Gustatory responses of cortical neurons in rats. I. Response characteristics.

Abstract

The responses of 111 cortical neurons to the four classical taste stimuli (sucrose, NaCl, HCl, and quinine HCl) applied to the anterior part of the tongue were recorded extracellularly in lightly anesthetized rats. Basic response properties of these cortical taste neurons were analyzed. The location of 88 of 111 neurons were histologically identified. They were distributed from anterodorsal to posteroventral direction in the insular cortex just dorsal to the rhinal sulcus and ventral to the somatic sensory area I. The receptive fields of 17 cortical neurons were examined. Most (94%) of the neurons had a narrow focus on the ipsilateral, contralateral, or bilateral sides of the tongue surface. Half of the foci were surrounded by a less-sensitive receptive field of relatively wide size. No apparent relationship was detected between the location of the cortical neurons and the site or extent of the receptive fields of those neurons, indicating a lack of topographical organization in the cortical gustatory area. The mean rate of the spontaneous discharges was 7.1 impulses/3 s, which is about 3 times larger than that in a first-order taste nerve (chorda tympani). The statistically significant difference of spontaneous discharges among response types of cortical neurons was observed only between the neurons responding in an excitatory manner to only one or two kinds of basic stimuli (6.2 impulses/3 s) and the neurons responding in an inhibitory manner to more than three kinds of taste stimuli (14.2 impulses/3 s). When the net responses (spontaneous rate subtracted) to each of the four tastes were compared with the spontaneous discharges in each neuron, the magnitude of spontaneous discharges was significantly negatively correlated with the net response to sucrose. This fact indicates that a neuron with a larger spontaneous discharge rate has a tendency to respond less to sucrose. Response characteristics of cortical taste neurons were quite distinct from those of the first-order taste neurons in the following respects: 1) a decrease in the average evoked discharge rate, which resulted in a small signal-to-noise ratio; 2) a tendency toward equalization of effectiveness of the four basic taste stimuli; 3) about 27% of the neurons decreased their firing rate during the first 3 s after the onset of taste stimulation; and 4) no clear initial phasic response, with a fluctuation in impulse discharges in some neurons.(ABSTRACT TRUNCATED AT 400 WORDS)