Neuron and stimulus typologies in the rat gustatory system

Although gustatory neurons may be categorized in terms of one or a few characteristics (e.g. ‘best stimulus’), such typologies are essentialistic and inconsistent with modern taxonomic methods¹⁵. If polythetic taxonomic criteria are used and the variability among neuronal responses is closely analyzed, neuronal ‘types’ are found to disappear, at least within the acid-salt range. This applies to both the primary nerve level (chorda tympani nerve) and secondary level (nucleus tractus solitarius) of the taste system in the rat. In the same context, taste stimuli may fall into different groups if several very similar stimuli are used (e.g. sodium and lithium salts). This is not surprising, and may depend on the choice of stimulus arrays rather than a differentiation of a few stimulus types by the taste system. Finally, it should be noted that the arguments regarding neuron and stimulus typologies presented here for the taste system are also valid for other sensory systems, although the conclusions may be different.     

Cytoarchitecture and topographic projections of the gustatory centers in a teleost, Carassius carassius

The neuronal connections in the central gustatory system of the crucian carp were examined by means of degeneration and HRP methods. Cell morphology in the primary gustatory lobes was studied in Golgi-impregnated material. Medium-sized neurons of the facial lobe emit axons which project to the secondary gustatory nucleus. The nucleus intermedius facialis of Herrick ('05) projects bilaterally. Large neurons send axons through the spinal trigeminal tract to terminate in the spinal trigeminal nucleus and in the medial funicular nucleus. In the vagal lobe, second-order neurons for the ascending projections are located in the superficial part of the sensory zone. These neurons project exclusively to the ipsilateral secondary gustatory nucleus. Neurons located in the deeper part of the sensory zone send axons to the motor zone and to the brainstem reticular formation to form short reflex arcs. The glossopharyngeal lobe has similar neuronal connections to the vagal sensory zone. Both facial and vagal lobes receive afferent projections from the following central structures: nucleus posterioris thalami, nucleus diffusus lobi inferioris, optic tectum, motor nucleus of the trigeminal nerve, medullary reticular formation, and the gray matter of the upper spinal cord. The facial lobe has an additional afferent from the mesencephalic reticular formation. The major sources to the medullary gustatory lobes are the nucleus posterioris thalami and nucleus diffusus lobi inferioris. Each type of neuron classified by morphology and location in the facial, glossopharyngeal, and vagal lobes was correlated with its particular destination. Topographic projections were demonstrated in the secondary and tertiary gustatory centers.     

Tactile input to the facial lobe of the carp,Cyprinus carpio L.

Single unitary discharges in the facial lobe and trigeminofacial nerve trunks of the carp,Cyprinus carpio L., were studied electrophysiologically in response to electrical stimulation of the trigeminofacial nerve complex and the facial skin, and to chemical and tactile stimulation of the facial skin. Recording bimodal responses to chemical and tactile stimulation after sectioning the cranial Vth or VIIth (communis) nerves, and microelectrode recordings of trigeminal and facial (communis) nerve trunks revealed that taste messages are transmitted to the brain by the communis fibers and tactile ones by the trigeminus.Latencies measured in the facial lobe by electrical stimulation of the trigeminofacial nerve complex or the facial skin surface ranged from 6 to 59 msec, most firing between 10 and 29 msec in both cases. The receptive field sizes of the lobe neurons were larger than those of the primary ones.Of 84 neurons recorded from the facial lobe, 96.5% were facilitated by press and gliding movements with a glass rod on the facial skin and 3.5% by changing barbel's position. The glide group was classified into three types which were tonically firing (52.4% of total neurons), adaptive firing (39.3%) and after firing (4.8%) types. Twelve out of 84 tactile neurons responded to chemical solution, as well. The latencies of taste neurons were not centered at a certain range.The facial lobe of the carp is not only a primary gustatory center, but also a tactile one, and might play an important role for the purpose of effecting a correlation of the two diverse modalities.     

