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PubMed2004

Functional imaging of gustatory perception and imagery: "top-down" processing of gustatory signals.

By recalling gustatory memories, it is possible to generate vivid gustatory perceptions in the absence of gustatory inputs. This gustatory image influences our gustatory processing. However, the mechanism of the "top-down" modulation of gustatory perception in the human is still unclear. Our findings propose a new perspective on the neural basis of gustatory processing. Although gustatory imagery and gustatory perception shared common parts of neural substrates, there was an asymmetrical topography of activation in the insula: the left insula was predominantly activated by gustatory imagery tasks. In addition, the middle and superior frontal gyri were not activated by gustatory perception but they participated in the generation of gustatory hallucinations. These regions in the frontal cortex may mediate the "top-down" control of retrieving gustatory information from the storage of long-term memories.

Adult↗
PubMed1998

Temporal process from receptors to higher brain in taste detection studied by gustatory-evoked magnetic fields and reaction times.

Using magnetoencephalography (MEG) and a taste stimulator with rapid-rise time, we previously located the primary gustatory area in the human cerebral cortex and also investigated the relation between the onset latency of the gustatory-evoked magnetic fields (GEM) and reaction times (RT) in different taste qualities. In the present study, we investigated the temporal process from receptors to the higher brain in taste detection based on the results of the GEM and RT of different tastes. We used 100 mM, 300 mM and 1 M NaCl and 3 mM saccharine. The duration of each stimulus was 400 ms. The interstimulus interval was approximately 30 s. The temperature of both taste solution and deionized water was maintained the same as that of the tongue. Four subjects participated in this experiment. The 64-channel whole-head SQUID system (CTF Systems Inc., Canada) was used to measure GEM. The sampling rate was 250 Hz, and the low-pass filter was 40 Hz. In each subject, GEM and RT to a given taste were measured separately by applying 40 trials of stimulation. After each trial of both measurements, subjects showed a perceived intensity by using their fingers. In the GEM study, the trials contaminated with eye movements were rejected and the remaining trials were averaged. Averaged GEM were super-imposed on the same sheet with all 64 channels to measure the onset latency of GEM from the stimulus onset. RT and onset latencies of GEM were longer for saccharine than NaCl, and the value of RT minus the onset latency of GEM from RT, presumably indicating the time for higher brain process plus motor process, did not differ between 3 mM saccharine and 1 M NaCl. With increased concentrations of NaCl, RT became shorter, but onset latencies of GEM remained constant. Sweet taste took a longer time than salty taste at receptor process including the time for diffusion to receptors.

Cerebral Cortex↗
PubMed2000

GABA-mediated corticofugal inhibition of taste-responsive neurons in the nucleus of the solitary tract.

The nucleus of the solitary tract (NST) receives descending connections from several forebrain targets of the gustatory system, including the insular cortex. Many taste-responsive cells in the NST are inhibited by gamma-aminobutyric acid (GABA). In the present study, we investigated the effects of cortical stimulation on the activity of gustatory neurons in the NST. Multibarrel glass micropipettes were used to record the activity of NST neurons extracellularly and to apply the GABA(A) antagonist bicuculline methiodide (BICM) into the vicinity of the cell. Taste stimuli were 0.032 M sucrose (S), 0.032 M NaCl (N), 0.00032 M citric acid (H), and 0.032 M quinine hydrochloride (Q), presented to the anterior tongue. Each of 50 NST cells was classified as S-, N-, H-, or Q-best on the basis of its response to chemical stimulation of the tongue. The ipsilateral insular cortex was stimulated both electrically (0.5 mA, 100 Hz, 0.2 ms) and chemically (10 mM DL-homocysteic acid, DLH), while the spontaneous activity of each NST cell was recorded. The baseline activity of 34% of the cells (n=17) was modulated by cortical stimulation: eight cells were inhibited and nine were excited. BICM microinjected into the NST blocked the cortical-induced inhibition but had no effect on the excitatory response. Although the excitatory effects were distributed across S-, N-, and H-best neurons, the inhibitory effects of cortical stimulation were significantly more common in N-best cells. These data suggest that corticofugal input to the NST may differentially inhibit gustatory afferent activity through GABAergic mechanisms.

Animals↗
PubMed2006

[Bilateral gustatory disturbance associated with left putaminal hemorrhage].

We reported a 39-year-old, left-handed man with sudden onset hypogeusia. Taste threshold examined by a filter-paper disc method was elevated remarkably on both sides of the tongue. Additionally, the patient showed mild right central facial nerve palsy and mild weakness in the right upper limb. Brain CT showed left putaminal hemorrhage. Brain MRI demonstrated a hemorrhage in the left putamen and edema affecting the insular cortex. In this case, the gustatory information from both sides of the tongue, regardless of whether the nerves cross in a brainstem, is suggested to project to the left insular cortex before ascending to the higher order taste and language areas.

