Tomio Hayama

Responsiveness of solitario-parabrachial relay neurons to taste and mechanical stimulation applied to the oral cavity in rats

SummaryA total of 311 units, responsive to natural stimulation of the oral cavity, were isolated from the rostral part of the solitary tract nucleus (NTS) of rats. Of these, 169 “taste neurons”, activated by taste stimulation, and 142 mechanoreceptive units, exclusively sensitive to mechanical stimulation of the oral cavity, were found. Most taste units (62.3%) were also excited by mechanical stimulation. Forty-three (34.1%) of the 126 taste units examined were identified as solitario-parabrachial relay (SP) neurons by antidromic stimulation from the ipsilateral dorsal pons, while only eleven (12.6%) of the 87 mechanoreceptive units were SP neurons. Taste SP neurons could be divided into two subgroups according to their antidromic latency; the fast SP units with an antidromic latency shorter than 9 ms and slow SP units with a longer antidromic latency. These two subgroups were not differentiated in any physiological properties except that the fast SP neurons were frequently excited by sucrose. Taste neurons were classified according to the best stimulus of the four basic taste solutions to produce the largest number of discharges in each neuron. All types of taste neurons were found among the SP and non-SP neurons, but only a small number of quinine-best neurons (n = 2) were found in the SP neuron group compared to the number of quinine-best neurons in the non-SP neuron group (n = 10). A histological examination of the recording sites revealed that taste relay neurons were found at the central or dorsal part of the nucleus but mechanoreceptive relay neurons were found at the peripheral part, although relay and non-relay neurons of either class were intermingled in the nucleus.

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.

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).

Receptive fields of solitario-parabrachial relay neurons responsive to natural stimulation of the oral cavity in rats.

SummaryThe receptive field (RF) of 67 taste and 85 mechanoreceptive neurons in the solitary tract nucleus (NTS) were located in the oral cavity in albino rats. All of the taste and most (62.4%) of the mechanoreceptive neurons examined had an RF on the ipsilateral side of the tongue and/or the palate. Regardless of whether they were solitario-parabrachial relay (SP) neurons or non-SP neurons, RFs of taste neurons were found on the anterior as well as the posterior tongue. But there were some differences in the RF distribution between the SP and non-SP mechanoreceptive neurons. Most of the mechanoreceptive SP neurons (9 of 11) had an RF on the tongue, while ca. half of the mechanoreceptive non-SP neurons (43 of 79) had an RF on the tongue and palate, but the rest had an RF on other tissue. Most of the neurons studied had a small restricted RF, but complex RFs, e.g. two separate RFs on the tongue, were found in a relatively small number of neurons (four taste and five mechanoreceptive neurons). An inhibitory RF, usually in a remote place from the excitatory RFs, was found in four mechanoreceptive neurons but no inhibitory RFs for taste neurons. Electrical stimulation of the epithelium in the RF with a low current of short duration evoked a few spikes in most units. Two of the three units, giving rise to a vigorous response to taste stimulation, but having single restricted RFs on the anterior tongue, produced a train of spikes lasting more than 20 ms in response to electrical stimulation of the RF. Neurons with RFs on the anterior tongue and those with RFs on the posterior tongue were located in different regions in the NTS, suggesting a possible somatotopic representation of the oral cavity in the nucleus. RFs of neither taste neurons nor mechanoreceptive neurons could be found in the tongue region containing the circumvallate papilla. The possible reasons are discussed.

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.

Thermal sensitivity of neurons in a rostral part of the rat solitary tract nucleus.

While stimulating the entire oral cavity of anesthetized rats, we recorded 3 types of neurons in the solitary tract nucleus; taste, mechanoreceptive and cold neurons. Most of the taste neurons were sensitive to thermal as well as to mechanical stimulations. Taste neurons predominantly sensitive to sucrose responded to warming and those most excited by NaCl or HCl were sensitive to cooling, and significant correlations were found between sucrose and warming and between NaCl and cooling. Most of the cold-sensitive taste neurons had receptive fields (RFs) at the anterior tongue and warm-sensitive taste neurons had whole or part of the RFs at the nasoincisor duct. About half the number of mechanoreceptive neurons were sensitive to cooling, producing phasic responses. RFs of some thermosensitive mechanoreceptive neurons and cold neurons were located. Warm-sensitive mechanoreceptive neurons or warm neurons were not evident. Therefore, interaction between thermal and taste sensations in the oral cavity probably takes place in the solitary tract nucleus, as well as in the chorda tympani.

Taste relay neurons in the solitary tract nucleus of rats.

Impulse discharges of 82 solitary tract nucleus neurons, in response to natural stimulation of the oral cavity, were recorded. Among these, 52 units responded to taste stimuli and 30 units to mechanical stimuli. When the caudal end of the parabrachial nucleus was stimulated ipsilaterally, 16 taste and 5 mechanoreceptive units were excited antidromically. Response types of rostrally projecting taste neurons were not different from those of the non-projecting ones, and both of them were similar to that of the chorda tympani.

Anatomical location of a taste-related region in the thalamic reticular nucleus in rats

To locate a taste-related region in the thalamic reticular nucleus (Rt), we explored a reticular region having connections with the thalamic taste relay and the cortical taste area (CTA), by neuronal tracing methods using HRP, WGA-HRP and biocytin. Tracer injections at the thalamic taste relay, i.e., the parvicellular part of the thalamic posteromedial ventral nucleus (VPMpc), labeled cell bodies and axon terminals in a confined portion of the ipsilateral Rt. This was located at the ventromedial-most portion of the nucleus at the level of approx. 1.2 mm rostral to the rostral end of the VPMpc. Tracer injections at the CTA ipsilaterally labeled axon terminals in the same region of the Rt, as did the thalamic injections. When WGA-HRP was injected at this taste-related region in the Rt, we observed labeled cell bodies in layer VI in the CTA; in the VPMpc we saw densely labeled axon terminals but few, if any, labeled cell bodies. The results indicated that the taste-related region in the Rt receives input from the VPMpc and CTA, and sends output to the VPMpc. They also showed that the reticulo-thalamic projections were much heavier than the thalamo-reticular ones in the taste system.

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.

Electrophysiological evidence of collateral projections of parabrachio-thalamic relay neurons

We studied axonal branching of 14 parabrachial nucleus neurons, activated antidromically from 2 of the 3 stimulation sites, i.e. the ipsi- and contralateral thalamic taste area (TTAs) and the ipsilateral central nucleus of the amygdala (CA). Making use of antidromic latencies, collision times and refractory periods at the 2 sites of stimulation, the conduction times were calculated for the distance between the branching point of the axon and the stimulation sites or the recording site at the soma. Nine of these 14 neurons had a significant length of axon branches terminating at 2 of the 3 sites of stimulation. Five neurons sent axon branches to the bilateral TTAs, 3 to both the CA and the ipsilateral TTA and the remaining one to both the CA and the contralateral TTA. Four of these 9 neurons with collateral branches responded to taste stimulation.