Satiety does not affect gustatory activity in the nucleus of the solitary tract of the alert monkey

Feeding to satiety decreases the acceptability of the taste of food. In order to determine whether the responsiveness of gustatory neurons in the nucleus tractus solitarius (NTS) is influenced by hunger, neural activity in the NTS was analyzed while monkeys were fed to satiety. Gustatory neural activity to glucose, fruit juice, NaCl, HCl and quinine HCl was measured before, while and after the monkey was fed to satiety with glucose, fruit juice or sucrose. While behavior turned from avid acceptance to active rejection upon repletion, the responsiveness of NTS neurons to the stimulus array, including the satiating solution, was unmodified. It is concluded that at the first central synapse of the taste system of the primate, neural responsiveness is not influenced by the normal transition from hunger to satiety. This is in contrast to the responses of a population of neurons recorded in the hypothalamus, which only occur to the taste of food when the monkey is hungry. Thus, NTS gustatory activity appears to occur independently of normal hunger and satiety, whereas hypothalamic neuronal activity is more closely related to the influence of motivational state on behavioral responsiveness to gustatory stimuli.     

Sensory-specific satiety: Food-specific reduction in responsiveness of ventral forebrain neurons after feeding in the monkey

It has been shown previously that some neurons in the lateral hypothalamus and substantia innominata respond to the sight of food, others to the taste of food, and others to the sight or taste of food, in the hungry monkey. It is shown here that feeding to satiety decreases the responses of hypothalamic neurons to the sight and/or taste of a food on which the monkey has been satiated, but leaves the responses of the same neurons to other foods on which the monkey has not been satiated relatively unchanged. This suggests that the responses of these neurons in the ventral forebrain are related to sensory-specific satiety, an important phenomenon which regulates food intake. In sensory-specific satiety, the pleasantness of the sight or taste of a food becomes less after it is eaten to satiety, whereas the pleasantness of the sight or taste of other foods which have not been eaten is much less changed; correspondingly, food intake is greater if foods which have not already been eaten to satiety are offered.     

Neuronal activity in the medial orbitofrontal cortex of the behaving monkey: Modulation by glucose and satiety

To investigate neuronal responses to interoceptive information, single neuron activity of the orbitofrontal cortex (OBF) of the behaving monkey was recorded during glucose injection, natural feeding and an operant bar press feeding task. Intravenous glucose injection had almost no effect on rates of spontaneous firing, but tended to attenuate neuronal responses during the bar press and reward periods. In about half of the neurons tested, the spontaneous firing rate changed for a relatively long period after the animal ate to satiety. The results suggest that blood glucose concentration is a modulatory factor in neuronal processing for feeding, but other interoceptive information generated by satiety strongly affects the activity of OBF neurons.     

The effect of satiety on responses of gustatory neurons in the amygdala of alert cynomolgus macaques

An alert cynomolgus macaque was fed a sweet solution to satiety as the activity of a gustatory neuron in the amygdala was recorded to that solution and to four other taste stimuli. This experiment was conducted a total of 14 times in two monkeys. The responses of individual neurons to the satiety stimuli were suppressed by as little as 1%, and as much as 100% by the induction of satiety (mean suppression = 58%). Nine of the 14 cells responded to the satiety solution with excitation, and their responses were suppressed by a mean of 62% by satiety. Five neurons responded with inhibition, and their responses were suppressed by a mean of 50%. Responses to other taste stimuli, not associated with satiety, were affected to a lesser extent. The amygdala is a taste relay between the primary gustatory cortex, where satiety has no influence on responses to taste stimuli, and the lateral hypothalamic area where the effect of satiety is total. The data presented here indicate that the amygdala is a functional as well as anatomical intermediary between these two areas, and serves as a stage in the process through which sensory stimuli are imbued with motivational significance.     

