Identification and characterization of neurons initiating patterned neural activity in the buccal ganglia of Aplysia

Susswein, Abraham J.; Byrne, John H.

doi:10.1523/jneurosci.08-06-02049.1988

Cited by 144 publications

(185 citation statements)

References 33 publications

(41 reference statements)

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“…3A,C). These cells f unction both as pattern initiators and protractor motor neurons (Susswein and Byrne, 1988;. Closure motor neurons B8 contributed to the large-amplitude activity recorded from R n.1, and retractor motor neurons B3, B6, and B9 contributed to the activity recorded from n.2,1 (Fig.…”

Section: Rhythmic Motor Programs Elicited By Tonic Stimulation Of N23mentioning

confidence: 87%

“…Key neural elements underlying these behaviors have been identified in the buccal ganglia. They include sensory neurons (Rosen et al, 1982), pattern-generating cells (Susswein and Byrne, 1988;Plummer and K irk, 1990;, and motor neurons (Morton and Chiel, 1993b;Church and L loyd, 1994). We developed a preparation to examine how a C PG might be modified by operant conditioning.…”

Section: Neural Analog Of Operant Conditioningmentioning

confidence: 99%

See 1 more Smart Citation

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

Nargeot¹,

Baxter²,

Byrne³

1997

J. Neurosci.

111

183

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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...

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Section: Rhythmic Motor Programs Elicited By Tonic Stimulation Of N23mentioning

confidence: 87%

Section: Neural Analog Of Operant Conditioningmentioning

confidence: 99%

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

Nargeot¹,

Baxter²,

Byrne³

1997

J. Neurosci.

111

183

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“…Like the SO in Lymnaea, a variety of buccal neurons are capable of driving rhythmic fictive feeding in Aplysia (Susswein and Byrne, 1988;Kirk, 1989;Teyke et al, 1993;Hurwitz and Susswein, 1996;Kabotyanski et al, 1998), Helisoma (Quinlan et Figure 7. Alternative schemes for the organization of neurons for higher-order control of the Lymnaea feeding CPG.…”

Section: Comparisons With Other Systemsmentioning

confidence: 99%

“…Two of these cell types, the B1 cells of Achatina (Yoshida and Kobayashi, 1992) and the N1a cells of Helisoma (Quinlan et al, 1997), were tested for chemosensory responses, and it was shown that activity in these neurons was not necessary for fictive feeding to occur. N1M-type buccal CPG interneurons also have been found in other molluscan feeding systems (Aplysia, Susswein and Byrne, 1988;Teyke et al, 1993;Clione, Arshavsky et al, 1989;Planorbis, Arshavsky et al, 1988a,b), but their role in the sensory activation of feeding has not yet been investigated.…”

Section: Comparisons With Other Systemsmentioning

confidence: 99%

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

2001

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Modulatory interneurons that can drive central pattern generators (CPGs) are considered as good candidates for decisionmaking roles in rhythmic behaviors. Although the mechanisms by which such neurons activate their target CPGs are known in detail in many systems, their role in the sensory activation of CPG-driven behaviors is poorly understood. In the feeding system of the mollusc Lymnaea, one of the best-studied rhythmical networks, intracellular stimulation of either of two types of neuron, the cerebral ventral 1a (CV1a) and the slow oscillator (SO) cells, leads to robust CPG-driven fictive feeding patterns, suggesting that they might make an important contribution to natural food-activated behavior. In this paper we investigated this contribution using a lip-CNS preparation in which feeding was elicited with a natural chemostimulant rather than intracellular stimulation. We found that despite their CPG-driving capabilities, neither CV1a nor SO were involved in the initial activation of sucrose-evoked fictive feeding, whereas a CPG interneuron, N1M, was active first in almost all preparations. Instead, the two interneurons play important and distinct roles in determining the characteristics of the rhythmic motor output; CV1a by modulating motoneuron burst duration and SO by setting the frequency of the ongoing rhythm. This is an example of a distributed system in which (1) interneurons that drive similar motor patterns when activated artificially contribute differently to the shaping of the motor output when it is evoked by the relevant sensory input, and (2) a CPG rather than a modulatory interneuron type plays the most critical role in initiation of sensory-evoked rhythmic activity.

