Long-term sensitization training produces spike narrowing in Aplysia sensory neurons.

Both short- and long-term sensitization of withdrawal reflexes of Aplysia are attributable at least in part to facilitation of the sensorimotor synapse. Previously, short-term synaptic facilitation has been associated with spike broadening and no change in temporal dynamics of burst transmission. In the present study, we examined whether long-term sensitization (LTS) is also associated with spike broadening and whether long-term synaptic facilitation is accompanied by changes in temporal dynamics. The results indicate that the temporal dynamics of the sensorimotor synapse are preserved after long-term facilitation. However, in contrast to short-term sensitization, LTS was accompanied by spike narrowing. The spike narrowing was observed both in centrally triggered spikes in isolated ganglia and in peripherally triggered spikes in reduced tail preparations. In addition, in reduced tail preparations, fewer spike failures in the afferent discharge of sensory neurons occurred in response to tail stimulation after ipsilateral LTS. Collectively, the results reveal that long-term sensitization affects the spike waveform of sensory neurons and enhances the sensory neuron responses to peripheral stimuli, but does not modify the synaptic dynamics of homosynaptic depression.

Long-term sensitization training primes Aplysia for further learning.

Repetitive, unilateral stimulation of Aplysia induces long-term sensitization (LTS) of ipsilaterally elicited siphon-withdrawal responses. Whereas some morphological effects of training appear only on ipsilateral sensory neurons, others appear bilaterally. We tested the possibility that contralateral morphological modifications may have functional significance. Therefore, we examined whether LTS training primes subsequent sensitization. Twenty-four hours after LTS training the effects of brief shock treatment (BST) were examined. BST failed to sensitize animals that had previously received either 4-d control treatment or 4-d ipsilateral LTS training. In contrast, BST did sensitize animals that had previously received 4-d contralateral LTS training, suggesting the presence of a latent trace that primes the animal for further learning.

Learning insights transmitted by glutamate.

Plasticity of the Aplysia sensorimotor synapse plays a crucial role in learning and memory of withdrawal reflexes. During the past ten years, a growing body of evidence has indicated that the sensorimotor synapse is glutamatergic. This new information has guided several studies that implicate AMPA and NMDA receptors in synaptic plasticity. However, further work is necessary to delineate the exact properties of the postsynaptic receptors, and their role in transmission and plasticity. Despite the still incomplete picture of the intrinsic properties of the sensorimotor synapse, identifying the endogenous transmitter has provided a foundation for new avenues of research, the results of which will further improve our understanding of the neurobiology of learning and memory.

Desensitization of postsynaptic glutamate receptors contributes to high-frequency homosynaptic depression of aplysia sensorimotor connections.

Withdrawal reflexes of Aplysia are mediated in part by a monosynaptic circuit of sensory (SN) and motor (MN) neurons. A brief high-frequency burst of spikes in the SN produces excitatory postsynaptic potentials (EPSPs) that rapidly decrease in amplitude during the burst of activity. It is generally believed that this and other (i.e., low-frequency) forms of homosynaptic depression are entirely caused by presynaptic mechanisms (e.g., depletion of releasable transmitter). The present study examines the contribution that desensitization of postsynaptic glutamate receptors makes to homosynaptic depression. Bath application of cyclothiazide, an agent that reduces desensitization of non-NMDA glutamate receptors, reduced high-, but not low-frequency synaptic depression. Thus, a postsynaptic mechanism, desensitization of glutamate receptors, can also contribute to homosynaptic depression of sensorimotor synapses.

Burst-induced synaptic depression and its modulation contribute to information transfer at Aplysia sensorimotor synapses: empirical and computational analyses.

The Aplysia sensorimotor synapse is a key site of plasticity for several simple forms of learning. Plasticity of this synapse has been extensively studied, albeit primarily with individual action potentials elicited at low frequencies. Yet, the mechanosensory neurons fire high-frequency bursts in response to even moderate tactile stimuli delivered to the skin. In the present study, we extend this analysis to show that sensory neurons also fire bursts in the range of 1-60 Hz in response to electrical stimuli similar to those used in behavioral studies of sensitization. Intracellular stimulation of sensory neurons to fire a burst of action potentials at 10 Hz for 1 sec led to significant homosynaptic depression of postsynaptic responses. The depression was transient and fully recovered within 10 min. During the burst, the steady-state depressed phase of the postsynaptic response, which was only 20% of the initial EPSP of the burst, still contributed to firing the motor neuron. To explore the functional contribution of transient homosynaptic depression to the response of the motor neuron, computer simulations of the sensorimotor synapse with and without depression were compared. Depression allowed the motor neuron to produce graded responses over a wide range of presynaptic input strength. In addition, enhancement of synaptic transmission throughout a burst increased motor neuron output substantially more than did preferential enhancement of the initial phase of a burst. Thus, synaptic depression increased the dynamic range of the sensorimotor synapse and can, in principle, have a profound effect on information processing.