Effects of hunger on the responses of neurons in the lateral hypothalamus to the sight and taste of food

Recordings were made from single neurons in the monkey lateral hypothalamus and substantia innominata which had previously been shown to respond with an increase or decrease of their firing rates when the hungry monkey tasted food, and/or when he looked at food. It was found that the responsiveness of these neurons to food decreased over the course of a meal of glucose as satiety increased. When satiety, measured by whether the monkey rejected the glucose, was complete, there was no response of the neurons to the taste and/or to the sight of glucose. The spontaneous firing rates of these cells were not affected by the transitions from hunger to satiety. This modulation of responsiveness to food of hypothalamic cells was specific to them in that it was not seen in cells in the globus pallidus which responded in relation to swallowing and mouth movements, or in cells in the visual inferotemporal cortex which responded when the monkey looked at the glucose-containing syringe. On the basis of this and other evidence it is suggested that the hypothalamic cells described here could be involved in the autonomic, the endocrine, and/or the feeding responses which occur when an animal sees or tastes food.     

Human cortical gustatory areas: a review of functional neuroimaging data

In an effort to define human cortical gustatory areas we reviewed functional neuroimaging data for which coordinates standardized in Talairach proportional space were available. We observed a wide distribution of peaks within the insula and parietal and frontal opercula, suggesting multiple gustatory regions within this cortical area. Multiple peaks also emerged in the orbitofrontal cortex. However, only two peaks, both in the right hemisphere, were observed in the caudolateral orbitofrontal cortex, the region likely homologous to the secondary taste area described in monkeys. Overall significantly more peaks originated from the right hemisphere suggesting asymmetrical cortical representation of taste favoring the right hemisphere.     

Administration of satiety factors and gustatory responsiveness in the nucleus tractus solitarius of the rat.

The administration of certain factors associated with postprandial satiety decreases gustatory responsiveness. We compared the effects of intravenous injections of glucose, insulin, pancreatic glucagon (PG), and cholecystokinin (CCK) on multiunit activity evoked from taste responsive neurons in the nucleus tractus solitarius of rats. Glucose, insulin, and PG reliably suppressed evoked responses to lingual application of 1.0M glucose, whereas responses that followed CCK remained unchanged. A common physiological consequence of glucose, insulin, and glucagon is increased glucose availability which may impact directly on gustatory neurons or indirectly through modifications in ventral forebrain or vagal afferent activity.     

An electrophysiological and behavioural study of self-stimulation in the orbitofrontal cortex of the rhesus monkey

It was found that neurons in the posterior orbitofrontal cortex, area 13, of the rhesus monkey were activated from self-stimulation electrodes (in 142 of 168 possible instances), and that neurons in the anterior orbitofrontal areas were much less likely to be activated from the self-stimulation electrodes (in only 28 of 177 possible instances). This activation of neurons in the posterior orbitofrontal cortex was found mainly from self-stimulation sites in the nucleus accumbens septi, lateral hypothalamus, and the orbitofrontal cortex itself. In a second investigation the orbitofrontal cortex was mapped for self-stimulation, and it was found that self-stimulation occurred in the posterior orbitofrontal area. These results implicate the posterior or caudal orbitofrontal cortex, mainly area 13, but not the more anterior orbitofrontal areas, in self-stimulation.     

Projections of thalamic gustatory and lingual areas in the monkey, Macaca fascicularis

The efferent projections of the parvicellular division of the ventroposteromedial nucleus of the thalamus (VMPpc; thalamic taste area) were traced to cortex in Macaca fascicularis by using tritiated amino acid autoradiography. Labeled fascicles could be traced from VPMpc to two discrete regions of cortex. The primary efferent projection was located on ipsilateral insular-opercular cortex adjacent to the superior limiting sulcus and extended as far rostrally as the posterior lateral orbitofrontal cortex. An additional projection was located within primary somatosensory (SI) cortex subjacent to the anterior subcentral sulcus. Following autoradiographic injections in VPM, the trigeminal somatosensory relay, a dense terminal plexus was labeled on SI cortex of both pre- and postcentral gyri, but not within insular-opercular cortex. The autoradiographic data were verified by injecting each cortical projection area with horseradish peroxidase (HRP) and observing the pattern of retrogradely labeled somata within the thalamus. Injections in the precentral gyrus near the anterior subcentral sulcus retrogradely labeled neurons within VPMpc, whereas injections further caudally near the floor of the central sulcus labeled neurons within VPM. Injections of HRP within opercular, insular, or posterior lateral orbitofrontal cortex retrogradely labeled neurons within VPMpc.     

