Shin-Ichi Ito

Response properties of the parabrachio-thalamic taste and mechanoreceptive neurons in rats

SummaryA total of 66 taste and 33 mechanoreceptive neurons were isolated from the parabrachial nucleus (PB) of rats. Among them, 39 taste and 8 mechanoreceptive neurons were identified as parabrachio-thalamic relay (P-T) neurons on the basis of antidromic activation from either or both sides of the thalamic taste areas (TTAs). On average, the P-T taste neurons produced larger response magnitudes than the non-P-T taste neurons, and whereas about half the P-T taste neurons were NaCl-best, only a small number of the non-P-T taste neurons were NaCl-best. Both the P-T and non-P-T taste neurons showed a similar breadth of responsiveness to four basic taste stimuli. The response magnitudes of the P-T taste neurons to all taste stimuli were ca. 3 times larger than those of the solitario-parabrachial relay (SP) neurons (afferents to the PB); in particular, the response magnitudes of the NaCl-best P-T neurons were 4–5 times larger than those of the NaCl-best SP neurons. The response magnitudes and breadth of taste responsiveness of the P-T taste neurons were reciprocally correlated with the antidromic latencies from either side of the TTAs. A histological examination revealed that the P-T taste neurons in the ventral part of the PB had a shorter antidromic latency from the ipsilateral TTA than those in the dorsal part of the nucleus. Mechanoreceptive neurons were excited by stroking the tissue in the oral cavity or perioral tissue, or by pinching them with non-serrated forceps. The mechanoreceptive P-T neurons were also activated from either or both sides of the TTAs. No particular relation was noticed between the antidromic latency of the mechanoreceptive P-T neurons and their response properties or locations in the nucleus.

Taste area in granular and dysgranular insular cortices in the rat identified by stimulation of the entire oral cavity

While applying natural stimulation to the entire oral cavity, we recorded responses from 489 neurons (400 mechanoreceptive, 84 taste and 5 cold neurons) in the insular cortex of urethane-anesthetized rats. Intermingled with the mechanoreceptive neurons was a major group of taste neurons located in the granular or dysgranular insular area at levels of 2.55-1.20 mm anterior to the bed nucleus of the anterior commissure as stereotaxically located. Most of the taste neurons were also sensitive to mechanical stimulation of the oral and/or perioral tissue.

Oral cavity representation at the frontal operculum of macaque monkeys

Receptive properties of neurons at areas 3 and 1-2, and the gustatory area (area G) in the frontal operculum (Fop) and the neighboring areas were investigated in the cerebral cortex of Macaca irus and Macaca fuscata by applying mechanical and taste stimulation to the oral cavity and lips. Tactile neurons with different receptive properties were noted in areas 3, 1-2 and G. Areas 3 and G were packed with tongue neurons, though a considerable number of palate neurons were also found in area G, while area 1-2 was involved in representation of the tongue, palate, periodontia and lips. Both the anterior and posterior parts of the tongue were represented on these areas, and of the palate, the posterior part (the soft palate) was largely represented. The anterior and posterior periodontia were represented, without separation. Various tissues were represented with different laterality: Periodontia and the lips were most frequently represented bilaterally or contralaterally, but the tongue and palate often ipsilaterally. In area 6, the insula and other areas surrounding areas 3, 1-2 and G, tactile neurons were also found to have receptive fields on the lips, tongue, palate or periodontium, and the receptive fields on the tongue or palate were mainly bilateral. On the other hand, most of the taste neurons were located in area G and some in area 1-2 and the insula. The present study demonstrated that in macaque monkeys, tactile sensation of the oral cavity is represented on areas 3, 1-2 and G in the Fop as well as on the surrounding areas (e.g., area 6 and the insula), and taste sensation on areas G and 1-2 and the insula.

Location and taste responses of parabrachio-thalamic relay neurons in rats

Thirty of the 55 taste units in the parabrachial nucleus were activated antidromically by stimulation of either or both of the ipsi- or contralateral thalamic taste areas. Such parabrachio-thalamic taste relay neurons produced bilateral thalamic afferent fibers (B type, N = 14), exclusively ipsilateral thalamic afferent fibers (I type, N = 12), or exclusively contralateral thalamic afferent fibers (C type, N = 4). Most of the B-type neurons were excited best by NaCl among the four basic taste stimuli; approximately one-half the I-type neurons by HCl. Most of the NaCl-best neurons were located in the medial part of the parabrachial nucleus but most of the HCl-best neurons were in the lateral part. In addition, NaCl-best neurons had shorter ipsilateral latencies (modal value = 1.0 to 3.0 ms) from the ipsilateral thalamic taste area, whereas HCl-best neurons had longer latencies (modal value = 4.0 to 6.0 ms).

Possible representation of somatic pain in the rat insular visceral sensory cortex: a field potential study

Vagus nerve stimulation evokes a potential in the dorsal insular cortex in rats. To determine whether this cortical visceral area, like the brainstem visceral nuclei, also receives somatic input, somatic potentials were examined. Subcutaneous electrical stimulation, regardless of the laterality and site, evoked a potential closely resembling the vagal potential in shape, surface distribution and depth profile. This somatic potential had a higher threshold and a longer latency than the potentials in the nearby somatosensory cortices, and was attributed to primary Adelta afferents based on conduction velocity measurements and the relationship to peripheral nerve activity. No Abeta afferent-related response was found. These results suggest that the insula receives convergent sensory input from both the viscera and body surface, and the latter probably conveys somatic nociceptive information.

