Neural circuits for taste. Excitation, inhibition, and synaptic plasticity in the rostral gustatory zone of the nucleus of the solitary tract.

Abstract

The rostral nucleus of the solitary tract (rNST) plays a key role in modulating, organizing and distributing the sensory information arriving at the central nervous system from gustatory receptors. However, except for some anatomical studies of rNST synapses, the neural circuits responsible for this first stage in synaptic processing of taste information are largely unknown. Over the past few years we have used an in vitro brain slice preparation of the rNST to study synaptic processing, and it has become apparent that the rNST is a very complex neural relay. Synaptic potentials recorded in rNST neurons resulting from stimulation of afferent taste fibers are a composite of excitatory and inhibitory post synaptic potentials. Pure excitatory postsynaptic potentials (EPSP) can be isolated by using gamma-aminobutyric acid type A (GABAA) receptor blockers to eliminate the inhibitory postsynaptic potentials (IPSP). Application of glutamate ionotropic receptor blockers effectively eliminates all postsynaptic activity, indicating that glutamate is the transmitter at the first central synapse in the taste pathway. Stimulation of the afferent taste fibers originating from the anterior (chorda tympani) and posterior (glossopharyngeal) tongue results in a postsynaptic potential that is a complex sum of the two individual potentials. Thus, rNST neurons receive convergent synaptic input from the anterior and posterior tongue. The IPSP component of the synaptic potentials in rNST results from stimulation of interneurons. If these IPSPs are initiated by tetanic stimulation they undergo both short-term and long-term changes. Short-term changes result in the development of biphasic depolarizing IPSPs, and long-term changes result in potentiation of the IPSPs that can last over an hr in some neurons. This remarkable synaptic plasticity may be involved in the mechanism of learned taste behaviors. Synaptic transmission in rNST consists of excitation combined with inhibition. The inhibition does not simply depress excitation but probably serves many roles such as shaping and limiting excitation, coordinating the timing of synaptic events and participating in synaptic plasticity. Knowledge of these synaptic mechanisms is essential to understanding how the rNST processes taste information.