Taste and olfactory intensity perception changes following left insular stroke

The authors tested suprathreshold intensity perception of gustatory and olfactory stimuli in a 70-year-old right-handed man following a left posterior insular stroke and compared his results with those of age-matched controls. Both modalities revealed significant differences between left (ipsilateral to lesion) and right (contralateral) ratings of intensity. In both gustation and olfaction, these differences were driven primarily by trends toward increased contralateral sensitivity relative to controls. Intensity changes were most pronounced for unpleasant odors and for tastes perceived strongly as either pleasant (sweet) or unpleasant (salty, bitter). These results show that a left posterior insula lesion may affect taste and olfactory perception similarly by increasing sensitivity contralateral to the lesion. One possible mechanism is release from inhibition at the cortical level.     

Electrical neuroimaging reveals intensity-dependent activation of human cortical gustatory and somatosensory areas by electric taste

To analyze the neural basis of electric taste we performed electrical neuroimaging analyses of event-related potentials (ERPs) recorded while participants received electrical pulses to the tongue. Pulses were presented at individual taste threshold to excite gustatory fibers selectively without concomitant excitation of trigeminal fibers and at high intensity evoking a prickling and, thus, activating trigeminal fibers. Sour, salty and metallic tastes were reported at both intensities while clear prickling was reported at high intensity only. ERPs exhibited augmented amplitudes and shorter latencies for high intensity. First activations of gustatory areas (bilateral anterior insula, medial orbitofrontal cortex) were observed at 70-80 ms. Common somatosensory regions were more strongly, but not exclusively, activated at high intensity. Our data provide a comprehensive view on the dynamics of cortical processing of the gustatory and trigeminal portions of electric taste and suggest that gustatory and trigeminal afferents project to overlapping cortical areas.     

Taste perception in patients with insular cortex lesions.

Research on nonhuman primates suggests that the primary taste cortex in humans is located in the rostrodorsal insula. Qualitative and quantitative assessment of taste perception was performed on 6 patients with unilateral damage to the insula, 3 patients with brain damage outside the insula, and 11 age-matched, normal subjects. Each subject identified the quality and intensity of the gustatory stimuli applied separately to the left and right sides of the anterior tongue. Damage to the right insula produced ipsilateral taste recognition and intensity deficits. Damage to the left insula caused an ipsilateral deficit in taste intensity but a bilateral deficit in taste recognition. The unexpected deficit in the left-hemispheric stroke patients for taste recognition on the right side of the tongue suggests that taste information from both sides of the tongue passes through the left insula.     

Facial and affective reactions to tastes and their modulation by sadness and joy

This study examined adults' affective and facial reactions to tastes which differ in quality and valence, and the impact of sadness and joy on these reactions. Thirty-six male and female subjects participated voluntarily. Subjects each tasted 6 ml of a sweet chocolate drink, a bitter quinine solution (0.0015 M) and a bitter-sweet soft drink. Following a baseline period, either joy or sadness was induced using film clips before the same taste stimuli were presented for a second time. Subjects rated the drinks' pleasantness and intensity of taste immediately after each stimulus presentation. Facial reactions were videotaped and analysed using the Facial Action Coding System (FACS [P. Ekman, W.V. Friesen, Facial Action Coding System: Manual. Palo Alto, CA: Consulting Psychologists Press; 1978., P. Ekman, W. Friesen, J. Hager, Facial Action Coding System. Salt Lake City, Utah: Research Nexus; 2002.]). The results strongly indicated that the tastes produced specific facial reactions that bear strong similarities to the facial reactivity patterns found in human newborns. The data also suggest that some adults' facial reactions serve additional communicative functions. Emotions modulated taste ratings, but not facial reactions to tastes. In particular, ratings of the sweet stimulus were modulated in congruence with emotion quality, such that joy increased and sadness decreased the pleasantness and sweetness of the sweet stimulus. No emotion-congruent modulation was found for the pleasantness and intensity ratings of the bitter or the bitter-sweet stimulus. This 'robustness' of bitter taste ratings may reflect a biologically meaningful mechanism.     