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“…Various neurons have been identified that are involved in the process of detecting (e.g., Teyke, Weiss, & Kupfermann, 1990a, 1990b and ingesting food (e.g., Cropper, Kupfermann, & Weiss, 1990;Fiore & Meunier, 1979;JahanPawar & Fredman, 1983;Rosen, Miller, Weiss, & Kupfermann, 1988;. Moreover, Susswein and Byrne (1988) have characterized buccal cells that appear to serve as initiators of patterned activity consistent with that observed in the ingestion and rejection of food. Other work has succeeded in identifying several neuropeptides in the buccal cells (Cropper, Miller, et aI., 1990;Cropper, Tenenbaum, Kolks, Kupfermann, & Weiss, 1987;Lloyd, Frankfurt, Stevens, Kupfermann, & Weiss, 1987;Lloyd, Mahon, et aI., 1985) and in characterizing their modulatory effects on specific buccal neurons (Baux, Fossier, Trudeau, & Tauc, 1993;Sossin, Kirk, & Scheller, 1987).…”

Section: Discussionmentioning

confidence: 89%

Pavlovian appetitive discriminative conditioning inAplysia californica

Colwill

Goodrum

Martin

1997

Animal Learning & Behavior

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Three experiments demonstrated Pavlovian appetitive discrimination learning in the marine mollusc, Aplysia californica. In each experiment, subjects were exposed to two conditioned stimuli; one stimulus (CS+) was paired with food presentations and the other stimulus (CS-) was never followed by food. In Experiments 1 and 3 different chemosensory stimuli were used, and in Experiment 2 different tactile stimuli were used. For both types of conditioned stimuli, bite responses occurred significantly more often to the CS+ than to the CS-. Experiment 2 also showed that Aplysia could learn a reversal of this discrimination. Experiment 3 showed that nonreinforced presentations of CS+ resulted in a decline in the frequency of conditioned biting. The implications of these results for neurobiological analyses of learning are discussed.In a typical Pavlovian discriminative conditioning procedure, subjects are exposed to two conditioned stimuli (CSs) that differ in their temporal relation to an unconditioned stimulus (US). One of these stimuli (CS+) immediately precedes presentations of the US; the other stimulus (CS-) is never paired with that US. Differential responding to the CS+ and CS-is found to emerge over the course of discrimination training in various vertebrate (e.g., Hammond, 1967;Hoffman & Fitzgerald, 1982;Moore, 1972;Pavlov, 1927;Rescorla, 1980;Schneiderman, 1972) and invertebrate subjects (e.g., Bitterman, Menzel, Fietz, & Schafer, 1983;Block & McConnell, 1967;Fukushi, 1979;Nelson, 1971;Ricker, Brzorad, & Hirsch, 1986).Of particular interest are reports of Pavlovian discriminative conditioning in those invertebrates especially suited to a neurophysiological analysis of plasticity. Behavioral sensitivity to the differential treatments ofa CS+ and CS -has been found in several experiments using aversive USs with the marine mollusc Aplysia califomica , the leech Haemopis marmorata (Karrer & Sahley, 1988), and the terrestrial mollusc Limax maximus (Sahley, Gelperin, & Rudy, 1981). For example, in the leech, Karrer and Sahley (1988) paired one food (e.g., raw chicken) but not This research was supported by National Science Foundation Grant BNS-8922551 to R.M.C. and by funds from the Howard Hughes Medical Institute. K.G. and A.M. were supported by research fellowships awarded by Brown University's Early Identification Program. We thank Robin Absher and Emily Whitcomb for assistance with data collection. Experiment 1 was presented at the 65th Annual Meeting ofthe Eastern Psychological Association in Providence and at the Second Annual Summer Research Symposium at Brown University in August 1993. A brief description of Experiment 1 also appears in Colwill (1996). Reprint requests should be addressed to R. M. Colwill, Department of Psychology, Brown University, Box 1853, Providence, RI 02912 (e-mail: ruth_colwill@brown.edu).another food (e.g., raw liver) with a quinidine sulfate solution. On test trials, subjects were given a choice between raw beefand either the CS+ or the CS-foods. The preference for the CS+ relative ...

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Identification and characterization of neurons initiating patterned neural activity in the buccal ganglia of Aplysia

Cited by 144 publications

References 33 publications

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

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

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

Pavlovian appetitive discriminative conditioning inAplysia californica

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