Pathways between the nucleus tractus solitarius and neurosecretory neurons of the supraoptic nucleus: Electrophysiological studies

In anesthetized cats recordings were made from hypothalamo-neurohypophysial neurons in a supraoptic nucleus (SON) of the hypothalamus. The region of the nucleus tractus solitarius in the medulla, identified electrophysiologically as the site of termination of the first relay neurons of the sinus and aortic nerves, was stimulated with single or short trains of pulses (2–3 at 200 Hz). Out of 133 SON neurons 67 were affected by such stimuli. In 14 cells (21% of ‘responsive’ neurons) the stimulus produced profound inhibition of SON neuron activity after a latency of 10–30 msec. In another 8 neurons (12%) the inhibitory effect was observed after a longer latency of over 100 msec. An increase in intensity of stimulus merely prolonged or increased the inhibitory effect without changing the response qualitatively. The other 45 (67%) SON neurons were excited by stimulation of the nucleus tractus solitarius. In a small proportion of these neurons (5 cells, 7%) the stimulus evoked discharges, even in spontaneously silent neurosecretory cells, after a latency of 10–20 msec with little fluctuation. In the remaining 40 neurons, i.e. 60% of the ‘responsive’ neurons, the excitatory effect was observed after a latency of 40–120 msec. Again, changes in intensity of stimulation did not alter the nature of this response. The results indicate that both ‘fast’ as well as ‘slow’ pathways between the nucleus tractus solitarius and SON neurons exist and impulses travelling through the latter pathway from the carotid sinus or aortic nerve affect the larger proportion of SON neurons.     

Hunger Modulates the Responses to Gustatory Stimuli of Single Neurons in the Caudolateral Orbitofrontal Cortex of the Macaque Monkey

1. In order to determine whether the responsiveness of neurons in the caudolateral orbitofrontal cortex (a secondary cortical gustatory area) is influenced by hunger, the activity evoked by prototypical taste stimuli (glucose, NaCl, HCl, and quinine hydrochloride) and fruit juice was recorded in single neurons in this cortical area before, while, and after cynomolgous macaque monkeys were fed to satiety with glucose or fruit juice. 2. It was found that the responses of the neurons to the taste of the glucose decreased to zero while the monkey ate it to satiety during the course of which his behaviour turned from avid acceptance to active rejection. 3. This modulation of responsiveness of the gustatory responses of the neurons to satiety was not due to peripheral adaptation in the gustatory system or to altered efficacy of gustatory stimulation after satiety was reached, because modulation of neuronal responsiveness by satiety was not seen at earlier stages of the gustatory system, including the nucleus of the solitary tract, the frontal opercular taste cortex, and the insular taste cortex. 4. The decreases in the responsiveness of the neurons were relatively specific to the food with which the monkey had been fed to satiety. For example, in seven experiments in which the monkey was fed glucose solution, neuronal responsiveness decreased to the taste of the glucose but not to the taste of blackcurrant juice. Conversely, in two experiments in which the monkey was fed to satiety with fruit juice, the responses of the neurons decreased to fruit juice but not to glucose. 5. These and earlier findings lead to a proposed neurophysiological mechanism for sensory-specific satiety in which the information coded by single neurons in the gustatory system becomes more specific through the processing stages consisting of the nucleus of the solitary tract, the taste thalamus, and the frontal opercular and insular taste primary taste cortices, until neuronal responses become relatively specific for the food tasted in the caudolateral orbitofrontal cortex (secondary) taste area. Then sensory-specific satiety occurs because in this caudolateral orbitofrontal cortex taste area (but not earlier in the taste system) it is a property of the synapses that repeated stimulation results in a decreased neuronal response. 6. Evidence was obtained that gustatory processing involved in thirst also becomes interfaced to motivation in the caudolateral orbitofrontal cortex taste projection area, in that neuronal responses here to water were decreased to zero while water was drunk until satiety was produced.     

