Endogenous Motor Neuron Properties Contribute to a Program-Specific Phase of Activity in the Multifunctional Feeding Central Pattern Generator ofAplysia

Abstract

Multifunctional central pattern generators (CPGs) are circuits of neurons that can generate manifold actions from a single effector system. This study examined a bilateral pair of pharyngeal motor neurons, designated B67, that participate in the multifunctional feeding network of Aplysia californica. Fictive buccal motor programs (BMPs) were elicited with four distinct stimulus paradigms to assess the activity of B67 during ingestive versus egestive patterns. In both classes of programs, B67 fired during the phase of radula protraction and received a potent inhibitory postsynaptic potential (IPSP) during fictive radula retraction. When programs were ingestive, the retraction phase IPSP exhibited a depolarizing sag and was followed by a postinhibitory rebound (PIR) that could generate a postretraction phase of impulse activity. When programs were egestive, the depolarizing sag potential and PIR were both diminished or were not present. Examination of the membrane properties of B67 disclosed a cesium-sensitive depolarizing sag, a corresponding Ih-like current, and PIR in its responses to hyperpolarizing pulses. Direct IPSPs originating from the influential CPG retraction phase interneuron B64 were also found to activate the sag potential and PIR of B67. Dopamine, a modulator that can promote ingestive behavior in this system, enhanced the sag potential, Ih-like current, and PIR of B67. Finally, a pharyngeal muscle contraction followed the radula retraction phase of ingestive, but not egestive motor patterns. It is proposed that regulation of the intrinsic properties of this motor neuron can contribute to generating a program-specific phase of motor activity.

Octopamine promotes rhythmicity but not synchrony in a bilateral pair of bursting motor neurons in the feeding circuit of Aplysia

“…Under these conditions, B67 exhibits two forms of patterned activity, multiphasic buccal motor programs (BMPs) and monophasic endogenous bursts [ Fig. 3A (see also Serrano et al, 2007)]. BMPs consist of a stereotyped protractionretraction sequence that reflects the coordinated activity of a large number of buccal neurons (see Morton and Chiel, 1993a;Morton and Chiel, 1993b;Elliott and Susswein, 2002;Murphy, 2001;Cropper et al, 2004).…”

“…3Biii) did OA elicit BMPs that periodically interrupted B67's regular bursting (see also Vehovszky et al, 1998). The motor programs evoked by OA were always classified as ingestive using the criteria of Morton and Chiel (Morton and Chiel, 1993a; Morton and Chiel, 1993b) (see also Serrano et al, 2007).…”

“…All experiments in this study were performed on B67, a large superficial MN located on the caudal surface of each buccal hemiganglion [designated pharynx burster (PB) in Aplysia kurodai (Nagahama and Takata, 1987) and B67 in A. californica (Park et al, 1999;Serrano and Miller, 2006)]. Previous studies established the presence of endogenous burst-and rhythmgenerating properties in B67, including a tetrodotoxin (TTX)-resistant driver potential (DP), a slowly developing depolarization ('sag' potential) in response to prolonged imposed hyperpolarization, and post-inhibitory rebound (PIR) (Serrano and Miller, 2006;Serrano et al, 2007). Independent microelectrodes were used for recording the membrane potential (10-20MW) and injecting current (5-10 MW) into B67.…”

Implication of dopaminergic modulation in operant reward learning and the induction of compulsive-like feeding behavior inAplysia

“…Moreover, these modulatory actions vary according to the target cell type and whether exposure to the amine is continuous or intermittent. For example, tonic DA application decreases the excitability of buccal circuit neurons B4/5, B34, B64 (Kabotyanski et al 2000), enhances post-inhibitory rebound in B8 (Kabotyanski et al 2000), and increases the bursting and plateauing properties of B67 (Serrano and Miller 2006;Serrano et al 2007). Alternatively, phasic DA release induced by contingent reward reinforcement in vivo or contingent En.2 stimulation in vitro augments both the intrinsic excitability and plateauing capability of neuron B51 (Nargeot et al 1999a;Brembs et al 2002;Lorenzetti et al 2008).…”

Contextual modulation of multifunctional central pattern generator

“…The neural networks controlling such programmed behaviors are termed central pattern generators (CPGs) and they have the potential to produce different motor outputs depending on the current external and internal environment of the organism (McCrea and Rybak, 2008;Rossignol et al, 2006;Selverston, 2010;Serrano et al, 2007). In some cases the functional reorganization of a multi-functional CPG is under the influence of projection neurons (Benjamin and Elliott, 1989;Combes et al, 1999;Croll et al, 1985;Jing and Weiss, 2001;Meyrand et al, 1994;Rosen et al, 1991) or sensory neurons (Bässler and Büschges, 1998;Blitz and Nusbaum, 2011;Smotherman, 2007).…”