Long-Term Expression of Two Interacting Motor Pattern-Generating Networks in the Stomatogastric System of Freely Behaving Lobster

Abstract

Rhythmic movements of the gastric mill and pyloric regions of the crustacean foregut are controlled by two stomatogastric neuronal networks that have been intensively studied in vitro. By using electromyographic recordings from the European lobster, Homarus gammarus, we have monitored simultaneously the motor activity of pyloric and gastric mill muscles for </=3 mo in intact and freely behaving animals. Both pyloric and gastric mill networks are almost continuously active in vivo regardless of the presence of food. In unfed resting animals kept under "natural-like" conditions, the pyloric network expresses the typical triphasic pattern seen in vitro but at considerably slower cycle periods (2. 5-3.5 s instead of 1-1.5 s). Gastric mill activity occurs at mean cycle periods of 20-50 s compared with 5-10 s in vitro but may suddenly stop for up to tens of minutes, then restart without any apparent behavioral reason. When conjointly active, the two networks express a strict coupling that involves certain but not all motor neurons of the pyloric network. The posterior pyloric constrictor muscles, innervated by a total of 8 pyloric (PY) motor neurons, are influenced by the onset of each gastric mill medial gastric/lateral gastric(MG/LG) neuron powerstroke burst, and for one cycle, PY neuron bursts may attain >300% of their mean duration. However, the duration of activity in the lateral pyloric constrictor muscle, innervated by the unique lateral pyloric (LP) motor neuron, remains unaffected by this perturbation. During this period after gastric perturbation, LP neuron and PY neurons thus express opposite burst-to-period relationships in that LP neuron burst duration is independent of the ongoing cycle period, whereas PY neuron burst duration changes with period length. In vitro the same type of gastro-pyloric interaction is observed, indicating that it is not dependent on sensory inputs. Moreover, this interaction is intrinsic to the stomatogastric ganglion itself because the relationship between the two networks persists after suppression of descending inputs to the ganglion. Intracellular recordings reveal that this gastro-pyloric interaction originates from the gastric MG and LG neurons of the gastric network, which inhibit the pyloric pacemaker ensemble. As a consequence, the pyloric PY neurons, which are inhibited by the pyloric dilator (PD) neurons of the pyloric pacemaker group, extend their activity during the time that PD neuron is held silent. Moreover, there is evidence for a pyloro-gastric interaction, apparently rectifying, from the pyloric pacemakers back to the gastric MG/LG neuron group.

A newly identified extrinsic input triggers a distinct gastric mill rhythmviaactivation of modulatory projection neurons

“…This pyloric regulation of the gastric mill rhythm during the protractor phase, via feedback inhibition of MCN1 and CPN2, occurs only during the POC-type of gastric mill rhythm Blitz et al, 2004;Christie et al, 2004). Previous work documented additional cellular and synaptic mechanisms underlying inter-circuit regulation during other versions of the gastric mill rhythm (Bartos and Nusbaum, 1997;Clemens et al, 1998;Bartos et al, 1999;Wood et al, 2004). Although coordination between different behaviors, such as locomotion and respiration, occurs in many animals (Bramble and Carrier, 1983;Syed and Winlow, 1991;Kawahara et al, 1989;Morin and Viala, 2002;Saunders et al, 2004), the underlying cellular mechanisms remain to be determined in these other systems.…”

Intercircuit Control via Rhythmic Regulation of Projection Neuron Activity

“…There are, for example, well documented interactions between the respiratory and locomotory systems (Cattaert and Clarac, 1983;Kawahara et al, 1989;Morin and Viala, 2002), between respiration and vocalization (Larson et al, 1994;Suthers, 1997), and between different aspects of feeding (Perrins and Weiss, 1996;Clemens et al, 1998). However, there is little information available regarding the cellular basis of how such interactions coordinate the relevant neuronal circuits.…”

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).…”