Neurophysiological analysis of brain-stimulation reward in the monkey

Neuronal activity related to brain-stimulation reward and to feeding was analyzed in rhesus monkeys and squirrel monkeys as follows. First, self-stimulation of the lateral hypothalamus, orbitofrontal cortex, amygdala and nucleus accumbens was found. Second, a population of single neurones in the lateral hypothalamus was found to be trans-synaptically activated from one or several self-stimulation sites. It was also found that populations of neurones in the orbitofrontal cortex and amygdala were activated from at least some of the self-stimulation sites. Thus, in the monkey, there is evidence for an interconnected set of self-stimulation sites, stimulation in any one of which may activate neurones in the other regions. These sites include the lateral hypothalamus, amygdala, and orbitofrontal cortex. Third, in one sample of 764 neurones in the lateral hypothalamis and substantia innominata which were activated from brain-stimulation reward sites, 13.6% were also activated during feeding, by the sight and/or taste of food. The responses of the neurones with activity associated with taste occurred only while some substances (e.g. sweet substances such as glucose) were in the mouth, depended on the concentration of the substances being tasted, and were independent of mouth movements made by the monkeys. Fourth, the responses of these neutrones occurre to food when the monkeys were hungry, but not when they were satiated. Fifth, self-stimulation occurred in the region of these neurones in the lateral hypothalamus and substantia innominata, and was attenuated by satiety. These results suggest that self-stimulation of some brain sites occurs because of activation of neurones in the lateral hypothalamus and substantia innominata activated by the sight and/or taste of food in the hungry animal, and that these neurones are involved in responses to food reward.     

Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex

When a food is eaten to satiety, its reward value decreases. This decrease is usually greater for the food eaten to satiety than for other foods, an effect termed sensory-specific satiety. In an fMRI investigation it was shown that for a region of the orbitofrontal cortex the activation produced by the odour of the food eaten to satiety decreased, whereas there was no similar decrease for the odour of a food not eaten in the meal. This effect was shown both by a voxel-wise SPM contrast (p<0.05 corrected) and an ANOVA performed on the mean percentage change in BOLD signal in the identified clusters of voxels (p<0.006). These results show that activation of a region of the human orbitofrontal cortex is related to olfactory sensory-specific satiety.     

Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex

When a food is eaten to satiety, its reward value decreases. This decrease is usually greater for the food eaten to satiety than for other foods, an effect termed sensory-specific satiety. In an fMRI investigation it was shown that for a region of the orbitofrontal cortex the activation produced by the odour of the food eaten to satiety decreased, whereas there was no similar decrease for the odour of a food not eaten in the meal. This effect was shown both by a voxel-wise SPM contrast (p <0.05 corrected) and an ANOVA performed on the mean percentage change in BOLD signal in the identified clusters of voxels (p <0.006). These results show that activation of a region of the human orbitofrontal cortex is related to olfactory sensory-specific satiety.     