Adult↗
PubMed2004

Biochemical modulation of NMDA receptors: role in conditioned taste aversion.

Glutamate neurotransmission plays a crucial role in a variety of functions in the central nervous system, including learning and memory. However, little is known about the mechanisms underlying this process in mammals because of the scarceness of experimental models that permit correlation of behavioral and biochemical changes occurring during the different stages of learning and the retrieval of the acquired information. One model that has been useful to study these mechanisms is conditioned taste aversion (CTA), a paradigm in which animals learn to avoid new tastes when they are associated with gastrointestinal malaise. Glutamate receptors of the N-methyl-D-aspartate (NMDA) type appear to be necessary in this process, because blockade of this receptor prevents CTA. Phosphorylation of the main subunits of the NMDA receptor is a well-established biochemical mechanism for the modulation of the receptor response. Such modulation seems to be involved in CTA, because inhibitors of protein kinase C (PKC) block CTA acquisition and because the exposure to an unfamiliar taste results in an increased phosphorylation of tyrosine and serine residues of the NR2B subunit of the receptor in the insular cortex, the cerebral region where gustatory and visceral information converge. In this work we review these mechanisms of NMDA receptor modulation in CTA.

Animals↗
PubMed2001

Taste laterality in the split brain.

Two patients with corpus callosum resection, one complete and the other sparing the genu and the rostrum, were tested for discrimination of three basic taste stimuli (sour, bitter, salty) applied to the right or left sides of the tongue. Responses were made by pointing with either hand to written words or images of visual objects corresponding to the stimuli, a language-based discrimination. In both patients, response accuracy was significantly above chance for both hemitongues but there was a significant advantage for the left side. Reaction time was shorter for left stimuli than for right stimuli but the difference was not significant. Eight normal controls matched for age with the patients performed equally well with right and left hemitongue stimuli and so did a third callosotomy patient with sparing of the posterior callosum, including the splenium. Tactile and visual tests showed that the left hemisphere was responsible for language-based responses in the first two patients. The results confirm and extend previous findings in another callosotomy patient, indicating that: (i) taste information from either side of the tongue can reach the left hemisphere in the absence of the corpus callosum; (ii) the ipsilateral input from the tongue to the left hemisphere is more potent functionally than the contralateral input and (iii) in the normal brain, the corpus callosum, specifically its posterior part including the splenium, appears to equalize the effects of the ipsilateral and contralateral gustatory inputs on the left hemisphere. Taken together with evidence about lateralized taste deficits following unilateral cortical lesions, the results also suggest that the gustatory pathways from tongue to cortex are bilaterally-distributed with an ipsilateral predominance that may be subject to individual variations.

Adult↗
PubMed1999

Spatio-temporal analysis of cortical activity evoked by gustatory stimulation in humans.

Gustatory activated regions in the cerebral cortex have not been identified precisely in humans. In this study we recorded the magnetic fields from the brain in response to two tastants, 1 M NaCl and 3 mM saccharin. We estimated the location of areas activated sequentially after the onset of stimulation with magnetic source imaging. We investigated the primary gustatory area (area G) precisely, and found it at the transition between the parietal operculum and the insular cortex. The central sulcus was activated less frequently than area G but with almost the same latency in cases of NaCl stimulation. Following area G, we found activation in several cortical regions, e.g. both the frontal operculum and the anterior part of the insula, the hippocampus, the parahippocampal gyrus and the superior temporal sulcus.

Adult↗
PubMed1993

Effects of catecholaminergic depletion of the amygdala and insular cortex on the potentiation of odor by taste aversions.

This experiment examined the effects of catecholamine depletion of the amygdala or insular cortex on the acquisition of olfactory and gustatory learning tasks. Bilateral lesions with 6-hydroxydopamine (4 micrograms/0.5 microliters) were done in either amygdala or insular cortex of Wistar male rats, with two groups receiving sham lesions. All four groups of animals were trained and tested in the potentiation of odor by taste aversion paradigm. The results showed that the amygdala-lesioned group acquired the taste, but not hte odor aversion, while the insular cortex-lesioned group acquired odor, but not taste aversion. Both sham groups showed strong taste and odor aversions. Catecholamine levels in both lesioned groups were significantly lower than those in the sham groups. These results suggest that catecholamines are necessary in the insular cortex for the acquisition of taste and in the amygdala for the acquisition of odor aversion in the potentiation of odor by taste aversion paradigm.

