Contingent-Dependent Enhancement of Rhythmic Motor Patterns: AnIn VitroAnalog of Operant Conditioning

Abstract

Operant conditioning is characterized by the contingent reinforcement of a designated behavior. Previously, feeding behavior in Aplysia has been demonstrated to be modified by operant conditioning, and a neural pathway (esophageal nerve; E n.) that mediates some aspects of reinforcement has been identified. As a first step toward a cellular analysis of operant conditioning, we developed an in vitro buccal ganglia preparation that expressed the essential features of operant conditioning. Motor patterns that represented at least two different aspects of fictive feeding (i.e., ingestion-like and rejection-like motor patterns) were elicited by tonic stimulation of a peripheral buccal nerve (n.2,3). Three groups of preparations were examined. In a contingent-reinforcement group, stimulation of E n. was contingent on the expression of a specific type of motor pattern (i.e., either ingestion-like or rejection-like). In a yoke-control group, stimulation of E n. was not contingent on any specific pattern. In a control group, E n. was not stimulated. The frequency of the reinforced pattern increased significantly only in the contingent-reinforcement group. No changes were observed in nonreinforced patterns or in the motor patterns of the control and yoke-control groups. Contingent reinforcement of the ingestion-like pattern was associated with an enhancement of activity in motor neuron B8, and this enhancement was specific to the reinforced pattern. These results suggest that the isolated buccal ganglia expressed an essential feature of operant conditioning (i.e., contingent reinforcement modified a designated operant) and that this analog of operant conditioning is accessible to cellular analysis. Key words: buccal ganglia; Aplysia californica; central pattern generator; operant conditioning; learning and memory; contingent reinforcementOperant conditioning, which was introduced by Thorndike (1911), is an example of associative learning in which an association is established between a specific behavior (the operant) and a stimulus (the reinforcement). A key feature of operant conditioning is the contingency of the reinforcement (i.e., the correlation between the expression of a designated operant behavior and the delivery of a reinforcement; Skinner, 1938;Konorski, 1948). As a result of this contingency the frequency of the reinforced behavior is modified. This phenomenon, known as the "law of effect" (Thorndike, 1933), provided evidence that the nervous system has mechanisms by which a particular motor output can be selected from among many different behaviors that may be expressed.Rhythmic motor acts such as locomotion, feeding, respiration, and heart rate can be modified by operant conditioning (Skinner, 1938;Miller, 1969;Cook and C arew, 1986;Susswein et al., 1986;Jaeger et al., 1987; L ukowiak et al., 1996). It is believed generally that rhythmic motor acts are mediated by groups of neurons referred to as central pattern generators (C PGs;Delcomyn, 1980;Selverston and Moulins, 1985). C PGs are multif unctional netwo...

Cognition in Invertebrates

“…These neurons will be modified by activity-dependent plasticity to bias any future behavior toward the behaviors controlling the heat. Such a process has been found in a similarly isolated behavioral preparation, that is physiologically much more accessible, the operant conditioning of feeding behavior in Aplysia (Nargeot et al, 1997(Nargeot et al, , 1999a(Nargeot et al, , 1999b(Nargeot et al, , 1999cBrembs et al, 2002Brembs et al, , 2004Brembs, 2003aBrembs, , 2003b. In this paradigm, spontaneous bites (or the corresponding neural patterns in the reduced preparation) are rewarded by dopamine-releasing nerve stimulation.…”

“…It was described above how the feeding behavior of Aplysia can be conditioned classically and operantly (Nargeot et al, 1997(Nargeot et al, , 1999a(Nargeot et al, , 1999b(Nargeot et al, , 1999cLechner et al, 2000aLechner et al, , 2000bBrembs et al, 2002Brembs et al, , 2004Brembs, 2003aBrembs, , 2003bMozzachiodi et al, 2003). Taking advantage of the greater physiological accessibility, a reduced preparation of the isolated buccal and cerebral ganglia was used.…”

Operant conditioning in invertebrates

“…Early on, the esophageal nerve appeared to be crucial for the effectiveness of these conditioning experiments [31,38,39]. Recording extracellularly from the esophageal nerve in the intact animal during a biting movement that fails to grasp food reveals little activity.…”

Predictions of Phase-Locking in Excitatory Hybrid Networks: Excitation Does Not Promote Phase-Locking in Pattern-Generating Networks as Reliably as Inhibition

“…Hybrid network construction has the advantage of providing a controlled environment for testing our methodology that incorporates an actual biological neuron and realistic synapses. Endogenously bursting neurons have been shown to be important in the pyloric network (Hartline 1979;Hartline and Gassie 1979;Miller and Selverston 1982), the heartbeat of crustaceans (Tazaki and Cooke 1990), the gastric CPGs of the crustacean stomatogastric system (Harris-Warrick et al 1992;Panchin et al 1993;Selverston and Moulins 1987), the feeding CPG in mollusks (Arshavsky et al 1989(Arshavsky et al , 1991, and appetitive conditioning in the buccal ganglia of Aplysia (Nargeot et al 1997(Nargeot et al , 2007. Therefore we chose to examine circuits constructed with endogenous bursters.…”