Habituation of Reflexes in
            <i>Aplysia</i>
            : Contribution of the Peripheral and Central Nervous Systems

Peretz, Bertram; Jacklet, Jon W.; Lukowi, Kenneth

doi:10.1126/science.1246622

Cited by 65 publications

(86 citation statements)

References 19 publications

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“…Central motor neurons are responsible for most of the gill withdrawal in response to weak-moderate intensity stimulation of the siphon. A peripheral pathway from siphon to gill contributes greatly (15) (15) that, after removal of the central nervous system, the gill withdrawal mediated by the peripheral pathway is, on the average, as large as the response with the central nervous system intact. Differences in findings between the laboratories were agreed to be 2-fold: (i) a "tapper" stimulator (15) evoked large responses after central nervous system removal, a "probe" stimulator (12) (2,3).…”

Section: Discussionmentioning

confidence: 99%

Facilitation at neuromuscular junctions: contribution to habituation and dishabituation of the Aplysia gill withdrawal reflex.

Jacklet¹,

Rine²

1977

Proc. Natl. Acad. Sci. U.S.A.

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The gill withdrawal reflex of Aplysia has been used as a model for studying the neuronal mechanisms of habituation, a behavioral plasticity. We have assessed the contribution of neuromuscular facilitation, an elementary synaptic plasticity, during habituation of the reflex by recording gill muscle potentials, which we show are caused by excitatory junctional potentials. These potentials show systematic frequency-dependent changes in amplitude. The gill withdrawal evoked by central motor neuron firing during each habituation trial is determined by facilitation of the excitatory junctional potentials during the trial and the facilitated state of the initial excitatory junctional potential in a trial, determined by neuron activity prior to the trial. The neuromuscular junctions, therefore, act like a frequency-dependent amplifier of central motor activity. They are fully responsive to the dynamic changes of motor neuron firing that occurs during habituation and especially after dishabituation.The neural correlates of habituation have been extensively studied in three invertebrate preparations, the crayfish (Procambaxrus) (1-3), the locust (Schistocerca) (4), and the sea hare (Apiysia). Habituation, the decrement of a behavioral response with repeated stimulation and its restoration or dishabituation by a novel stimulus, can be studied in these preparations at the level of synaptic communication between neurons. In these animals, and possibly in vertebrates (5), homosynaptic depression at central neuronal synapses has been identified as a mechanism of habituation (1-4, 6, 7).In Aplysia the reflex withdrawal of the gill evoked by siphon stimulation has been used as a model for the study of habituation (7-9). Several central motor neurons participate in this reflex, and studies of motor neuron L7 have shown that it receives excitatory postsynaptic potential (EPSP) input from a cluster of central sensory neurons (10-12). These EPSPs decrease in amplitude with successive stimuli and therefore, as a consequence of a decrease in the number of quanta of transmitter released (13) at the sensory-motor chemical synapses, homosynaptic depression has been proposed as the mechanism of habituation of the reflex (7, 9). The train of action potentials evoked by synaptic input to neuron L7 during behavioral habituation and dishabituation has been shown (9) but the firing of other major motor neurons (LDG1 and LDG2) has not. The firing of L7 decreases slowly during behavioral habituation of the gill and recovers slowly after dishabituation (9). If habituation is caused solely by synaptic depression at sensory-motor synapses (9, 13), the firing of the motor neurons should parallel the evoked gill withdrawal because these neurons synapse directly on gill muscles and are reported to produce temporally stable nondecrementing gill withdrawal (10, 14). However, it was shown that the neuron-gill muscle synapses showed pronounced facilitation (14).We examined the possibility that changes in the efficacy of gill neuromuscular junction...

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Section: Discussionmentioning

confidence: 99%

Facilitation at neuromuscular junctions: contribution to habituation and dishabituation of the Aplysia gill withdrawal reflex.

Jacklet¹,

Rine²

1977

Proc. Natl. Acad. Sci. U.S.A.

