Classical and operant conditioning differentially modify the intrinsic properties of an identified neuron

Lorenzetti, Fred D.; Mozzachiodi, Riccardo; Baxter, Douglas A.; Byrne, John H.

doi:10.1038/nn1593

Cited by 79 publications

(92 citation statements)

References 12 publications

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“…Ideally, the question of whether classical and operant conditioning involve similar mechanisms should be addressed by analyzing both types of learning of the same behavior. This is becoming possible for feeding in Aplysia (Lechner et al, 2000a,b;Mozzachiodi et al, 2003;Brembs et al, 2004;Lorenzetti et al, 2006) and should now be possible for gill withdrawal as well.…”

Section: Discussionmentioning

confidence: 99%

Operant Conditioning of Gill Withdrawal inAplysia

2006

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A basic question in neuroscience is how different forms of learning are related. To further address that question, we examined whether gill withdrawal in Aplysia, which has already been studied extensively for neuronal mechanisms contributing to habituation, sensitization, and classical conditioning, also undergoes operant conditioning. Animals were run in pairs. During the initial training period, the contingent (experimental) animal received a siphon shock each time its gill relaxed below a criterion level, and the yoked control animal received a shock whenever the experimental animal did, regardless of its own gill position. This was followed by an extinction period when there was no shock, a retraining period when both animals were contingent, and another extinction period. The experimental animals spent more time with their gills contracted above the criterion level than did the control animals during each period, demonstrating operant conditioning. The type of gill behavior modified by learning shifted over time: the experimental animals had a larger increase in the frequency and duration of spontaneous contractions than did the control animals during the first but not the last extinction period and a larger increase in the level of tonic contraction during the last but not the first extinction period. Because many of the neurons controlling spontaneous and tonic gill withdrawal have already been identified, it should now be possible to examine the cellular locus and mechanism of operant conditioning and compare them with those for other forms of learning of the same behavior.

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Section: Discussionmentioning

confidence: 99%

Operant Conditioning of Gill Withdrawal inAplysia

2006

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“…Previously, it was demonstrated that different aspects of Aplysia feeding can be modified by food intake or buccal sensory nerve stimulation through classical or operant conditioning (Susswein et al, 1986;Lechner et al, 2000a,b;Brembs et al, 2002;Lorenzetti et al, 2006). Insights into the neuronal networks that generate Aplysia feeding, particularly those governing biting movements of the rasp-like radula, have derived from the use of isolated preparations of the buccal ganglia that contain the underlying motor circuitry.…”

Section: Introductionmentioning

confidence: 99%

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

Nargeot¹,

Petrissans²,

Simmers³

2007

J. Neurosci.

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Motivated behaviors comprise appetitive actions whose occurrence results partly from an internally driven incentive to act. Such impulsive behavior can also be regulated by external rewarding stimuli that, through learning processes, can lead to accelerated and seemingly automatic, compulsive-like recurrences of the rewarded act. Here, we explored such behavioral plasticity in Aplysia by analyzing how appetitive reward stimulation in a form of operant conditioning can modify a goal-directed component of the animal's food-seeking behavior. In naive animals, protraction/retraction cycles of the tongue-like radula are expressed sporadically with highly variable interbite intervals. In contrast, animals that were previously given a food-reward stimulus in association with each spontaneous radula bite now expressed movement cycles with an elevated frequency and a stereotyped rhythmic organization. This rate increase and regularization, which was retained for several hours after training, depended on both the reward quality and its contingency because accelerated, stereotyped biting was not induced in animals that had previously received a less-palatable food stimulus or had been subjected to nonassociative reward stimulation. Neuronal correlates of these learning-induced changes were also expressed in the radula motor pattern-generating circuitry of isolated buccal ganglia. In such in vitro preparations, moreover, manipulation of the burst frequency of the bilateral motor pattern-initiating B63 interneurons indicated that the regularization of radula motor pattern generation in contingently trained animals occurred separately from an increase in cycle rate, thereby suggesting independent processes of network plasticity. These data therefore suggest that operant conditioning can induce compulsive-like actions in Aplysia feeding behavior and provide a substrate for a cellular analysis of the underlying mechanisms.

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“…Successful swallowing is presumably signaled by the esophageal nerves. In other learning paradigms affecting Aplysia feeding, the esophageal nerves have a key role in learning (Nargeot et al 1997(Nargeot et al , 2007Lechner et al 2000;Mozzachiodi et al 2003;Brembs et al 2004;Lorenzetti et al 2006). In both classical and operant conditioning, esophageal nerve stimuli contingent on other stimuli lead to increased feeding.…”

Section: Learning With Edible Foodsmentioning

confidence: 99%

“…Classical and operant conditioning tasks depending on two contingent events affect Aplysia feeding (Nargeot et al 1997(Nargeot et al , 2007Lechner et al 2000;Brembs et al 2002Brembs et al , 2004Mozzachiodi et al 2003;Lorenzetti et al 2006). In these tasks, an unconditional stimulus or a reinforcer from the esophageal nerve is paired with a conditional stimulus or an operant, or with their neural analogs.…”

Section: Cellular Basis Of Learning a Triple Contingencymentioning

confidence: 99%

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Nitric oxide and histamine signal attempts to swallow: A component of learning that food is inedible inAplysia

Katzoff¹,

Miller²,

Susswein³

2009

Learn. Mem.

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Memory that food is inedible in Aplysia arises from training requiring three contingent events. Nitric oxide (NO) and histamine are released by a neuron responding to one of these events, attempts to swallow food. Since NO release during training is necessary for subsequent memory and NO substitutes for attempts to swallow, it was suggested that NO functions during training as a signal of attempts to swallow. However, it has been shown that NO may also be released in other contexts affecting feeding, raising the possibility that its role in learning is unrelated to signaling attempts to swallow. We confirmed that NO during learning signals attempts to swallow, by showing that a variety of behavioral effects on feeding of blocking or adding NO do not affect learning and memory that a food is inedible. In addition, histamine had effects similar to NO on learning that food is inedible, as expected if the transmitters are released together when animals attempt to swallow. Blocking histamine during training blocked long-term memory, and exogenous histamine substituted for attempts to swallow. NO also substituted for histamine during training. Histamine at concentrations relevant to learning activates neuron metacerebral cell (MCC). However, MCC activity is not a good monitor of attempts to swallow during training, since the neuron responds equally well to other stimuli. These findings support and extend the hypothesis that NO and histamine signal efforts to swallow during learning, acting on targets other than the MCC that specifically respond to attempts to swallow.

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Classical and operant conditioning differentially modify the intrinsic properties of an identified neuron

Cited by 79 publications

References 12 publications

Operant Conditioning of Gill Withdrawal inAplysia

Operant Conditioning of Gill Withdrawal inAplysia

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

Nitric oxide and histamine signal attempts to swallow: A component of learning that food is inedible inAplysia

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