher, 2001)
Summary
Cellular and network mechanisms of behavioral choice or motor pattern selection are best understood for several invertebrate model systems containing a relatively small number of individually identifiable neurons (Morton and Chiel, 1994; Marder and Calabrese, 1996; Kupfermann and Weiss, 2001; Marder and Bucher, 2001; Marder et al, 2005; Katz and Hooper, 2007; Briggman and Kristan, 2008). Studies on these model systems have focused on the motor patterns underlying short-latency escape or withdrawal responses and forward swimming in all three animals, struggling in tadpoles and zebrafish, and three forms of scratching in turtles.
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