The crustacean swimmeret system includes a distributed set of local circuits that individually control movements of one jointed limb. These modular local circuits occur in pairs in each segmental ganglion, and normally operate synchronously to produce smoothly coordinated cycles of limb movements on different body segments. The system presents exceptional opportunities for computational and experimental investigation of neural mechanisms of coordination because: a. The system will express in vitro the periodic motor pattern that normally drives cycles of swimmeret movements during forward swimming. b. The intersegmental neurons which encode information that is necessary and sufficient for normal coordination have been identified, and their activity can be recorded. c. The local commissural neurons that integrate this coordinating information and tune the phase of each swimmeret are known. d. The complete set of synaptic connections between coordinating neurons and these commissural neurons have been described. e. The synaptic connections onto each local pattern-generating circuit through which coordinating information tunes the circuit's phase have been discovered. These factors make possible for the first time a detailed, comprehensive cellular and synaptic explanation of how this neural circuit produces an effective, behaviorally-significant output. This paper is the first comprehensive review of the system's neuroanatomy and neurophysiology, its local and intersegmental circuitry, its transmitter pharmacology, its neuromodulatory control mechanisms, and its interactions with other motor systems. Each of these topics is covered in detail in an attempt to provide a complete review of the literature as a foundation for new research. The series of hypotheses that have been proposed to account for the system's properties are reviewed critically in the context of experimental tests of their validity.

Arthropods are very diverse, come in many different forms with diverse adaptations, and through such diversity have populated all environmental niches on the planet. Almost 80% of the animals on planet Earth belong to this phylum. Despite their very diverse phenotypes they share fundamental similarities which were previously used to generate a phylogenetic tree. All arthropods have segmented bodies and possess jointed limbs at all or many of their body segments. An additional common feature of arthropods is their exoskeleton, made mainly of chitin and/or sclerotin.

We describe the synaptic connections through which information required to coordinate limb movements reaches the modular microcircuits that control individual limbs on different abdominal segments of the crayfish, Pacifastacus leniusculus. In each segmental ganglion, a local commissural interneuron, ComInt 1, integrates information about other limbs and transmits it to one microcircuit. Five types of nonspiking local interneurons are components of each microcircuit's pattern-generating kernel (Smarandache-Wellmann et al., 2013). We demonstrate here, using paired microelectrode recordings, that the pathway through which information reaches this kernel is an electrical synapse between ComInt 1 and one of these five types, an IRSh interneuron. Using single-electrode voltage clamp, we show that brief changes of ComInt 1's membrane potential affect the timing of its microcircuit's motor output. Changing ComInt 1's membrane potential also changes the phase, duration, and strengths of bursts of spikes in its microcircuit's motor neurons and corresponding changes in its efferent coordinating neurons that project to other ganglia. These effects on coordinating neurons cause changes in the phases of motor output from other microcircuits in those distant ganglia. ComInt 1s function as hub neurons in the intersegmental circuit that synchronizes distributed microcircuits. The synapse between each ComInt 1 and its microcircuit's IRSh neuron completes a five synapse pathway in which analog information is encoded as a digital signal by efference-copy neurons and decoded from digital to analog form by ComInt 1. The synaptic organization of this pathway provides a cellular explanation of this nervous system's key dynamic properties.

We describe synaptic connections through which information essential for encoding efference copies reaches two coordinating neurons in each of the microcircuits that controls limbs on abdominal segments of the crayfish, Pacifastacus leniusculus. In each microcircuit, these coordinating neurons fire bursts of spikes simultaneously with motor neurons. These bursts encode timing, duration, and strength of each motor burst. Using paired microelectrode recordings, we demonstrate that one class of nonspiking neurons in each microcircuit's pattern-generating kernel-IPS-directly inhibits the ASC E coordinating neuron that copies each burst in power-stroke (PS) motor neurons. This inhibitory synapse parallels IPS's inhibition of the same PS motor neurons. Using a disynaptic pathway to control its membrane potential, we demonstrate that a second type of nonspiking interneuron in the pattern-generating kernel-IRSh-inhibits the DSC coordinating neuron that copies each burst in return-stroke (RS) motor neurons. This inhibitory synapse parallels IRS's inhibition of the microcircuit's RS motor neurons. Experimental changes in the membrane potential of one IPS or one IRSh neuron simultaneously changed the strengths of motor bursts, durations, numbers of spikes, and spike frequency in the simultaneous ASC E and DSC bursts.ASC E and DSC coordinating neurons link the segmentally distributed microcircuits into a coordinated system that oscillates with the same period and with stable phase differences. The inhibitory synapses from different pattern-generating neurons that parallel their inhibition of different sets of motor neurons enable ASC E and DSC to encode details of each oscillation that are necessary for stable, adaptive synchronization of the system.

We conducted a quantitative analysis of the different nonspiking interneurons in the local pattern-generating circuits of the crayfish swimmeret system. Within each local circuit, these interneurons control the firing of the power-stroke and return-stroke motor neurons that drive swimmeret movements. Fifty-four of these interneurons were identified during physiological experiments with sharp microelectrodes and filled with dextran Texas red, Neurobiotin, or both. Five types of neurons were identified on the basis of combinations of physiological and anatomical characteristics. Anatomical categories were based on 16 anatomical parameters measured from stacks of confocal images obtained from each neuron. The results support the recognition of two functional classes: inhibitors of power stroke (IPS) and inhibitors of return stroke (IRS). The IPS class of interneuron has three morphological types with similar physiological properties. The IRS class has two morphological types with physiological properties and anatomical features different from the IPS neurons but similar within the class. Three of these five types have not been previously identified. Reviewing the evidence for dye coupling within each type, we conclude that each type of IPS neuron and one type of IRS neuron occur as a single copy in each local pattern-generating circuit. The last IRS type includes neurons that might occur as a dye-coupled pair in each local circuit. Recognition of these different interneurons in the swimmeret pattern-generating circuits leads to a refined model of the local pattern-generating circuit that includes synaptic connections that encode and decode information required for intersegmental coordination of swimmeret movements.