Electrical stimulation of the medial prefrontal cortex supports both ‘pure reward’ and ‘reward-escape’ behavior in rats

In female Sprague-Dawley rats, 8 of 12 medial prefrontal cortex (MPFC) sites that yielded criterion self-stimulation behavior supported only self-stimulation, i.e. were ‘pure reward’ in type. The remaining 4 sites supported behavior to escape from experimenter-administered stimulation of the same parameter as well, i.e. were ‘reward-escape’ in type. ‘Pure reward’ and ‘reward-escape’ sites in the MPFC were distinguished by both the magnitude and temporal form of the escape response functions generated, and by the prevalence of ‘pounce-back’, a vigorous and repetitive barpressing during the 3-s MPFC stimulation-escape interval produced by an effective barpress. The finding that both ‘pure reward’ and ‘reward-escape’ patterns of behavior can be elicited by stimulation on the MPFC provides a basis for futher assessment of similarities and differences in medial prefrontalcortical and lateral hypothalamic (LH) ‘reward’ systems. It is suggested that ‘reward-escape’ in the MPFC may be mediated by the activity of ‘reward’ neurones which respond to stimulus offset, rather than by a secondary aversive process as is proposed to underlie ‘reward-escape’ in the LH.     

Hypoglossal motor nerve activity elicited by taste and thermal stimuli applied to the tongue in rats

Single unit activity of hypoglossal motor nerve fibers which innervate the tongue muscles was recorded in lightly anesthetized non-decerebrate and acute decerebrate rats. The pattern of responses to taste and thermal stimuli applied to the tongue surface was classified into 4 types. The type 1 response is characterized by short-lasting rhythmic burst discharges, the type 2 consists of both the rhythmic burst and tonic discharges, the type 3 is long-lasting tonic discharges and the type 4 shows short-lasting burst or short-lasting tonic discharges. In non-decerebrate rats, most of the fibers (93%) showed no or a few spontaneous firings. Sucrose and NaCl were the most effective stimulants, and 70–80% of the fibers showed the type 1 response to these stimuli. Calculating the correlations between response patterns of the fiber to a pair of the stimuli, sucrose and NaCl, and HCl and quinine produced a similar response profile, respectively. In decerebrate rats, however, about 21% of fibers showed a highly regular spontaneous firing (about 30 Hz). Rhythmic burst responses (types 1 and 2) were not induced, and thermal (especially cold) stimulation elicited much better responses than the taste stimuli. HCl and quinine, but not sucrose and NaCl, produced a similar response profile. These characteristic properties of the response in acute decerebrate rats may in part be attributed to inactivation of a ‘rhythmic center’ in the brain stem.     

Gustatory afferents to ventral forebrain

The pontine taste area (PTA) receives afferents from the gustatory zone of the nucleus of the solitary tract, and projects bilaterally to the thalamic taste area. Lesions of PTA also result in degenerating axons entering the substantia innominata in the ventral forebrain. The technique of antidromic activation has been used to demonstrate that pontine neurons which respond to gustatory stimuli send collaterals to both the thalamic taste area and substantia innominata. This establishes that, like olfactory input, gustatory information reaches the ventral telencephalon without first synapsing in the diencephalon.     

Antidromic identification of neurons in the ventrolateral part of the medulla oblongata with ascending projections to the preoptic and anterior hypothalamic area (POA/AHA)

Seventy neurons in the ventrolateral medulla oblongata were antidromically activated by electrical stimulation of the preoptic and anterior hypothalamic area (POA/AHA) in female rats under urethane anesthesia. These identified cells were located within and adjacent to the nucleus reticularis lateralis and could be readily distinguished into at least two types of neurons, designated as ‘fast’ and ‘slow’ cells, on the basis of their waveform and conduction velocity.     

Neuronal activity in the monkey dorsolateral prefrontal cortex during a discrimination task with delay

Ninety-nine single neuron activities of the dorsolateral prefrontal cortex of 3 monkeys were recorded during performance of a Konorski task. Green or red lights were presented successively with a separation of fixed delay interval. The monkey responded as soon as the second stimulus was presented. If the two stimuli were color-matched, the ‘YES’ lever press was rewarded; if the two stimuli were not, the ‘NO’ lever press was rewarded. In the second task, after paired color stimuli, a tone pip was presented as the ‘GO’ signal for lever presses. During sample and matching periods 50 neurons increased their discharge rates and 10 decreased. In 86% of increasing type neurons rate increase occurred during both periods. During auditory GO periods, 27 neurons increased their rates and 11 decreased. Discharge peak was before or at the moment of hold key release. In 60% of these neurons were also observed the rate changes to sample and matching stimuli. Differential activations between left and right levers were found in 20%. It was suggested that the prefrontal cortex is related to a sensorial attention mechanism to the visual stimulus which enables correct choice of the behavior to be rewarded.     

