Classical Conditioning of Feeding inAplysia: II. Neurophysiological Correlates

Abstract

Feeding behavior in Aplysia californica can be classically conditioned using tactile stimulation of the lips as conditional stimulus (CS) and food as unconditional stimulus (US) [ (companion paper)]. Conditioning resulted in an increase in the number of CS-evoked bites that persisted for at least 24 hr after training. In this study, neurophysiological correlates of classical conditioning training were identified and characterized in an in vitro preparation of the cerebral and buccal ganglia. Stimulation of a lip nerve (AT(4)), which mediates mechanosensory information, resulted in a greater number of buccal motor patterns (BMPs) in ganglia isolated from animals that had received paired training than in ganglia from control animals. The majority of the evoked BMPs were classified as ingestion-like patterns. Intracellular recordings from pattern-initiating neuron B31/32 revealed that stimulation of AT(4) evoked greater excitatory input in B31/32 in preparations from animals that had received paired training than from control animals. In contrast, excitatory input to buccal neuron B4/5 in response to stimulation of AT(4) was not significantly increased by paired training. Moreover, correlates of classical conditioning were specific to stimulation of AT(4). The number of spontaneously occurring BMPs and the intrinsic properties of two buccal neurons (B4/5 and B31/32) did not differ between groups. These results suggest that appetitive classical conditioning of feeding resulted in the pairing-specific strengthening of the polysynaptic pathway between afferent fibers and pattern-initiating neurons of the buccal central pattern generator.

Behavioral andIn VitroCorrelates of Compulsive-Like Food Seeking Induced by Operant Conditioning inAplysia

“…These feeding networks have also been found to be the target sites for other types of functional plasticity induced by associative learning both in vivo and via equivalent paradigms of sensory nerve stimulation in vitro (Nargeot et al, 1999a,b;Lechner et al, 2000b;Mozzachiodi et al, 2003;Lorenzetti et al, 2006) and therefore offer the most likely cellular loci for the behavioral plasticity described in the present study.…”

“…The central neural circuitry that drives radula movements is contained in the bilaterally symmetrical buccal ganglia (Elliott and Susswein, 2002) and is already known to provide a neuronal locus for different forms of operant and classical conditioning of feeding-related behavior both in vivo (Lechner et al, 2000b;Brembs et al, 2002) and in vitro (Nargeot et al, 1999a,b;Mozzachiodi et al, 2003). Therefore, in a first step toward a cellular examination of the behavioral plasticity described in the present study, an additional series of control, contingently and noncontingently trained animals (12 in each case) was used to assess whether the buccal ganglia after isolation in vitro were still able to express essential features of the operant conditioning of radula movements that were previously induced in vivo.…”

Cognition in Invertebrates

“…Changes in neuronal activity and cellular properties that were recorded following tactile conditioning occur at all levels of the system, including central sensory pathways, modulatory interneurons, central pattern generator (CPG) interneurons, and motoneurons involving several possible plasticity sites. Aplysia biting behavior can be conditioned similarly (Lechner et al, 2000a(Lechner et al, , 2000b. A brief touch to the lips with a small brush (CS) does not usually elicit a bite.…”

“…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.…”

Neural Analog of Arousal: Persistent Conditional Activation of a Feeding Modulator by Serotonergic Initiators of Locomotion

“…Tail shock or direct stimulation of P9 mimics noxious sensory inputs and has been used extensively as a reinforcement for sensitization paradigms (Walters et al, 1983;Mackey et al, 1989;Marinesco et al, 2004). Branch 4 of the AT (AT 4 ) carries sensory information from the head (Lechner et al, 2000), and stimulation of this nerve has been used as a conditioned stimulus for classic conditioning of feeding responses (Lechner et al, 2000;Mozzachiodi et al, 2003;Brembs et al, 2004).…”