Sensory input induces long-lasting changes in the output of the lobster pyloric network

Abstract

1. A long-lasting restructuring of the pyloric neural network of the lobster stomatogastric nervous system (STS) by a multisynaptic sensory afferent is described. This restructuring can be obtained either by mechanical stimulation of the pyloric region of the stomach or by brief high-frequency electrical stimulation of a nerve that innervates this region, the lateral posterolateral nerve (lpln). Electron microscopy shows that this nerve contains several thousand very small fibers (approximately 0.3 microns diam), the activation of some subset of which is responsible for the effects of lpln stimulation. 2. These stimulation paradigms result in both short-duration changes in pyloric activity and modulatory effects long outlasting the stimulus end. The long-lasting changes include the cessation of rhythmic ventricular dilator (VD) and lateral pyloric (LP) neuron activity, and thus result in a reduced pyloric pattern in which only the pyloric dilator (PD), inferior cardiac (IC), anterior burster (AB), and pyloric (PY) neurons are active. 3. Tonic low-frequency lpln stimulation, alternatively, results in the VD neuron rhythmically firing long spike bursts with a cycle frequency much slower than that of the pyloric network while an otherwise complete pyloric pattern continues. In this new bursting pattern the VD neuron fires exclusively with another STS neural network, the cardiac sac (CS) network, and thus functionally "switches" from the pyloric to the CS network. This switch of the VD neuron from the pyloric to the CS network also occurs when the CS network is spontaneously active. 4. Our results thus demonstrate that sensory input can provoke a long-lasting modification of the functional configuration of a rhythmic neural network. They further extend the concept of flexibility in nervous systems by showing that individual neurons can belong to more than one neural network, "switching" from one to another in response to sensory input or spontaneous central nervous activity.

Characterization of a descending pathway: activation and effects on motor patterns in the brachyuran crustacean stomatogastric nervous system

“…For example, we did not observe any PSPs in pyloric neurons, which is similar to C. borealis, but is in contrast to the findings for the spiny lobster P. interruptus (Hooper et al, 1990;Marder, 1984;Russell and Hartline, 1981;Sigvardt and Mulloney, 1982a) and H. gammarus (Cazalets et al, 1987;Faumont et al, 2005;Meyrand et al, 1991;Meyrand et al, 1994). Also, in C. pagurus and C. borealis, ivn stimulation inhibited VD and IC neurons, which contrasts with the findings for P. interruptus (Hooper et al, 1990;Russell and Hartline, 1981;Sigvardt and Mulloney, 1982b). In all species (Christie et al, 2004;Dando and Selverston, 1972;Sigvardt and Mulloney, 1982b), however, the activity of the PD motor neuron decreased in response to IV activation (Fig.…”

“…The effects of the IV (or PS) neurons on the different motor patterns (pyloric, gastric mill and esophageal rhythms) were described previously in different crustacean species (Claiborne and Selverston, 1984;Dando and Selverston, 1972;Faumont et al, 2005;Hooper et al, 1990;Marder and Eisen, 1984a;Marder and Eisen, 1984b;Russell and Hartline, 1981;Sigvardt and Mulloney, 1982a;Sigvardt and Mulloney, 1982b). It appears that the effects of the IV neurons on the pyloric rhythm are more similar among brachyuran species than between Brachyura, Astacidea and Palinura.…”

“…By contrast, previous work has demonstrated the influence of two identified neurons in the brain, the IV (or PS) neurons, on the STNS motor patterns in various lobster and crab species (Christie et al, 2004;Dando and Selverston, 1972;Hooper et al, 1990;Meyrand et al, 1994;Sigvardt and Mulloney, 1982a;Sigvardt and Mulloney, 1982b). The IV neurons project to the STNS via a unilateral nerve, the ivn.…”

Multiple Types of Control by Identified Interneurons in a Sensory-Activated Rhythmic Motor Pattern

“…Despite the observation that some stomatogastric CPGs can be almost continuously active in freely behaving animals (Clemens et al, 1998) and therefore do not appear to be gated by peripheral sensory inputs in the same way as other CPGs, multiple higher-order control by a variety of extrinsic modulatory interneurons is very important in shaping the motor output of all known stomatogastric CPGs (Marder and Calabrese, 1996;Harris-Warrick et al, 1997;Blitz and Nusbaum, 1999). It has been shown that many of these interneurons receive mechanosensory inputs from the stomach (Sigvardt and Mulloney, 1982;Simmers and Moulins, 1988), which can profoundly alter ongoing motor patterns (Hooper et al, 1990;Katz and Harris-Warrick, 1991;Nargeot and Moulins, 1997;Combes et al, 1999).…”

Mechanosensory Activation of a Motor Circuit by Coactivation of Two Projection Neurons

“…The actions of several sensory systems on the STG circuits have been documented (Simmers and Moulins, 1988a,b;Katz et al, 1989;Hooper et al, 1990;Meyrand et al, 1994;Combes et al, 1999a;Beenhakker et al, 2004). One of these systems, the ventral cardiac neuron (VCN) mechanosensory system, is a population of sensory neurons innervating the wall of the cardiac sac stomach compartment that are hypothesized to detect foregut distention .…”