Forebrain connections of the gustatory system in ictalurid catfishes

Horseradish peroxidase tracing and extracellular electrophysiological recording techniques were employed to delineate prosencephalic connections of the gustatory system in ictalurid catfishes. The isthmic secondary gustatory nucleus projects rostrally to several areas of the ventral diencephalon including the nucleus lobobulbaris and the nucleus lateralis thalami. Injections of HRP in the vicinity of the nucleus lobobulbaris reveal an ascending projection to the telencephalon terminating in the area dorsalis pars medialis (Dm) and the medial region of area dorsalis pars centralis (Dc). Conversely, injections of HRP into the gustatory region of area dorsalis pars medialis label small neurons in the nucleus lobobulbaris. Gustatory neurons in the telencephalon send descending projections via the medial and lateral forebrain bundles to several nuclei in the anterior and ventroposterior diencephalon. The nucleus lateralis thalami, a diencephalic nucleus, receives ascending gustatory projections from the secondary gustatory nucleus but does not project to the telencephalon. Neurons in both the nucleus lateralis thalami and the telencephalic gustatory target exhibit multiple extraoral and oral receptive fields and complex responses to chemical (taste) and tactile stimulation.     

Role of the central amygdaloid nucleus in shaping the discharge of gustatory neurons in the rat parabrachial nucleus

The central amygdaloid nucleus (CeA) receives projection from the parabrachial nucleus (PBN) gustatory neurons and descendingly projects to the PBN. To assess if the CeA is involved in modulating the activity of gustatory neurons in the PBN, the effects of electrical stimulation and electrolytic lesion of CeA on PBN gustatory neurons were observed. Of 60 neurons observed, 30 were classified as NaCl-best, 18 as HCl-best, 5 as Quinine HCl (QHCl)-best, and 7 as sucrose-best. During CeA stimulation, the responses to at least one effective stimulus were inhibited in most PBN neurons, with the response magnitudes to HCl and QHCl significantly decreased (P<0.01). In contrast, bilateral lesions of CeA facilitated the responses to HCl and QHCl (P<0.01). According to the best-stimulus category, the effects on the responses to HCl and QHCl were similarly subjected to these modulations either during electrical stimulation or after electrolytic lesions of CeA. Analyses of across-unit patterns indicated that the CeA stimulation increased the chemical selection of PBN taste neurons while the CeA lesions depressed the effect on the chemical selection between NaCl and QHCl. These findings suggest that the CeA may be involved in mediating feeding behavior via modulating the activity of gustatory neurons of PBN.     

Properties of velocity-mechanosensitive neurons of the cat ventrobasal thalamic nucleus with special reference to the concept of convergence

Neurons in the ventrobasal (VB) thalamic nucleus of lightly anesthetized cats were studied in order to analyze their discharge properties in response to controlled mechanical stimuli. Properties of the vast majority of the neuronal population largely resemble those of peripheral sensitive mechanoreceptors in their response to the velocity and, to a more limited extent, the amplitude component, of skin and hair displacement within restricted receptive fields. Detailed examination reveals some ‘complex’ characteristics suggestive of central integration in about 11% of VB neurons. Complex properties appear to indicate convergent input reflecting receptive field organization, the variety of velocity-related discharges and patterns of inhibition. The rarity of isolated ‘surround’ inhibition and the definition of what constitutes ‘lemniscal’ properties are discussed in the context of these and other related findings.     

