Synaptic characteristics of rostral nucleus of the solitary tract neurons with input from the chorda tympani and glossopharyngeal nerves

Abstract

Chorda tympani (CT) and glossopharyngeal (IXth) nerves relay taste information from anterior and posterior tongue to brainstem where they synapse with second order neurons in the rostral nucleus of solitary tract (rNST). rNST neurons monosynaptically connected to afferent gustatory input were identified both by anatomical labeling and synaptic latency measures. Anterograde tracing was used to label the CT and IXth terminal fields, and neurons surrounded by fluorescent neural profiles visualized with differential interference contrast (DIC) optics in horizontal brainstem slices. Anatomically identified neurons were patch-clamped and excitatory postsynaptic currents (EPSCs) evoked by electrically stimulating the solitary tract (ST) under GABA(A) receptor blockade. Monosynaptic connections were confirmed by measures of the standard deviation of synaptic latency (jitter). rNST neurons responded to ST stimulation with either all-or-none or graded amplitude EPSCs. Most (70%) of the rNST neurons with CT input and 30% with IX input responded with all-or-none EPSCs. The remainder of the neurons with CT and IX input responded with increasing EPSC amplitudes to greater intensity stimulus shocks. EPSCs evoked in rNST neurons by increasing shock frequency to both CT and IXth nerves resulted in reduced amplitude EPSCs characteristic of frequency-dependent synaptic depression. Our results suggest that the second order rNST neurons respond to afferent input with different patterns of EPSCs that potentially influence transmission of gustatory information. Frequency-dependent synaptic depression would act as a low pass filter important in the initial processing of gustatory derived sensory messages.

Fig. 1

Characterization of monosynaptic contacts between gustatory afferent input and second order rNST neurons. A. Examples of DIC images of rNST neurons surrounded by labeled afferent profiles. The profiles surrounding the neurons on the left resulted from Alexa Fluor dextran 488 (green) applied to the CT and the profiles surrounding the neurons on the right resulted from Alexa Fluor dextran 568 (red) applied to the IX nerve. Examples of the labeled profiles are indicated by white arrow heads. Bar = 10 μm. B. Location of a subset of the recorded neurons. Lucifer yellow labeled neurons with definite co-ordinates were mapped relative their position rostral to the obex and lateral to the midline of the brainstem. C Distribution of synaptic latencies evoked by ST stimulation for neurons with input from the CT and IX nerves. D. Distribution of the standard deviation of synaptic latency (jitter) for neurons with input from the CT and IX nerves.

Fig. 2

A. EPSC evoked by increasing intensity stimulation of the ST. Once threshold is exceeded a constant amplitude all-or-none EPSC is evoked. B. Relationship between stimulus current intensity and EPSC amplitude that is characteristic of all-or-none EPSCs. C. EPSC evoked by increasing intensity stimulation of the ST characterized by a graded amplitude response. D. Relationship between stimulus current intensity and EPSC amplitude that is characteristic of graded EPSCs

Fig. 3

Frequency dependence of EPSCs evoked by ST stimulation. A. EPSCs evoked in an rNST neuron at frequencies of 0.5, 5, 10, 20 and 50 Hz. At higher frequencies the amplitude of the EPSCs declined when compared to the first evoked EPSC. Note the different timescale for the 0.5 Hz trace. B. and C. Relationship of EPSC amplitude at each stimulus frequency shock to the ST as a percentage of the amplitude of the EPSC evoked by the first (control) stimulus.