Experience-dependent neural integration of taste and smell in the human brain

Flavor perception arises from the central integration of peripherally distinct sensory inputs (taste, smell, texture, temperature, sight, and even sound of foods). The results from psychophysical and neuroimaging studies in humans are converging with electrophysiological findings in animals and a picture of the neural correlates of flavor processing is beginning to emerge. Here we used event-related fMRI to evaluate brain response during perception of flavors (i.e., taste/odor liquid mixtures not differing in temperature or texture) compared with the sum of the independent presentation of their constituents (taste and/or odor). All stimuli were presented in liquid form so that olfactory stimulation was by the retronasal route. Mode of olfactory delivery is important because neural suppression has been observed in chemosensory regions during congruent taste-odor pairs when the odors are delivered by the orthonasal route and require subjects to sniff. There were 2 flavors. One contained a familiar/congruent taste-odor pair (vanilla/sweet) and the other an unfamiliar/incongruent taste-odor pair (vanilla/salty). Three unimodal stimuli, including 2 tastes (sweet and salty) and one odor (vanilla), as well as a tasteless/odorless liquid (baseline) were presented. Superadditive responses during the perception of the congruent flavor compared with the sum of its constituents were observed in the anterior cingulate cortex (ACC), dorsal insula, anterior ventral insula extending into the caudal orbitofrontal cortex (OFC), frontal operculum, ventral lateral prefrontal cortex, and posterior parietal cortex. These regions were not present in a similar analysis of the incongruent flavor compared with the sum of its constituents. All of these regions except the ventrolateral prefrontal cortex were also isolated in a direct contrast of congruent - incongruent. Additionally, the anterior cingulate, posterior parietal cortex, frontal operculum, and ventral insula/caudal OFC were also more active in vanilla + salty minus incongruent, suggesting that delivery of an unfamiliar taste-odor combination may lead to suppressed neural responses. Taken together with previous findings in the literature, these results suggest that the insula, OFC, and ACC are key components of the network underlying flavor perception and that taste-smell integration within these and other regions is dependent on 1) mode of olfactory delivery and 2) previous experience with taste/smell combinations.     

Taste mixture interactions: Suppression, additivity, and the predominance of sweetness

Most of what is known about taste interactions has come from studies of binary mixtures. The primary goal of this study was to determine whether asymmetries in suppression between stimuli in binary mixtures predict the perception of tastes in more complex mixtures (e.g., ternary and quaternary mixtures). Also of interest was the longstanding question of whether overall taste intensity derives from the sum of the tastes perceived within a mixture (perceptual additivity) or from the sum of the perceived intensities of the individual stimuli (stimulus additivity). Using the general labeled magnitude scale together with a sip-and-spit procedure, we asked subjects to rate overall taste intensity and the sweetness, sourness, saltiness and bitterness of approximately equi-intense sucrose, NaCl, citric acid and QSO₄ stimuli presented alone and in all possible binary, ternary and quaternary mixtures. The results showed a consistent pattern of mixture suppression in which sucrose sweetness tended to be both the least suppressed quality and the strongest suppressor of other tastes. The overall intensity of mixtures was found to be predicted best by perceptual additivity. A second experiment that was designed to rule out potentially confounding effects of the order of taste ratings and the temperature of taste solutions replicated the main findings of the first experiment. Overall, the results imply that mixture suppression favors perception of sweet carbohydrates in foods at the expense of other potentially harmful ingredients, such as high levels of sodium (saltiness) and potential poisons or spoilage (bitterness and sourness).     

Bilateral lesions of the thalamic trigeminal orosensory area dissociate natural from drug reward in contrast paradigms

Substance abuse and addiction are associated with an apparent devaluation of, and inattention to, natural rewards. This consequence of addiction can be modeled using a reward comparison paradigm where rats avoid intake of a palatable taste cue that comes to predict access to a drug of abuse. Evidence suggests rats avoid intake following such pairings, at least in part, because the taste cue pales in comparison to the highly rewarding drug expected in the near future. In accordance, lesions of the gustatory thalamus or cortex eliminate avoidance of a taste cue when paired with either a drug of abuse or a rewarding sucrose solution, but not when paired with the aversive agent, LiCl. The present study used bilateral ibotenic acid lesions to evaluate the role of a neighboring thalamic structure, the trigeminal orosensory area (TOA), in avoidance of a gustatory cue when paired with sucrose (experiment 1), morphine (experiment 2), cocaine (experiment 3), or LiCl (experiment 4). The results show that the TOA lesion disrupts, but does not eliminate avoidance of a taste cue that predicts access to a preferred sucrose solution and leaves intact the development of a LiCl-induced conditioned taste aversion. The lesion does, however, eliminate the suppression of intake of a taste cue when paired with experimenter-administered morphine or cocaine using our standard parameters. As such, this is the first manipulation found to dissociate avoidance of a taste cue when mediated by a sweet or by a drug of abuse.     