Responses of solitary tract nucleus neurons to taste and mechanical stimulations of the oral cavity in decerebrate rats.

SummaryPhysiological characteristics of 45 taste and 15 mechanoreceptive units were examined in the solitary tract nucleus (NTS) of rats decerebrated at the pre-or midcollicular level, and compared with previous findings in the intact rat. The rostro-caudal extent of the area, where taste and mechanoreceptive neurons were recorded, was almost the same in the decerebrate rat as that in intact rat. The spontaneous discharge rate was significantly lower in the decerebrate rat than in the intact rat. The taste profile of the NTS units in decerebrate rats was quite different from that in intact rats; significant decreases in correlation coefficients were found between certain pairs of taste stimuli and spontaneous discharge rate, e.g. NaCl-quinine, sucrose-quinine. A large number of taste (18 of 31) and mechanoreceptive (12 of 15) units examined had receptive fields (RFs) on the palate, and four taste and two mechanoreceptive units on the circumvallate area. This contrasts with the findings in the intact rat. Some taste (n = 1) and mechanoreceptive units (n = 2) had large RFs. Taste units with different RF locations showed different taste profiles. Acute i.v. injection of amobarbital sodium affected only the response magnitude of taste units, suggesting that most of the differences between intact and decerebrate rats might be caused by decerebration. The present findings indicate that neural structures above the pre- or midcollicular level have tonic inhibitory or facilitatory effects on the response properties of NTS taste units.

Electrophysiological evidence for projections of myelinated and non-myelinated primary vagal afferents to the rat insular cortex

Two types of vagal evoked potentials were recorded in chloralose-anesthetized rats: a positive-negative one and a negative-positive one in granular and agranular insular cortical subareas, respectively, the former being more susceptible to barbiturate. Both potentials consisted of two subtypes which were distinct as to threshold and latency. Peripheral conduction velocities as well as thresholds of these two subtypes corresponded to myelinated and non-myelinated primary afferents, respectively. Thus, these two primary vagal afferents are probably both represented in two insular cortical subareas, through pharmacologically distinct pathways.

Receptive field properties of the parabrachio-thalamic taste and mechanoreceptive neurons in rats

SummaryReceptive fields (RFs) of 36 taste (the 22 parabrachio-thalamic relay (P-T) and 14 non-P-T) and 23 mechanoreceptive neurons (7 P-T and 16 non P-T) were located in the oral cavity of rats. All of the taste and most of the mechanoreceptive units examined had an RF on the ipsilateral side of the tongue or palate, but some mechanoreceptive P-T and non-P-T units had RFs bilaterally. When the RFs of taste neurons were examined with the most effective of the four basic taste (the best stimulus) and non-best stimuli, no difference was noticed in the location of RFs between the P-T and non-P-T neurons. Though most of the P-T neurons (7/11) and all of the non-P-T neurons (6/6) had an RF for non-best stimuli at a region similar to that for the best stimulus, some P-T neurons (4/11) had an RFs for non-best stimulus outside the RF for the best stimulus and/or on the region separate from the RF for the best stimulus. The P-T neurons, responding vigorously to non-optimal stimuli as well as to the best stimulus, had an RF outside the RF for the best stimulus. RFs for mechanical stimulation were also examined in some taste and mechanoreceptive neurons. The mechanoreceptive P-T units rarely had an RF exclusively on the palate. Some mechanoreceptive units had an RF on the region where no taste RF has been found, e.g. the intermolar eminence and the folium of the hard palate.

Cytochrome oxidase staining facilitates unequivocal visualization of the primary gustatory area in the fronto-operculo-insular cortex of macaque monkeys

Fronto-opercular and insular cortices of Japanese macaques were histochemically stained for cytochrome oxidase activity. The laminated pattern of enzyme activity differed in the different cytoarchitectonic areas. Area G, the presumed primary gustatory area, as well as area 3 were prominent because the third stripe, corresponding to the termination layers of the specific thalamocortical projection in these areas was very dark and thick in comparison with that from the neighboring areas. This approach provides a convenient histological aid for identification of area G.

Neuronal activity in the monkey fronto-opercular and adjacent insular/prefrontal cortices during a taste discrimination GO/NOGO task: response to cues

The neural coding of taste information in the fronto-opercular cortex (Fop) and the orbitofrontal area (OFA) was investigated by recording neural activities in monkeys performing a NaCl-water discrimination GO/NOGO task. Responses to GO (NaCl) and NOGO cues (water) were recorded from 160 neurons, of which 118 differentially responded to two cues (differential, Dif neurons), and 42 showed the same response (non-differential, ND neurons). Differential neurons included equal numbers of GO- and NOGO-dominant subtypes. Dif and ND neurons may code for different cues, e.g., taste and touch, as shown by our previous study [Jpn. J. Physiol. 44 (1994) 141]. The response latency of neurons in the exposed Fop was distributed with two modes, one at the shortest bin (100 ms) and one at the bin of 400-800 ms, but neurons in the buried Fop and OFA all had long latency. Such a difference between the two cortical groups of neurons suggests different roles in taste discrimination tasks. Most neurons did not show changes in the discharges or latency with varying concentrations of NaCl. The results indicate that neurons in the areas surveyed code for taste information differently in the task-performing state compared with the non-behaving state examined in previous studies.