Excitatory amino acid neurotransmission at sensory-motor and interneuronal synapses of Aplysia californica

1. Although the gill and siphon withdrawal reflex of Aplysia has been used as a model system to study learning-associated changes in synaptic transmission, the identity of the neurotransmitter released by the sensory neurons and excitatory interneurons of the network mediating this behavior is still unknown. The identification of the putative neurotransmitter of these neurons should facilitate further studies of synaptic plasticity in Aplysia. 2. We report that sensory-motor transmission within this circuit is mediated through the activation of an excitatory amino acid receptor that is blocked by the non-N-methyl-D-aspartate excitatory amino acid receptor antagonists 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) and 1-(4-chlorobenzoyl)-piperazine-2,3-dicarboxylic acid (CBPD). Compound postsynaptic potentials evoked in motor neurons by electrical stimulation of the siphon nerve were blocked by 92% with CNQX (75 microM) and 89% with CBPD (75 microM). 3. Simultaneous intracellular recordings were obtained from sensory neurons, excitatory interneurons, and motor neurons. Monosynaptic excitatory postsynaptic potentials (EPSPs) evoked in motor neurons by an action potential in a sensory neuron were blocked by 86% with CNQX (75 microM) and 71% with CBPD (75 microM). The two antagonists also blocked monosynaptic interneuronal EPSPs onto motor neurons by 65% and 67%, respectively. 4. Potential agonists of the synaptic receptors were puff-applied in the intact abdominal ganglion. Homocysteic acid (HCA) was found to mimic the action of the synaptically released transmitter because it strongly excites motor neurons. This effect was blocked by CNQX. Kainate and domoic acid were also effective agonists. 5. The actions of L- and D-glutamate as well as quisqualate were found to be mainly hyperpolarizing, whereas aspartate and (+/-)-amino-3-hydroxy-5-methylisoxazole-4-propionic acid had no effect. 6. Several reasons may be proposed to explain the inability of puff-applied glutamate to excite effectively the postsynaptic neurons in the intact ganglion. It is possible nonetheless that other endogenous amino acids such as HCA act as neurotransmitters at these synapses.