Reflex connections of the facial and vagal gustatory systems in the brainstem of the bullhead catfish, Ictalurus nebulosus

The primary gustatory sensory nuclei in catfish are grossly divisible into a vagal lobe and a facial lobe. In this study, the reflex connections of each gustatory lobe were determined with horseradish peroxidase (HRP) tracing methods. In addition, in order to determine the loci and morphology of the other brainstem cranial nerve nuclei, HRP was applied to the trigeminal, facial, glossopharyngeal, or vagus nerve. The sensory fibers of the facial nerve terminate in the facial lobe. The facial lobe projects bilaterally to the posterior thalamic nucleus, superior secondary gustatory nucleus, and medial reticular formation of the rostral medulla. The facial lobe has reciprocal connections with the n. lobobulbaris, medial reticular formation of the rostral medulla, descending trigeminal nucleus, medial and lateral funicular nuclei, and the vagal lobe, ipsilaterally; and with the facial lobe contralaterally. In addition, the facial lobe receives inputs from the raphe nuclei, from a pretectal nucleus, and from perilemniscal neurons located immediately adjacent to the ascending gustatory lemniscal tract at the level of the trigeminal motor nucleus. The gustatory fibers of the vagus nerve terminate in the vagal lobe, while the general visceral sensory fibers terminate in a distinct general visceral nucleus. The vagal lobe projects ipsilaterally to the superior secondary gustatory nucleus, lateral reticular formation, and n. ambiguus; and bilaterally to the commissural nucleus of Cajal. The vagal lobe has reciprocal connections with the ipsilateral lobobulbar nucleus and facial lobe. In addition, the vagal lobe receives input from neurons of the medullary reticular formation and perilemniscal neurons of the pontine tegmentum. In summary, the facial gustatory system has connections consonant with its role as an exteroceptive system which works in correlation with trigeminal and spinal afferent systems. In contrast, the vagal gustatory system has connections (e.g., with the n. ambiguus) more appropriate to a system involved in control of swallowing. These differences in central connectivity mirror the reports on behavioral dissociation of the facial and vagal gustatory systems.     

电刺激大鼠杏仁中央核对脑桥臂旁核味觉神经元的影响(英文)

利用电生理学方法观察了电刺激杏仁中央核对脑桥臂旁核味觉神经元的影响。结果表明 :电刺激杏仁中央核抑制大部分臂旁核味觉神经元的活动 ,并且提高臂旁核味觉神经元对五种基本味觉刺激反应的特异性。电刺激杏仁中央核对臂旁核的抑制作用以对盐酸和奎宁刺激的反应尤为明显 (P <0 .0 1) ,并且对这两种厌味刺激反应的抑制作用是基本一致的。本研究的结果提示 ,杏仁中央核可能通过抑制脑干味觉神经元对厌味刺激的反应 ,从而参与对摄食行为的调控     

Electrophysiological evidence for the topographical arrangement of taste and tactile neurons in the facial lobe of the channel catfish

Neural responses in the facial lobe of the channel catfish to chemical and mechanical stimulation of the external skin surface were studied electrophysiologically. Taste and tactile neurons in the lobe were organized in a somatotopic manner, which confirms the anatomical reports of the facial lobe in the bullhead catfish, but is markedly different from that of the Cyprinidae. The taste neurons were arranged generally in the more dorsal regions of the tactile sensitive areas and responded with highest frequency to l-alanine or l-arginine HCl among several amino acids tested. The mechanically responsive neurons in the deeper layer of the antero-medial portion of the lobe, possibly corresponding to the intermediate nucleus of the facial lobe, had large receptive fields ranging from 100 mm² to the whole body surface; in addition, some of these neurons showed lateral inhibition. The present study revealed that the facial lobe of the channel catfish is a center not only for gustatory input, but also for tactile information.     