Saccharin pre‐exposure enhances appetitive flavor learning in pre‐weanling rats

In adult rats, data suggest that consumption of sweet tastes that do not deliver anticipated caloric consequences using high‐intensity, non‐caloric sweeteners, such as saccharin, interferes with learned relations that may contribute to energy balance. The goal of the present study was to assess the development of learning about sweet taste and calories by assessing whether pre‐exposure to saccharin solutions reduces cue competition in pre‐weanling rats. The results demonstrated that rats pre‐exposed to saccharin and then trained with a novel grape flavor paired with a glucose‐sweetened solution consumed more of the novel grape flavor presented alone than rats that had been pre‐exposed to saccharin and given the grape flavor paired with water alone. No differences in intake of the novel grape flavor were observed in groups given pre‐exposure to water or glucose solutions. Thus, by 15 days of age, rats appear to have established an association between sweet tastes and calories, and this association can be weakened by exposure to saccharin. © 2012 Wiley Periodicals,Inc. Dev Psychobiol 54: 818–824, 2012     

On the relationship between occipital cortex activity and inhibition of return

The present study explored the relationship between inhibition of return (IOR) and visual processes by seeking evidence that IOR and changes in event-related potential (ERP) indices of occipital cortex activity covary in response to experimental manipulation. The presence or absence of a central reorienting event was manipulated within the context of a cue–target experiment. When a reorienting event was presented in the interval between cue and target, IOR was accompanied by reductions in the amplitudes of early occipital ERP peaks on validly cued trials relative to invalidly cued trials. When a reorienting event was not presented, neither IOR nor modulations of the occipital ERP peaks was observed. These results provide strong evidence that IOR arises from changes in occipital visual processing. We propose that IOR arises from a slowing of response-selection processes on validly cued trials due differences in the perceptual input to the decision-making process.     

Signal transduction and information processing in mammalian taste buds

The molecular machinery for chemosensory transduction in taste buds has received considerable attention within the last decade. Consequently, we now know a great deal about sweet, bitter, and umami taste mechanisms and are gaining ground rapidly on salty and sour transduction. Sweet, bitter, and umami tastes are transduced by G-protein-coupled receptors. Salty taste may be transduced by epithelial Na channels similar to those found in renal tissues. Sour transduction appears to be initiated by intracellular acidification acting on acid-sensitive membrane proteins. Once a taste signal is generated in a taste cell, the subsequent steps involve secretion of neurotransmitters, including ATP and serotonin. It is now recognized that the cells responding to sweet, bitter, and umami taste stimuli do not possess synapses and instead secrete the neurotransmitter ATP via a novel mechanism not involving conventional vesicular exocytosis. ATP is believed to excite primary sensory afferent fibers that convey gustatory signals to the brain. In contrast, taste cells that do have synapses release serotonin in response to gustatory stimulation. The postsynaptic targets of serotonin have not yet been identified. Finally, ATP secreted from receptor cells also acts on neighboring taste cells to stimulate their release of serotonin. This suggests that there is important information processing and signal coding taking place in the mammalian taste bud after gustatory stimulation.     

Influence of simultaneous gustatory stimuli on orthonasal and retronasal olfaction

Orthonasal and retronasal olfaction processes differ. The aim of this study was to examine whether congruent and incongruent simultaneous gustatory stimuli influence orthonasal and retronasal odorant perception, using olfactory event-related potentials as a measure. Thirty-two young, healthy subjects (16 men, 16 women) took part in two test sessions. Olfactory event-related potentials were recorded in response to a food-like odor, vanillin, and to an odor usually not associated with foods, the rose-like phenylethylalcohol. Each session consisted of four randomized blocks of 15 stimuli each which were applied either orthonasally or retronasally. Simultaneously, sweet or sour gustatory stimuli were applied. In response to retronasal vanillin, stimuli latencies P2 of the event-related potentials were significantly shorter in the congruent “sweet condition” than the incongruent “sour condition”. In contrast, with orthonasal stimulation, shorter P2 latencies were seen for both odorants in the incongruent condition. Intensity of both odorants was perceived as less pronounced after retronasal stimulation than after orthonasal stimulation. In conclusion, application of a sweet taste significantly enhanced the processing of a congruent olfactory stimulus when presented through the retronasal route. Incongruent simultaneous gustatory stimulation applied during orthonasal olfaction seemed to induce conflict priming, also resulting in faster processing.     