Neurons in the posterior insular cortex are responsive to gustatory stimulation of the pharyngolarynx, baroreceptor and chemoreceptor stimulation, and tail pinch in rats

Extracellular unit responses to gustatory stimulation of the pharyngolaryngeal region, baroreceptor and chemoreceptor stimulation, and tail pinch were recorded from the insular cortex of anesthetized and paralyzed rats. Of the 32 neurons identified, 28 responded to at least one of the nine stimuli used in the present study. Of the 32 neurons, 11 showed an excitatory response to tail pinch, 13 showed an inhibitory response, and the remaining eight had no response. Of the 32 neurons, eight responded to baroreceptor stimulation by an intravenous (i.v.) injection of methoxamine hydrochloride (Mex), four were excitatory and four were inhibitory. Thirteen neurons were excited and six neurons were inhibited by an arterial chemoreceptor stimulation by an i.v. injection of sodium cyanide (NaCN). Twenty-two neurons were responsive to at least one of the gustatory stimuli (deionized water, 1.0 M NaCl, 30 mM HCl, 30 mM quinine HCl, and 1.0 M sucrose); five to 11 excitatory neurons and three to seven inhibitory neurons for each stimulus. A large number of the neurons (25/32) received converging inputs from more than one stimulus among the nine stimuli used in the present study. Most neurons (23/32) received converging inputs from different modalities (gustatory, visceral, and tail pinch). The neurons responded were located in the insular cortex between 2.0 mm anterior and 0.2 mm posterior to the anterior edge of the joining of the anterior commissure (AC); the mean location was 1.2 mm (n=28) anterior to the AC. This indicates that most of the neurons identified in the present study seem to be located in the region posterior to the taste area and anterior to the visceral area in the insular cortex. These results indicate that the insular cortex neurons distributing between the taste area and the visceral area receive convergent inputs from gustatory, baroreceptor, chemoreceptor, and nociceptive organs.     

The Representation of Information About Taste and Odor in the Orbitofrontal Cortex

Complementary neurophysiological recordings in macaques and functional neuroimaging in humans show that the primary taste cortex in the rostral insula and adjoining frontal operculum provides separate and combined representations of the taste, temperature, and texture (including viscosity and fat texture) of food in the mouth independently of hunger and thus of reward value and pleasantness. One synapse on, in the orbitofrontal cortex, these sensory inputs are for some neurons combined by learning with olfactory and visual inputs, and these neurons encode food reward in that they only respond to food when hungry and in that activations here correlate with subjective pleasantness and with individual differences in and cognitive modulation of the hedonic value of food. Information theory analysis shows a robust representation of taste in the orbitofrontal cortex, with an average mutual information of 0.45 bits for each neuron about which of six tastants (glucose, NaCl, HCl, quinine-HCl, monosodium glutamate, and water) was present, averaged across 135 gustatory neurons. The information increased with the number of neurons in the ensemble, but less than linearly, reflecting some redundancy. There was less information per neuron about which of six odors was present from orbitofrontal olfactory neurons, but the code was robust in that the information increased linearly with the number of neurons, reflecting independent information encoded by different neurons. Although some neurons were sharply tuned to individual tastants, the average encoding was quite distributed.     

Complex attributes of lateral hypothalamic neurons in the regulation of feeding of alert rhesus monkeys

To elucidate the roles of glucose-sensitive (GS) and glucose-insensitive (GIS) cells of the lateral hypothalamic area (LHA), single neuron activity was recorded during 1) microelectrophoretic administration of chemicals, 2) a conditioned bar press feeding task, 3) gustatory, 4) olfactory, and 5) electrical brain stimulation. GS and GIS neurons showed different firing rate changes during phases of the task, and the responses were highly influenced by the palatability of the food and the motivational (hunger or satiety) state of the animal. The two groups of cells also differed in their responsiveness to gustatory and olfactory stimuli: GS neurons were more likely to respond to tastes and odors than GIS cells. Taste- and odor-responsive GS neurons were primarily suppressed by electrophoretically applied noradrenaline and were localized ventromedially within the LHA. The chemosensitive GIS cells, being organized along a dorsolateral axis, were especially excited by dopamine. The two sets of neurons had distinct connections with associative (orbitofrontal, prefrontal) cortical areas. GS and GIS cells, thus, appear to have differential and complex attributes in the control of feeding.     