Amygdala↗
PubMed2000

Taste as a factor in the management of nutrition.

The sense of taste lies at the interface between the external and internal milieux, at the point at which the animal must decide which chemicals from the environment to incorporate into itself. Accordingly, taste is organized along a neural dimension of nutrients versus toxins, which corresponds to a behavioral dimension of acceptance versus rejection, and to a hedonic dimension of appetitive versus aversive qualities. Reflexive responses, cognitive analyses, and hedonic reactions appear to be managed at different levels of the nervous system. At the first central relay, the nucleus of the solitary tract, somatic reflexes for acceptance or rejection, and autonomic reflexes anticipating digestion are orchestrated. At the second, the parabrachial nucleus of the rodent, associative mechanisms important to the development of conditioned aversions and sodium appetite are manifested. In the thalamic taste relay, gustatory memories associated with non-visceral events may be formed. Primary taste cortex appears to be the site for a cognitive evaluation of gustatory quality and intensity. Finally, a hedonic assessment of the chemical may be made in secondary taste cortex and in the ventral forebrain sites to which it projects. With this assessment comes integration of the gustatory signal with those from other senses, perhaps to create a perception of flavor. Therefore, a sequence that begins with an analysis of the molecular structure of a chemical in the mouth serves to incorporate that gustatory component into an appreciation of flavor, and to participate in the control of motivational processes that guide dietary selection.

Animals↗
PubMed2006

Cortical network for representing the teeth and tongue in primates.

Sensory information from the tongue and teeth is used to evaluate and distinguish food and nonfood items in the mouth, reject some and masticate and swallow others. While it is known that primates have a complex array of 10 or more somatosensory areas that contribute to the analysis of sensory information from the hand, less is known about what cortical areas are involved in processing information from receptors of the tongue and teeth. The tongue contains taste receptors, as well as mechanoreceptors. Afferents from taste receptors and mechanoreceptors of the tongue access different ascending systems in the brainstem. However, it is uncertain how these two sources of information are processed in cortex. Here the parts of somatosensory areas 3b, 3a, and presumptive 1 that represent the mechanoreceptors of the teeth and tongue are identified, and evidence is presented that the representations of the tongue also get information from the taste nucleus of the thalamus, VPMpc. As areas 3b, 3a, and 1 project to other areas of somatosensory cortex, and those areas to additional areas, some or all of the currently defined somatosensory areas of cortex may be involved in processing gustatory, as well as tactile, information from the tongue and thus have a role in the biologically important function of evaluating food in the mouth.

Animals↗
PubMed1993

Fine structure of calcitonin gene-related peptide immunoreactive synaptic contacts in the thalamus of the rat.

Recent studies have shown a prominent calcitonin gene-related peptide immunoreactive (CGRP-ir) pathway extending from the external medial and external lateral para-brachial nuclei to the area surrounding and including the gustatory nuclei in the thalamus, and the cortex and amygdala. The function of the CGRP-ir pathway is not completely understood, but may be involved with the processing of both nociceptive and gustatory information in the thalamus. The purpose of this study was to characterize the nature of the CGRP-ir synaptic contacts in the gustatory nucleus. Electron microscopic examination of CGRP-ir synaptic contacts revealed two classes of CGRP-ir terminals. One class, which was large, formed asymmetric synaptic contacts on dendritic appendages, had many small, round synaptic vesicles, and heavy patches of reaction product which obscured any underlying organelles. Since similar terminals in unstained tissue contained large numbers of dense-cored vesicles, it was concluded that CGRP-ir was contained predominantly in dense-cored vesicles. A second class of CGRP-ir terminals was smaller and made either asymmetric or symmetric synaptic contacts. Both symmetric and asymmetric small terminals contained small, round synaptic vesicles and fewer patches of dense reaction product. Several of the CGRP-ir terminals making symmetric contacts also contained pleomorphic vesicles. There were very few contacts on cell bodies. There were no contacts on other CGRP-ir elements, somal or dendritic, or on axon terminals. None of the CGRP-ir terminal elements were postsynaptic to unlabeled terminals. Axons containing CGRP-ir were primarily unmyelinated, but a few myelinated axons were also seen.

Animals↗
PubMed1999

Prefrontal cortical networks related to visceral function and mood.