Attentional set effects on spinal and supraspinal responses to pain

The effects of attentional set on subjective magnitude ratings, spinal reflexes, and somatosensory evoked potentials (SEP) elicited by innocuous and painful sural nerve stimulation were investigated in 24 subjects. Cuing stimuli informed subjects as to whether a visual identification or a somatosensory rating task would follow. Twenty percent of the trials were invalidly cued, where the subjects were expecting a visual stimulus but were given a sural nerve stimulus and vice versa. Subjective magnitude ratings were lower in the invalidly cued condition than the validly cued condition. Attentional set had no effect on innocuous-related spinal or early cortical responses, nor on the spinal nociceptive withdrawal reflex. The pain-related negative difference potential (NDP) and P2 component of the SEP were largest in the invalidly cued condition. These results provide further support for our hypothesis that the NDP is generated in part by the anterior cingulate, and suggest that the anterior cingulate response to pain reflects non-pain-specific cognitive processes (e.g., orienting attention towards important stimuli in the environment and/or response competition) and not some aspect of the pain experience. The effects of attentional set on the pain-related P2 suggests that it might correspond to the P3a event-related potential. If this is the case, the pain-related P2 could serve as a useful index of neural processes involved in the cognitive-evaluative aspect of pain.     

Behavioral comparison of sucrose and l-2-amino-4-phosphonobutyrate (l-AP4) tastes in rats: Does l-AP4 have a sweet taste?

Even though it is generally thought that umami stimuli such as monosodium glutamate (MSG) and sweet stimuli such as sucrose are detected by different taste receptors, these stimuli appear to share taste qualities when amiloride (a sodium channel blocker) is present to reduce the sodium taste. Single fiber recording studies of the facial and glossopharyngeal nerves have shown that encoding of l-2-amino-4-phosphonobutyrate (l-AP4), a potent mGluR4 agonist that elicits a taste quite similar to MSG, may occur in the same fibers that also encode sweet stimuli. This suggests that l-AP4 and sweet substances may activate common receptors or afferent signaling mechanisms. We report results of behavioral experiments that test this hypothesis. In the first study, rats conditioned to avoid sucrose or l-AP4 generalized the aversion to the opposite substance, indicating that both substances elicited similar tastes. However, two taste discrimination experiments showed that rats easily discriminated between sucrose and l-AP4 over a wide range of concentrations, even when the cue function of sodium associated with l-AP4 was reduced by amiloride and neutralized by adding equimolar concentrations of NaCl to sucrose. These data suggest that even though l-AP4 and sucrose elicit similar taste qualities, one or both substances also elicit other taste qualities not shared by the opposite substance. They also suggest that the taste-mGluR4 receptor and the signal pathway activated by l-AP4 are not the same as those activated by sucrose. These data, when combined with fiber recording data, suggest that there is convergence of l-AP4 and sucrose signals at some point early in the gustatory pathway.     

Altering expectancy dampens neural response to aversive taste in primary taste cortex

The primary taste cortex consists of the insula and operculum. Previous work has indicated that neurons in the primary taste cortex respond solely to sensory input from taste receptors and lingual somatosensory receptors. Using functional magnetic resonance imaging, we show here that expectancy modulates these neural responses in humans. When subjects were led to believe that a highly aversive bitter taste would be less distasteful than it actually was, they reported it to be less aversive than when they had accurate information about the taste and, moreover, the primary taste cortex was less strongly activated. In addition, the activation of the right insula and operculum tracked online ratings of the aversiveness for each taste. Such expectancy-driven modulation of primary sensory cortex may affect perceptions of external events.     

The modulatory effects of nicotine on parietal cortex activity in a cued target detection task depend on cue reliability

This functional magnetic resonance imaging study investigates the effects of nicotine in a cued target detection task when changing cue reliability. Fifteen non-smoking volunteers were studied under placebo and nicotine (Nicorette polacrilex gum 1 and 2 mg). Validly and invalidly cued trials were arranged in blocks with high, middle and low cue reliability. Two effects of nicotine were investigated: its influence on i) parietal cortex activity underlying the processing of invalid vs. valid trials (i.e. validity effect) and ii) neural activity in the context of low, middle and high informative value of the cue (i.e. cue reliability effect). Nicotine did not affect behavioral performance. However, nicotine reduced the difference in the blood oxygenation level dependent (BOLD) signal between invalid and valid trials in the right intraparietal sulcus. The reduction of parietal activity in invalid trials was smaller in the low cue reliability condition. The same posterior parietal region exhibited a nicotinic modulation of BOLD activity in valid trials which was dependent on cue reliability: Nicotine specifically enhanced the neural activity during valid trials in the context of low cue reliability, i.e. when subjects are already in a state of low certainty. We speculate that the right intraparietal sulcus might be part of two networks working in parallel: one responsible for reorienting attention and the other for the cholinergic modulation of cue reliability. By reducing the use of the cue, nicotine modulates parietal activity related to reorienting attention in conditions with higher cue certainty. On the other hand, nicotine increases parietal activity in states of low certainty. This enhanced activation might influence brain regions, such as the posterior cingulate, directly involved in the processing of cue reliability.     

