The Construction of Movement with Behavior-Specific and Behavior-Independent Modules

Abstract

Growing evidence suggests that different forms of complex motor acts are constructed through flexible combinations of a small number of modules in interneuronal networks. It remains to be established, however, whether a module simply controls groups of muscles and functions as a computational unit for use in multiple behaviors (behavior independent) or whether a module controls multiple salient features that define one behavior and is used primarily for that behavior (behavior specific). We used the Aplysia feeding motor network to examine the two proposals by studying the functions of identifiable interneurons. We identified three types of motor programs that resemble three types of behaviors that Aplysia produce: biting, swallowing, and rejection. Two ingestive programs (biting, swallowing) are defined by two movement parameters of the feeding apparatus (the radula): one is the same in both programs (phasing of radula closure motoneurons relative to radula protraction-retraction), whereas the other parameter (protraction duration) is different in the two programs. In each program, these two parameters were specified together by an individual neuron, but the neurons in each were different (B40 for biting, B30 for swallowing). These findings support the existence of behavior-specific modules. Furthermore, neuron B51 was found to mediate a phase that can be flexibly added on to both ingestive and egestive-rejection programs, suggesting that B51 may be a behavior-independent module. The functional interpretation of the role played by these modules is supported by the patterns of synaptic connectivity that they make. Thus, both behavior-specific and behavior-independent modules are used to construct complex behaviors.

Spinal Interneurons That Are Selectively Activated during Fictive Flexion Reflex

“…The current results and other recent findings (Svoboda and Fetcho, 1996 2005) suggest that generation of several types of vertebrate hindlimb motor patterns may be mediated by a combination of shared and specialized circuitry, as has been seen in more numerous and detailed studies in invertebrates (Morton and Chiel, 1994;Marder and Calabrese, 1996;Kristan and Shaw, 1997;Edwards et al, 1999;Kupfermann and Weiss, 2001;Jing et al, 2004;Briggman et al, 2005;Marder et al, 2005;Briggman and Kristan, 2006). Moreover, the current results and a recent study in zebrafish (Ritter et al, 2001) both suggest that these shared and specialized subsets of spinal interneurons may to some extent be morphologically distinguishable.…”

“…Cellular mechanisms of behavioral choice are best understood for several invertebrate systems, in which many CNS neurons contribute to multiple behaviors, whereas others are dedicated to just one (Morton and Chiel, 1994;Marder and Calabrese, 1996;Kristan and Shaw, 1997;Edwards et al, 1999;Kupfermann and Weiss, 2001;Jing et al, 2004;Briggman et al, 2005;Marder et al, 2005;Briggman and Kristan, 2006). In some cases, CNS neurons dedicated to one behavior inhibit CNS neurons dedicated to another behavior.…”

Neuromechanics of Coordination during Swallowing inAplysia californica

“…Previous work has proposed the existence of movement control modules (Grillner, 1981(Grillner, , 1985Loeb, 1985;Bizzi et al, 1991), for which there is evidence in both vertebrates (Tresch et al, 2002 (Jing et al, 2004). Control modules incorporating both neural and biomechanical components may be referred to as "neuromechanical modules."…”

“…The interneuronal mechanisms that generate different feeding motor patterns in Aplysia have been studied intensively Weiss, 2001, 2002;Jing et al, 2004) using neural patterns identified through in vitro recordings of individual identified neurons or nerves. For example, to discriminate biting from swallowing, the authors use the duration of activity in the I2 motor neurons (Jing et al, 2004).…”

“…For example, to discriminate biting from swallowing, the authors use the duration of activity in the I2 motor neurons (Jing et al, 2004). However, the duration of I2 activity may be an indicator of a shift from type A to type B swallowing rather than from biting to swallowing.…”