Cortical connections of the frontoparietal opercular areas in the Rhesus monkey

The connections of the frontoparietal opercular areas were studied in rhesus monkeys by using antero- and retrograde tracer techniques. The rostral opercular cortex including the gustatory and proisocortical motor (ProM) areas is connected with precentral areas 3, 1, and 2 as well as with the rostral portion of the opercular area which resembles the second somatosensory type of cortex (area SII) and the ventral portion of area 6. Its distant connections are with the ventral portion of prefrontal areas 46, 11, 12, and 13 as well as with the rostral insula and cingulate motor area (CMAr). The mid opercular region (areas 1 and 2) is connected with pre- and postcentral areas 3, 1, and 2 as well as SII. Additionally, it is connected with the ventral portion of area 6, area 44, area ProM, the gustatory area, and the rostral insula. Its distant connections are with area 4, the ventral portion of area 46, area 7b, and area POa in the intraparietal sulcus (IPS). The rostral parietal opercular region is connected with the postcentral portions of areas 3, 1, and 2; areas 5, 7, and SII; the gustatory area; and the vestibular area. Its other connections are with area 4, area 44, the ventral portion of area 46, area ProM, CMAr, and the supplementary motor area (SMA). The caudal opercular region is connected with the dorsal portion of area 3; areas 2, 5, and 7a; and areas PEa as well as IPd of IPS. It is also connected with area SII, insula, and the superior temporal sulcus. Its distant connections are with area 44; the dorsal portion of area 8 and the ventral portion of area 46; as well as CMAr, SMA, and the supplementary sensory area. This connectivity suggests that the ventral somatosensory areas are involved in sensorimotor activities mainly related to head, neck, and face structures as well as to taste. Additionally, these areas may have a role in frontal (working) and temporal (tactile) memory systems. J. Comp. Neurol. 403:431–458, 1999. © 1999 Wiley-Liss, Inc.     

Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey.

The orbitofrontal cortex of the monkey can be subdivided into a caudal agranular sector, a transitional dysgranular sector, and an anterior granular sector. The neural input into these sectors was investigated with the help of large horseradish peroxidase injections that covered the different sectors of orbitofrontal cortex. The distribution of retrograde labeling showed that the majority of the cortical projections to orbitofrontal cortex arises from a restricted set of telencephalic sources, which include prefrontal cortex, lateral, and inferomedial temporal cortex, the temporal pole, cingulate gyrus, insula, entorhinal cortex, hippocampus, amygdala, and claustrum. The posterior portion of the orbitofrontal cortex receives additional input from the piriform cortex and the anterolateral portion from gustatory, somatosensory, and premotor areas. Thalamic projections to the orbitofrontal cortex arise from midline and intralaminar nuclei, from the anteromedial nucleus, the medial dorsal nucleus, and the pulvinar nucleus. Orbitofrontal cortex also receives projections from the hypothalamus, nucleus basalis, ventral tegmental area, the raphe nuclei, the nucleus locus coeruleus, and scattered neurons of the pontomesencephalic tegmentum. The non-isocortical (agranular-dysgranular) sectors of orbitofrontal cortex receive more intense projections from the non-isocortical sectors of paralimbic areas, the hippocampus, amygdala, and midline thalamic nuclei, whereas the isocortical (granular) sector receives more intense projections from the dorsolateral prefrontal area, the granular insula, granular temporopolar cortex, posterolateral temporal cortex, and from the medial dorsal and pulvinar thalamic nuclei. Retrograde labeling within cingulate, entorhinal, and hippocampal cortices was most pronounced when the injection site extended medially into the dysgranular paraolfactory cortex of the gyrus rectus, an area that can be conceptualized as an orbitofrontal extension of the cingulate complex. These observations demonstrate that the orbitofrontal cortex has cytoarchitectonically organized projections and that it provides a convergence zone for afferents from heteromodal association and limbic areas. The diverse connections of orbitofrontal cortex are in keeping with the participation of this region in visceral, gustatory, and olfactory functions and with its importance in memory, motivation, and epileptogenesis.     

