Reconfiguration of multiple motor networks by short- and long-term actions of an identified modulatory neuron Serge Faumont,* ,  Denis Combes,* ,à Pierre Meyrand and John Simmers à Laboratoire de Neurobiologie des Re ´ seaux, Universite ´ Bordeaux 1 & Centre National de la Recherche Scientifique, Unite ´ Mixte de Recherche 5816, Avenue des Faculte ´ s, 33405 Talence, France Keywords: lobster, motor networks, motor pattern selection, neuromodulation, projection neuron, stomatogastric ganglion Abstract The pyloric and gastric motor pattern-generating networks in the stomatogastric ganglion of the lobster Homarus gammarus are reconfigured into a new functional circuit by burst discharge in an identified pair of modulatory projection interneurons, originally named the pyloric suppressor (PS) neurons because of their inhibitory effects on pyloric network activity. Here we elucidate the actions of the PS neurons on individual members of the neighbouring gastric circuit, as well as describing their ability to alter synaptic coupling between the two networks. PS neuron firing has two distinct effects on gastric network activity: an initial short-lasting action mediated by transient inhibition of most gastric motoneurons, followed by a long-lasting circuit activation associated with a prolonged PS-evoked depolarization of the medial gastric (MG) motoneuron and the single network interneuron, Int1. These long-lasting effects are voltage-dependent, and experiments with hyperpolarizing current injection and photoablation suggest that excitation of both the MG neuron and Int1 is critical for PS-elicited gastric network rhythmicity. In parallel, PS neuron discharge persistently (lasting several minutes) enhances the strength of an inhibitory synaptic influence of the MG neuron on the pyloric dilator (PD)–anterior burster (AB) pacemaker neurons, thereby facilitating operational fusion of the two networks. Therefore, a single modulatory neuron may influence disparate populations of neurons via a range of very different and highly target-specific mechanisms: conventional transient synaptic drive and up- or down-modulation of membrane properties and synaptic efficacy. Moreover, distinctly different time courses of these actions allow different circuit configurations to be specified sequentially by a given modulatory input. Introduction It is now well established that central neuronal networks can alter their patterns of activity to fulfil different functions (Getting, 1989; Meyrand et al., 1991; Marder & Calabrese, 1996; McCormick & Bal, 1997; Westberg et al., 1998). In motor systems in particular, the selection mechanisms for different activity patterns from a single pool of neurons have been investigated in a variety of preparations (Stein et al., 1997; Combes et al., 1999; Pearson, 2000; Nusbaum & Beenhakker, 2002). Neural networks that generate motor rhythms can adopt several functional configurations in which cycle period, phase relationships and the numbers of participating neurons are different. Numerous studies have emphasized the role of neuromodulatory inputs in this network flexibility. Such projection neurons act by altering the membrane properties of individual network neurons, as well as their interconnecting synapses (Marder & Calabrese, 1996; Calabrese, 1998; Nusbaum & Beenhakker, 2002). However, whereas these general mechanisms for network modulation are now widely accepted, their collective employment by individual modulatory neurons in influencing multiple target networks is significantly less well understood. To address this issue we have studied modulatory neuron-induced reorganization of two different motor networks, the pyloric and gastric mill circuits, in the lobster stomatogastric nervous system (STNS). These two well-characterized networks (Harris-Warrick et al., 1992), which control filtering and chewing movements of the pyloric filter and gastric teeth, respectively, produce two distinct motor rhythms that continue to be generated in vitro. Both networks are profoundly influenced by a pair of identified modulatory projection interneurons, the pyloric suppressor (PS) neurons (Cazalets et al., 1990a; Meyrand et al., 1994), whose activation reorganizes the activity patterns of the two networks into a single new rhythm (Meyrand et al., 1991, 1994). Understanding the mechanisms by which such network reconstruc- tion occurs requires knowledge of the precise effects of the PS neurons on the cellular and synaptic properties of all motor network elements. Whereas the overall impact of the PS interneurons on STNS motor networks has been characterized (Meyrand et al., 1991, 1994), and their specific actions on pyloric circuit neurons analysed in detail (Cazalets et al., 1990a,b), the precise effects of the projection neurons on gastric network neurons remain to be elucidated. This goal is attainable given the small number of neurons in the pyloric and gastric networks (14 and 16 neurons, respectively). The PS neurons have an overall suppressive action on pyloric rhythmcity, mainly by dimin- ishing the oscillatory capability of individual pyloric neurons, with Correspondence: Dr Pierre Meyrand, as above. E-mail: p.meyrand@lnr.u-bordeaux1.fr   Present address: Institute of Neuroscience, University of Oregon, Eugene OR 97403– 1254, USA. à Present address: Laboratoire de Physiologie et Physiopathologie de la Signalization Cellulaire, CNRS-UMR 5543, Universite ´ Victor Segalen Bordeaux 2, 146 rue Le ´o Saignat, 33076 Bordeaux, France. *S.F. and D.C. contributed equally to this work. Received 4 February 2005, revised 7 July 2005, 26 August 2005, accepted 5 September 2005 European Journal of Neuroscience, Vol. 22, pp. 2489–2502, 2005 ª Federation of European Neuroscience Societies doi:10.1111/j.1460-9568.2005.04442.x