Exp Brain Res (1996) 112:163-180 9 Springer-Verlag 1996 F. Clarac 9 D. Cattaert Invertebrate presynaptic inhibition and motor control Received: 20 March 1996 / Accepted: 14 June 1996 Introduction Presynaptic inhibition was first investigated at nearly the same time in both vertebrates and invertebrates. In 1957, Frank and Fuortes reported that, in the cat spinal cord, applying a conditioning stimulus to group I afferent fi- bers of the flexor muscles decreased the monosynaptic excitatory postsynaptic potentials (EPSPs) elicited by stimulation of Ia fibers from extensors, by reducing their synaptic efficiency, i.e., by presynaptic inhibition. In 1961, Dudel and Kuffler described a similar phenome- non at the neuromuscular junction of a crustacean mus- cle innervated by a single excitatory and a single inhibi- tory motoneuron (MN). When the inhibitory impulse was timed to arrive 1-6 ms before the excitatory im- pulse, it reduced the excitatory junctional potential. Up- on studying the number and the size of the released quanta in response to an excitatory nerve stimulus, it was observed that the first inhibitory impulse reduced the number of quanta released, while their size remained un- changed. This inhibitory influence therefore acted at a presynaptic site on the excitatory nerve terminals. Since these two pioneering studies, each of the main phyla has provided various descriptions of presynaptic mechanisms. In mammals, most of the research on this topic has been focused on the sensory afferents, mainly in connection with pain and proprioceptive spinal mech- anisms (Schmidt 1971). Presynaptic mechanisms link up with the dorsal root potential (DRP) first described by Barron and Matthews (1938). In invertebrates, the sites of presynaptic connections are widely distributed throughout the central nervous system (CNS). At the neuromuscular junction, the phenomenon has been stud- ied in great detail and some new information has been obtained about the position of the inhibitory axoaxonal synapse (Atwood and Morin 1970; Atwood et al. 1984) and the neurotransmitter and ionic mechanisms involved F. Clarac (~) 9 D. Cattaert CNRS - NBM - 31, CheminJoseph Aiguier, F-13402 MarseilleCedex 20, France (Fuchs and Getting 1980; Miwa and Kawai 1990; Baxter and Bittner 1991). Similar control processes have also been described at the insect neuromuscular junction (Parnas and Grossman 1973). In arthropods, presynaptic inhibition has frequently been associated with the giant interneurons (GINs) involved in escape responses. Either it is the sensory afferent that controls the central inputs to that GINs (Boyan 1988) or it is the GIN that controls the afferents (Kirk and Govind 1990). In the stomatogas- tric system of crustacea, presynaptic inhibition is exerted onto an interneuron (IN) and regulates the central con- nections of the network (Nusbaum et al. 1992). In the mollusc, too, several neural circuits have been found to involve presynaptic connections. Recent studies on vertebrates and invertebrates have demonstrated that some of the mechanisms described so far are similar in both cases (Rudomin 1990; Watson 1992). In insects and crustacea, intracellular recordings have been carried out on the terminal proximal endings of the sensory afferents (Sillar and Skorupski 1986; Boyan 1988; Cattaert et al. 1992; Burrows and Laurent 1993). In these sensory fibers, primary afferent depolar- ization (PAD) has been observed, which is similar to the DRP studied extracellularly in vertebrate sensory affer- ents. Although in invertebrates most of the connections are inhibitory at the presynaptic sites, facilitatory activities of various kinds have also been found to occur: short- term facilitation (Zucker 1974); facilitation involved in the habituated gill-withdrawal reflex (Siegelbaum et al. 1982) and in the swimming network (Katz and Frost 1995); facilitation in sensory message due to electrical coupling existing between afferents (El Manira et al. 1993). In this review dealing with invertebrates, we will first describe presynaptic inhibition itself, taking the crayfish leg chordotonal afferent as an example (Cattaert et al. 1992); after a presentation of the electrical events occur- ring pre- and postsynaptically; we will then explain the ionic mechanisms involved in PAD, in the light of vari- ous examples, and their morphological location. In the