Concerted GABAergic Actions of<i>Aplysia</i>Feeding Interneurons in Motor Program Specification

Jing, Jian; Vilim, Ferdinand S.; Wu, Jianyong; Park, Ji-Ho; Weiss, Klaudiusz R.

doi:10.1523/jneurosci.23-12-05283.2003

Cited by 67 publications

(96 citation statements)

References 60 publications

(95 reference statements)

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“…Assays of monosynapticity were conducted in high-divalent saline containing (in mM): 312 NaCl, 10 KCl, 132 MgCl 2 , 33 CaCl 2 , and 10 HEPES, pH 7.6, a solution that elevates spike thresholds and thus curtails polysynaptic activation (Cohen et al, 1978;Trudeau and Castellucci, 1992). Neurons were identified on the basis of location, size, and electrophysiological and morphological characteristics (Rosen et al, 1991;Hurwitz et al, 1997;Jing and Weiss, 2001;Jing et al, 2003).…”

Section: Methodsmentioning

confidence: 99%

“…Previous work on biting and rejection-like motor programs Weiss, 2001, 2002;Jing et al, 2003) suggested that the Aplysia feeding network has a modular organization. Here, we characterize swallowing and rejection-like motor programs that are elicited by a higher-order interneuron, cerebral-buccal interneuron-4 (CBI-4), and determine whether modules are behavior specific or independent.…”

Section: Introductionmentioning

confidence: 98%

See 1 more Smart Citation

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

Jing¹,

Cropper²,

Hurwitz³

et al. 2004

J. Neurosci.

121

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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.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 98%

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

Jing¹,

Cropper²,

Hurwitz³

et al. 2004

J. Neurosci.

121

View full text Add to dashboard Cite

show abstract

“…Control of I2 duration and intensity may be attributable to actions of GABAergic interneurons (Jing et al, 2003). It is clear that the combination of shifting coalitions of muscles, and a reorganizing neural architecture, are critical for multifunctionality.…”

Section: Multifunctionality and Muscular Coalitionsmentioning

confidence: 99%

Neuromechanics of Multifunctionality during Rejection inAplysia californica

Morton

Chiel³

2006

J. Neurosci.

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“…Next, we sought to determine whether CBI-11 acts on buccal CPG elements that are important for the expression of different types of motor programs. We first recorded from B40 Jing et al, 2003), an interneuron that is critical for the expression of ingestive programs, by promoting more B8 activity during retraction and less B8 activity during protraction. We found that CBI-11 elicited monosynaptic EPSPs on B40, which persisted in high-divalent saline (Fig.…”

Section: Program Specification By Cbi-11 and Its Effects On Cbi-2-drimentioning

confidence: 99%

“…However, more recent work showed that pattern-generating networks activated by command neurons are often multifunctional; that is, they generate multiple types of motor programs (Nusbaum and Beenhakker, 2002;Jing and Weiss, 2005;Marder and Bucher, 2007;Briggman and Kristan, 2008;Benjamin, 2012). Therefore, to initiate behavior, it does not suffice to simply trigger activity in the motor network-the type of program induced must also be specified.…”

Section: Introductionmentioning

confidence: 99%

Complementary Interactions between Command-Like Interneurons that Function to Activate and Specify Motor Programs

Wang

Siniscalchi

et al. 2014

J. Neurosci.

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Motor activity is often initiated by a population of command-like interneurons. Command-like interneurons that reliably drive programs have received the most attention, so little is known about how less reliable command-like interneurons may contribute to program generation. We study two electrically coupled interneurons, cerebral-buccal interneuron-2 (CBI-2) and CBI-11, which activate feeding motor programs in the mollusk Aplysia californica. Earlier work indicated that, in rested preparations, CBI-2, a powerful activator of programs, can trigger ingestive and egestive programs. CBI-2 reliably generated ingestive patterns only when it was repeatedly stimulated. The ability of CBI-2 to trigger motor activity has been attributed to the two program-promoting peptides it contains, FCAP and CP2. Here, we show that CBI-11 differs from CBI-2 in that it contains FCAP but not CP2. Furthermore, it is weak in its ability to drive programs. On its own, CBI-11 is therefore less effective as a program activator. When it is successful, however, CBI-11 is an effective specifier of motor activity; that is, it drives mostly ingestive programs. Importantly, we found that CBI-2 and CBI-11 complement each other's actions. First, prestimulation of CBI-2 enhanced the ability of CBI-11 to drive programs. This effect appears to be partly mediated by CP2. Second, coactivation of CBI-11 with CBI-2 makes CBI-2 programs immediately ingestive. This effect may be mediated by specific actions that CBI-11 exerts on pattern-generating interneurons. Therefore, different classes of command-like neurons in a motor network may make distinct, but potentially complementary, contributions as either activators or specifiers of motor activity.

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Concerted GABAergic Actions ofAplysiaFeeding Interneurons in Motor Program Specification

Cited by 67 publications

References 60 publications

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

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

Neuromechanics of Multifunctionality during Rejection inAplysia californica

Complementary Interactions between Command-Like Interneurons that Function to Activate and Specify Motor Programs

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