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“…Such causal connections have proven to be frustratingly elusive [reviews by Mpitsos and Lukowiak, 1985;Glanzman, 1995;Walters and Cohen, 1997;Leonard and Edstrom, in preparation]. In part, the problems with identifying a specific role for each motor neuron and/or synapse in the behavior must be due to the contribution of a variety of other pathways, both within the PVG and in the peripheral nervous system, that have been found to contribute to gill behavior [Peretz et al, 1976;Mpitsos and Lukowiak, 1985;Zecevic et al, 1989;Leonard et al, 1992;Walters and Cohen, 1997;Kurokawa et al, 1999;Leonard and Edstrom, in preparation]. However, when one reexamines the original circuit described by Kupfermann and colleagues, one sees that the architecture is consistent with a neural network model in which the six PVG gill motor neurons represent a hidden layer without direct synaptic interconnections [ fig.…”

Section: The Modelsmentioning

confidence: 99%

Network Architectures and Circuit Function: Testing Alternative Hypotheses in Multifunctional Networks

Leonard

2000

Brain Behav Evol

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Understanding how species-typical movement patterns are organized in the nervous system is a central question in neurobiology. The current explanations involve ‘alphabet’ models in which an individual neuron may participate in the circuit for several behaviors but each behavior is specified by a specific neural circuit. However, not all of the well-studied model systems fit the ‘alphabet’ model. The ‘equation’ model provides an alternative possibility, whereby a system of parallel motor neurons, each with a unique (but overlapping) field of innervation, can account for the production of stereotyped behavior patterns by variable circuits. That is, it is possible for such patterns to arise as emergent properties of a generalized neural network in the absence of feedback, a simple version of a ‘self-organizing’ behavioral system. Comparison of systems of identified neurons suggest that the ‘alphabet’ model may account for most observations where CPGs act to organize motor patterns. Other well-known model systems, involving architectures corresponding to feed-forward neural networks with a hidden layer, may organize patterned behavior in a manner consistent with the ‘equation’ model. Such architectures are found in the Mauthner and reticulospinal circuits, ‘escape’ locomotion in cockroachs, CNS control of Aplysia gill, and may also be important in the coordination of sensory information and motor systems in insect mushroom bodies and the vertebrate hippocampus. The hidden layer of such networks may serve as an ‘internal representation’ of the behavioral state and/or body position of the animal, allowing the animal to fine-tune oriented, or particularly context-sensitive, movements to the prevalent conditions. Experiments designed to distinguish between the two models in cases where they make mutually exclusive predictions provide an opportunity to elucidate the neural mechanisms by which behavior is organized in vivo and in vitro.

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“…These snails were said to perseverate (defined as an inappropriate repetition of a behaviour). Typically, younger animals perseverate in situations where they are required to withhold a behavioural response (Peretz and Lukowiak, 1975;Peretz et al, 1976). However, Dutch juveniles are capable of both associative learning and LTM for tasks where withholding a behaviour is not required.…”

Section: Introductionmentioning

confidence: 99%

Juveniles ofLymnaeasmart snails do not perseverate and have the capacity to form LTM

Shymansky

Protheroe

Hughes

et al. 2016

Journal of Experimental Biology

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Previously, it was concluded that the nervous systems of juvenile snails were not capable of mediating long-term memory (LTM). However, exposure and training of those juvenile snails in the presence of a predator cue significantly altered their ability to learn and form LTM. In addition, there are some strains of Lymnaea which have been identified as 'smart'. These snails form LTM significantly better than the lab-bred strain. Here, we show that juveniles of two smart snail strains not only are capable of associative learning but also have the capacity to form LTM following a single 0.5 h training session. We also show that freshly collected 'wild' 'average' juveniles are also not able to form LTM. Thus, the smart snail phenotype in these strains is expressed in juveniles.

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Habituation of Reflexes in Aplysia : Contribution of the Peripheral and Central Nervous Systems

Cited by 65 publications

References 19 publications

Facilitation at neuromuscular junctions: contribution to habituation and dishabituation of the Aplysia gill withdrawal reflex.

Facilitation at neuromuscular junctions: contribution to habituation and dishabituation of the Aplysia gill withdrawal reflex.

Network Architectures and Circuit Function: Testing Alternative Hypotheses in Multifunctional Networks

Juveniles ofLymnaeasmart snails do not perseverate and have the capacity to form LTM

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