At least twenty-two architectonic areas can be distinguished within the orbital and medial prefrontal cortex (OMPFC). Although each of these areas has a distinct structure and connections, they can be grouped into two "networks," defined by cortico-cortical connections that primarily interconnect areas within each network. The networks also have different connections to the striatum, medial thalamus, and other brain regions. The orbital network consists of most of the areas in the orbital cortex. It receives several sensory inputs (olfactory, gustatory, visceral afferent, somatic sensory, and visual) that appear to be related to feeding. It also receives many limbic inputs from the amygdala, entorhinal and perirhinal cortex, and subiculum, including a specific projection from the ventrolateral part of the basal amygdaloid nucleus. The orbital network may therefore serve as a substrate to integrate viscerosensory information with affective signals. The medial network consists of areas on the medial frontal surface together with a few select areas in the orbital cortex. These areas have few direct sensory inputs, and their limbic inputs are somewhat different than those to the orbital network (e.g., from the ventromedial part of the basal amygdaloid nucleus). However, they provide the major output from the OMPFC to the hypothalamus and brain stem (especially the periaqueductal gray). The medial network may therefore serve as a visceromotor system to provide frontal cortical influence over autonomic and endocrine function. Connections between the networks presumably allow information flow from viscerosensory to visceromotor systems. In addition to a probable role in eating behavior, this system appears to be involved in guiding behavior and regulation of mood. Lesions of the ventromedial prefrontal cortex result in sociopathic behavior and difficulty in making appropriate choices, whereas functional imaging studies indicate that subjects with unipolar and bipolar depression have abnormal activity in medial and orbital prefrontal areas. Many of these areas also show volume changes and decreased glial number and density in mood-disordered subjects.

Affect↗
PubMed1999

Human forebrain activation by visceral stimuli.

Visceral function is essential for survival. Discreet regions of the human brain controlling visceral function have been postulated from animal studies (Cechetto and Saper [1987] J. Comp. Neurol. 262:27-45) and suspected from lethal cardiac arrythmias (Cechetto [1994] Integr. Physiol. Behv. Sci. 29:362-373). However, these visceral sites remain uncharted in the normal human brain. We used 4-Tesla functional magnetic resonance imaging (fMRI) to identify changes in activity in discrete regions of the human brain previously identified in animal studies to be involved in visceral control. Five male subjects underwent heart rate (HR) and/or blood pressure (BP) altering tests: maximal inspiration (MX), Valsalva's maneuver (VM), and isometric handgrip (HG). Increased neuronal activity was observed during MX, VM, and HG, localized in the insular cortex, in the posterior regions of the thalamus, and in the medial prefrontal cortex. To differentiate special visceral (taste) regions from general visceral (HR, BP) regions in these areas, response to gustatory stimulation was also examined; subjects were administered saline (SAL) and sucrose (SUC) solutions as gustatory stimuli. Gustatory stimulation increased activity in the ventral insular cortex at a more inferior level than the cardiopulmonary stimuli. The observed neural activation is the first demonstration of human brain activity in response to visceral stimulation as measured by fMRI.

Autonomic Nervous System↗
PubMed1990

Gustatory responses of single neurons in the insula of the macaque monkey.

1. In recordings made from 2,925 single neurons, a region of primary taste cortex was localized to the rostral and dorsal part of the insula of the cynomolgus macaque monkey, Macaca fascicularis. The area is part of the dysgranular field of the insula and is bordered laterally by the frontal opercular taste cortex. 2. The responses of 65 single neurons with gustatory responses were analyzed in awake macaques with the use of the taste stimuli glucose, NaCl, HCl, quinine HCl (QHCl), water, and black currant juice. 3. Intensity-response functions showed that the lowest concentration in the dynamic part of the range conformed well to human thresholds for the basic taste stimuli. 4. A breadth-of-tuning coefficient was calculated for each neuron. This is a metric that can range from 0.0 for a neuron that responds specifically to only one of the four basic taste stimuli to 1.0 for one that responds equally to all four stimuli. The mean coefficient for 65 cells in the taste insula was 0.56. This tuning is sharper than that of neurons in the nucleus of the solitary tract of the monkey, and similar to that of neurons in the primary frontal opercular taste cortex. 5. A cluster analysis showed that at least six different groups of neurons were present. For each of the taste stimuli, glucose, NaCl, HCl, QHCl, water, and black currant juice, there was one group of neurons that responded much more to that tastant than to the other tastants. Other subgroups of these neurons responded to two or more of these tastants, such as glucose and black currant juice, or NaCl and QHCl. 6. On the basis of this and other evidence, it is concluded that the primary insular taste cortex, in common with the primary frontal opercular taste cortex, represents a stage of information processing in the taste system of the primate at which the tuning of neurons has become sharper than that of neurons in the nucleus of the solitary tract, and is moving toward the fineness achieved in the secondary taste cortex in the caudolateral orbitofrontal taste cortex, where motivation-dependence first becomes manifest in the taste system.

