Decline in the Recovery from Synaptic Depression in Heavier Aplysia Results from Decreased Serotonin-Induced Novel PKC Activation

Tyler William Dunn,Wayne S Sossin,Riccardo Mozzachiodi

doi:10.1371/journal.pone.0136907

Tyler William Dunn, Wayne S Sossin + Show 1 more

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https://doi.org/10.1371/journal.pone.0136907

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Abstract

The defensive withdrawal reflexes of Aplysia are important behaviors for protecting the animal from predation. Habituation and dishabituation allow for experience-dependent tuning of these reflexes and the mechanisms underlying these forms of behavioral plasticity involve changes in transmitter release from the sensory to motor neuron synapses through homosynaptic depression and the serotonin-mediated recovery from depression, respectively. Interestingly, dishabituation is reduced in older animals with no corresponding change in habituation. Here we show that the cultured sensory neurons of heavier animals (greater than 120g) that form synaptic connections with motor neurons have both reduced recovery from depression and reduced novel PKC Apl II activation with 5HT. The decrease in the recovery from depression correlated better with the size of the animal than the age of the animal. Much of this change in PKC activation and synaptic facilitation following depression can be rescued by direct activation of PKC Apl II with phorbol dibutyrate, suggesting a change in the signal transduction pathway upstream of PKC Apl II activation in the sensory neurons of larger animals.

Highlights

Habituation and dishabituation of the defensive withdrawal reflexes of the marine mollusk Aplysia have long been examined as simple modifiable behaviors arising from simple underlying neurophysiological changes
Habituation and dishabituation allow for experience-dependent tuning of these reflexes and the mechanisms underlying these forms of behavioral plasticity involve changes in transmitter release from the sensory to motor neuron synapses through homosynaptic depression and the serotonin-mediated recovery from depression, respectively
5HT-mediated recovery from homosynaptic depression is reduced with sensory neurons isolated from animals >120g without changes in 5HTmediated increases in sensory neuron excitability

Summary

Introduction

Habituation and dishabituation of the defensive withdrawal reflexes of the marine mollusk Aplysia have long been examined as simple modifiable behaviors arising from simple underlying neurophysiological changes. Electrophysiological recordings in semi-intact preparations determined that a significant portion of the change in behavior can be attributed to changes in synaptic efficacy of the sensory to motor neuron synapses involved in the reflex [1,2]. The dramatic reduction in postsynaptic potential (PSP) amplitude with low frequency stimulation and the recovery from that depression with either nerve shock or serotonin (5-hydroxytryptamine, 5HT), are the result of presynaptic changes in transmitter release [3,4,5]. Loss of PKC Translocation in Heavier Aplysia between presynaptic sensory neurons and postsynaptic motor neurons in culture using low frequency stimulation of the sensory neuron and exogenous 5HT [6]. While the mechanisms of these two forms of plasticity have yet to be fully elucidated, it is known that behavioral dishabituation requires PKC activity in the sensory neuron [7]. Recovery from synaptic depression was shown to depend on 5HT activation of the novel PKC Apl II [8]

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