Aversive taste stimuli facilitate extracellular acetylcholine release in the insular gustatory cortex of the rat: a microdialysis study

The release of extracellular acetylcholine (ACh) in the insular gustatory cortex of conscious rats during taste stimulation was measured using the microdialysis technique. The mean basal release of ACh before stimulation was 273 ± 21 fmol/10 μl (mean ± S.E.M., n = 25). Intraorally applied taste stimuli or distilled water significantly increased the release of ACh. Among them, infusion of 0.001 M quinine HCl produced a marked increase in the release of ACh up to 355% of baseline levels. Infusion of 0.01 M saccharin to the subjects that had acquired an aversion to this taste also caused a prominent increase in ACh up to 343% of basal levels. In contrast, saccharin infusion to the naive subjects moderately increased ACh up to 243% of baseline. Water infusion resulted in the smallest increase in ACh up to 175% of baseline. Although intraoral infusions of quinine or distilled water caused a significant increase in ACh in the parietal cortex, the magnitude of increased ACh was smaller than that in the gustatory cortex. These results suggest that ACh release in the insular gustatory cortex is related to behavioral expression to aversive taste stimuli.     

Multimodal responses of taste neurons in the frog nucleus tractus solitarius

The responses of 216 neurons in the nucleus tractus solitarius (NTS) of the American bullfrog were recorded following taste, temperature, and tactile stimulation. Cells were classified on the basis of their responses to 5 taste stimuli: 0.5 M NaCl, 0.0005 M quinine-HCl (QHCl), 0.01 M acetic acid, 0.5 M sucrose, and deionized water (water). Neurons showing excitatory responses to 1, 2, 3, or 4 of the 5 kinds of taste stimuli were named Type I, II, III, or IV, respectively. Cells whose spontaneous rate was inhibited by taste and/or tactile stimulation of the tongue were termed Type V. Type VI neurons were excited by tactile stimulation alone. Of the 216 cells, 115 were excited or inhibited by taste stimuli (Types I-V), with 35 being Type I, 34 Type II, 40 Type III, 2 Type IV and 4 Type V. The remaining 101 cells were responsive only to tactile stimulation (Type VI). Of those 111 cells excited by taste stimulation (Types I-IV), 106 (95%) responded to NaCl, 66 (59%) to acetic acid, 44 (40%) to QHCl, 10 (9%) to water, and 9 (8%) to warming. No cells responded to sucrose. Of the 111 cells of Types I-IV, 76 (68%) were also sensitive to mechanical stimulation of the tongue. There was some differential distribution of these neuron types within the NTS, with more narrowly tuned cells (Type I) being located more dorsally in the nucleus than the more broadly tuned (Type III) neurons. Cells responding exclusively to touch (Type VI) were also more dorsally situated than those responding to two or more taste stimuli (Types II and III).     

Developmental changes in neurophysiological taste response from the medulla in sheep

To determine whether functional characteristics of the taste system change during development, electrophysiological taste responses were recorded from neurons in the solitary complex (nucleus and tractus solitarius) in the medulla of fetal, newborn and adult sheep. Taste stimuli included NH₄Cl, KCl, NaCl, LiCl, citric acid, and HCl, applied to the anterior tongue. Fetal neurons at all ages (84–137 days of gestation) responded to stimulation of the tongue with NH₄Cl and KCl, but responses to NaCl and LiCl were only obtained in older fetuses (after 114 days of gestation), lambs and adults. Responses to citric were obtained at all ages; however, HCl responses were only infrequently obtained in young fetuses. Other developmental changes included a progressive decrease in latency of the responses to NH₄Cl, KCl, citric acid and HCl, and an increase in the duration of the neural response discharge as a function of gestational age. Since taste buds do not acquire the structural characteristics of the adult until the last third of gestation ( 100–147 days), these functional changes in taste response characteristics take place concurrently with structural development. Mammalian fetuses swallow amniotic fluid in utero, and therefore, the fetal taste system is stimulated during structural and functional development. Thus, there is an opportunity for fetal gustatory experience to influence the developing taste system.     

Identification of prepositus neurons projecting to the oculomotor nucleus in the alert cat

A population of prepositus hypoglossi nucleus neurons with discharges correlated to gaze parameters and antidromically activated by stimulation of the ipsilateral oculomotor nucleus has been recorded in the alert cat. The latency for antidromic invasion was of 0.6–0.8 msec. Neuronal firing rate encoded eye position and eye velocity in the horizontal plane, showing in all cases ipsilateral ‘on’ direction.