Action Potentials↗
PubMed2006

Cerebral processing of food-related stimuli: effects of fasting and gender.

To maintain nutritional homeostasis, external food-related stimuli have to be evaluated in relation to the internal states of hunger or satiety. To examine the neural circuitry responsible for integration of internal and external determinants of human eating behaviour, brain responses to visual and complex gustatory food-related stimuli were measured using functional magnetic resonance imaging in 18 healthy non-smokers (10 women, 8 men). Each individual was studied on two occasions, the order of which was counterbalanced; after eating as usual and after 24 h fasting. Raised plasma free fatty acids and lower insulin and leptin concentrations confirmed that participants fasted as requested. When fasted, participants reported more hunger, nervousness and worse mood and rated the visual (but not gustatory) food-related stimuli as more pleasant. The effect of fasting on hunger was stronger in women than in men. No circuitry was identified as differentially responsive in fasting compared to satiety to both visual and gustatory food-related stimuli. The left insula response to the gustatory stimuli was stronger during fasting. The inferior occipito-temporal response to visual food-related stimuli also tended to be stronger during fasting. The responses in the occipito-temporal cortex to visual and in the insula to gustatory stimuli were stronger in women than in men. There was no interaction between gender and fasting. In conclusion, food reactivity in modality-specific sensory cortical areas is modulated by internal motivational states. The stronger reactivity to external food-related stimuli in women may be explored as a marker of gender-related susceptibility to eating disorders.

Adult↗
PubMed1984

Cortical and subcortical, including sensory-related, afferents to the thalamic mediodorsal nucleus of the cat.

Cortical and subcortical afferents to the cat's thalamic mediodorsal nucleus (MD) were investigated using the method of retrograde transport of horseradish peroxidase (HRP). HRP was applied using vertical or oblique approaches and either a microsyringe or implanted pipettes filled with HRP-powder. A wide variety of cortical afferents to MD was detected: Aside from afferents from the cat's classical prefrontal cortex (gyri proreus, rectus, frontalis), from adjacent areas of the premotor and cingulate cortex and from portions of the insular cortex, afferents were found from cortical areas related to the processing of somatosensory, gustatory, auditory and visual information and from portions of the parietal and temporal association cortex. A considerable number of afferents arose from the diagonal band of Broca and a small number from the precommissural septum, periamygdaloid , prepiriform , entorhinal, subicular and amygdalar regions. The preoptic region and hypothalamic areas contained some labeled cells. All brains, with the exception of one with a very small dorsomedial injection, contained labeled cells in the mamillary bodies. The reticular nuclear complex and the ventral lateral geniculate nucleus were the main sources of afferents on the thalamic level. In the brain stem the substantia nigra, the ventral tegmental area, the deep layers of the superior colliculus, pretectal and tegmental regions contained labeled cells. These results show that MD receives afferents from a large variety of structures. Among them are several cortical as well as subcortical regions related to the processing of sensory and motor information. Taken together, these connections and the numerous afferents to MD from regions related to emotional and motivational behavior confirm the view that MD has to be termed association nucleus.

Afferent Pathways↗
PubMed1998

Short-term and long-term excitability changes of the insular cortical neurons after the acquisition of taste aversion learning in behaving rats.

Conditioned taste aversion, a long-lasting type of learning established after a single pairing of a novel taste and subsequent internal malaise, is an adaptive behavior to prevent animals from repeated intakes of poisonous substances. The present study was designed to identify the time-dependent excitability changes of cortical neurons to gustatory stimuli after the acquisition of conditioned taste aversion in freely behaving rats. Conditioned taste aversion to saccharin was established by an intraperitoneal injection of lithium chloride, a sickness-inducing agent, soon after an intraoral infusion of saccharin. Twenty minutes after the pairing, 25 (29%) of 86 rats showed aversive taste reactivities to saccharin, and 30 min after the pairing, all of the rats showed aversive behaviors to saccharin; these behavioral changes lasted throughout the test session (over 360 min). When unit activities were recorded from the insular cortex simultaneously with the behavioral test, 14 (11%) of 122 neurons showed a significant enhancement of excitability in response to saccharin, but not to other taste stimuli, after the acquisition of taste aversion. Eight of these 14 neurons showed a short-term enhancement: significant effects were detected only 30 min after the pairing. The remaining six neurons exhibited a long-term enhancement: the effects lasted over 360 min after the pairing. The existence of such short-term and long-term excitability changes suggests that the gustatory insular cortex is involved in different aspects of taste aversion learning.

Animals↗