Neuronal Sianallina of Information Imoortant to Visual Recognition-Memory in Rat Rhinal aid Neighbouring Cortices

This study was conducted to discover whether the rat cortex contains neurons that signal information concerning the previous occurrence of stimuli, as has been found in the primate. Recordings of the activity of 396 single neurons were made while unanaesthetized rats were shown objects. The effects on neuronal responsiveness of stimulus repetition and of the relative familiarity of the stimuli were sought. The areas sampled were the rhinal (entorhinal and perirhinal) cortex, area TE of the temporal cortex, the lateral occipital cortex and the hippocampal formation. The response to the first presentations of objects was significantly different from that to their second presentations for 63 (34%) of the 185 responsive neurons; for 39 of the neurons the response was smaller when the stimulus was repeated, whereas for 24 it was larger. The incidence of decremental responses was higher in the non-hippocampal cortex than in the hippocampal formation, while the incidence of incremental responses was higher in the hippocampal formation than other cortical areas. The response to unfamiliar objects was significantly different from that to highly familiar objects for 15 (22%) of 67 responsive neurons so tested; for 12 of the neurons the response was smaller when the stimulus was repeated, and for three it was larger; most of these neurons were found in area TE. The responses of ten familiarity neurons varied significantly with the relative familiarity of the stimuli but not with stimulus repetition; the responses of seven recency neurons varied significantly upon stimulus repetition but not with the relative familiarity of the stimuli. Thus information concerning stimulus repetition and familiarity is separably encoded at the single neuron level in the rat cortex. The results demonstrate that in the rat cortex as in the monkey cortex there are neurons that signal information concerning the prior occurrence of stimuli; such information is of importance to recognition memory, working memory and priming memory.     

It’s in the eye of the beholder: selective attention to drink properties during tasting influences brain activation in gustatory and reward regions

Statements regarding pleasantness, taste intensity or caloric content on a food label may influence the attention consumers pay to such characteristics during consumption. There is little research on the effects of selective attention on taste perception and associated brain activation in regular drinks. The aim of this study was to investigate the effect of selective attention on hedonics, intensity and caloric content on brain responses during tasting drinks. Using functional MRI brain responses of 27 women were measured while they paid attention to the intensity, pleasantness or caloric content of fruit juice, tomato juice and water. Brain activation during tasting largely overlapped between the three selective attention conditions and was found in the rolandic operculum, insula and overlying frontal operculum, striatum, amygdala, thalamus, anterior cingulate cortex and middle orbitofrontal cortex (OFC). Brain activation was higher during selective attention to taste intensity compared to calories in the right middle OFC and during selective attention to pleasantness compared to intensity in the right putamen, right ACC and bilateral middle insula. Intensity ratings correlated with brain activation during selective attention to taste intensity in the anterior insula and lateral OFC. Our data suggest that not only the anterior insula but also the middle and lateral OFC are involved in evaluating taste intensity. Furthermore, selective attention to pleasantness engaged regions associated with food reward. Overall, our results indicate that selective attention to food properties can alter the activation of gustatory and reward regions. This may underlie effects of food labels on the consumption experience of consumers.     

Relations between the spontaneous firing rate and taste responsiveness of the dog cortical neurons

The breadth of responsiveness and the spontaneous discharge rates of dog cortical neurons to 4 taste stimuli (NaCl, tartaric acid, sucrose and quinine-HCl) were examined and compared to thalamic neurons.Spontaneous rates were higher in the cortex, and there was a smaller breadth of responsiveness. There were common tendencies observed in both thalamus and cortex; more narrowly tuned taste neurons and neurons having inhibitory responses had higher spontaneous rates. However, as shown by across-neuron correlations, the ability of cortical neurons to discriminate among the 4 tastes was less influenced by the level of spontaneous activity than thalamic neurons.