Nonspiking interneurons in the ventilatory central pattern generator of the shore crab, Carcinus maenas

Abstract

Eight nonspiking interneurons were identified that are elements of the central pattern generator controlling ventilation in the shore crab, Carcinus maenas. Intracellular recordings from these neurons in an isolated ganglion preparation revealed that these cells exhibit large amplitude oscillations in their membrane potentials, which are in-phase with the ventilatory motor pattern. These oscillations are present during the expression of the two distinct ventilatory motor output patterns corresponding to forward and reversed ventilation, and the oscillations stopped during pauses in the ventilatory rhythm. Injection of intracellular current pulses into these interneurons caused a resetting of the ongoing ventilatory rhythm, indicating that these cells are part of the ventilatory central pattern generator. The structure of each interneuron was determined by the intracellular injection of Lucifer Yellow dye. These neurons have a large diameter main neurite ranging from 10 to 20 microns in diameter with very restricted primary and secondary branching from the main neurite. All of the interneurons are restricted to a single hemiganglion and perturbation of these cells with intracellular current pulses only affect the motor output of the hemiganglion containing the interneuron. These eight nonspiking interneurons appear to be the primary components of the central pattern generator underlying ventilation in the crab.

Crustacean Motor Pattern Generator Networks

“…These data indicate that separate CPGs produce the left and right SG ventilatory patterns [93], and are consistent with data showing that the left and right ventilatory rhythms are generated and controlled independently [90,91,94]. Moreover, it reinforces the hypothesis that the loose phase coupling observed between bilateral CPGs [94] is mediated by the nonspiking frequency modulating interneurons (FMis; see below) [95] rather than midline crossing CPGi interconnections.…”

“…Unlike the stomatogastric system, the CPG contains large numbers of premotor interneurons. Although originally thought to be a single endogenously oscillating nonspiking neuron [91], the interneuronal ventilatory CPG was later shown to consist of at least two [92], and is now known in the crab, C. maenas, to consist of 8, nonspiking interneurons [CPG interneurons (CPGi) 1-8] [93]. Figure 3c shows extracellular recordings of the activity of all the ventilatory motor neurons, and intracellular recordings from a depressor motorneuron and one CPGi.…”

Temporal Dynamics of Graded Synaptic Transmission in the Lobster Stomatogastric Ganglion

“…Graded synaptic transmission is a common feature of many invertebrate sensory and motor networks (Pearson and Fourtner, 1975;Burrows and Siegler, 1978;DiCaprio, 1989;Nadim et al, 1995;Olsen et al, 1995) and of the vertebrate retina (Roberts and Bush, 1981). Synaptic potentials in the stomatogastric nervous system, like those in the leech Olsen et al, 1995), are both graded and spike-mediated.…”

Effect of a nonspiking neuron on motor patterns of the leech

“…They have been found to play several functions in insects and arthropods. Among them 1) NS neurons were described as premotor units that integrate descending signals and transmit these signals to groups of motoneurons (Burrows 1992;Wolf and Buschges 1995); 2) they were shown to be part of the CPGs of crayfish swimmeret (Mulloney 2003;Paul and Mulloney 1985;Pearson and Fourtner 1974), cockroach walking (Pearson and Fourtner 1974), and crab ventilation (Dicaprio 1989); 3) NS neurons in the crab have been described as frequency modulators (DiCaprio and Fourtner 1988), regulating the cycle frequency of ventilation; and 4) in crayfish they were shown to be part of a reflex network that controls the walking motor pattern (Elson et al 1992;Le Ray and Cattaert 1997).…”