Human hedonic responses to sweetness: role of taste genetics and anatomy

While past research has suggested an association between the ability to taste PROP and liking for the taste of sucrose, many aspects of this relationship remain ambiguous. To clarify this further, 60 volunteers (40 women and 20 men) were classified as PROP super-medium or non-tasters and as sweet likers or dislikers depending on hedonic and intensity ratings for PROP and sucrose. 67% of PROP super-tasters were sweet dislikers, compared to 12% of PROP non-tasters. PROP super-tasters also rated the intensity of salty and sweet tastes as greater than did non- or medium PROP tasters, but these differences in sweet intensity could not explain the group differences in sweet liking. The groups did not differ in restraint or BMI. Taste bud density was higher in PROP super-tasters and sweet dislikers than in PROP medium or non-tasters or sweet likers. Overall these data confirm that PROP super-tasters are more likely to be sweet dislikers, and that this cannot be explained as secondary to cognitive attitudes to sweetness (restraint) or enhanced sweet intensity.     

Target processing is facilitated by motivationally relevant cues

The effect that motivationally relevant stimuli have on processes of attentional engagement and disengagement was investigated during two modified peripheral cueing paradigms. Sexual, mutilation, threatening, and neutral stimuli served as peripheral cues in both experiments. Responses were made to target location in Experiment 1 (N=19 female) and target identity in Experiment 2 (N=18 female). As indexed by enhanced target-evoked P1 and P3b component amplitudes, target processing was facilitated by the presentation of sexual and mutilation stimuli in both experiments. This facilitation in response to targets cued by sexual and mutilation stimuli occurred regardless of whether cueing was valid or invalid as demonstrated by the non-significant cue validity x picture-type interaction. As such, the processes of attentional engagement (as inferred by responses to validly cued targets) and attentional disengagement (as inferred by responses to invalidly cued targets) were not differentially affected by the motivational relevance of the preceding cue. These results indicate that in a non-clinical sample, participants can shift attention rapidly to process information following the onset of motivationally relevant stimuli at attended (valid) and unattended (invalid) locations and that target processing is facilitated by the presence of appetitive and aversive cues.     

Influence of odor cueing on the retrieval processes for autobiographical memories

This study investigated the influence of odor cueing on the retrieval process for autobiographical memories. In Experiment 1, forty two participants were asked to retrieve autobiographical memories in response to a label cue only, or a label cue with a congruent odor cue, or label cue with an incongruent odor cue. The results showed that in the label cue only condition and the incongruent odor cue condition, the latency with a concurrent task was slower than with no concurrent task. However, this was not observed in the congruent odor cue condition. In order to verify the results of Experiment 1, in Experiment 2, twenty participants were investigated with regard to autobiographical memories cued by odors having a high or low rate of identification. The results showed that memories cued by odors with a high rate of identification were retrieved faster. These results suggest that dual processing by odor and label promotes retrieval processes for autobiographical memories.     

Spatially valid proprioceptive cues improve the detection of a visual stimulus

Vision and proprioception are the main sensory modalities that convey hand location and direction of movement. Fusion of these sensory signals into a single robust percept is now well documented. However, it is not known whether these modalities also interact in the spatial allocation of attention, which has been demonstrated for other modality pairings. The aim of this study was to test whether proprioceptive signals can spatially cue a visual target to improve its detection. Participants were instructed to use a planar manipulandum in a forward reaching action and determine during this movement whether a near-threshold visual target appeared at either of two lateral positions. The target presentation was followed by a masking stimulus, which made its possible location unambiguous, but not its presence. Proprioceptive cues were given by applying a brief lateral force to the participant’s arm, either in the same direction (validly cued) or in the opposite direction (invalidly cued) to the on-screen location of the mask. The d′ detection rate of the target increased when the direction of proprioceptive stimulus was compatible with the location of the visual target compared to when it was incompatible. These results suggest that proprioception influences the allocation of attention in visual space.     

Olfactory influences on appetite and satiety in humans

Odor stimuli play a major role in perception of food flavor. Food-related odors have also been shown to increase rated appetite, and induce salivation and release of gastric acid and insulin. However, our ability to identify an odor as food-related, and our liking for food-related odors, are both learned responses. In conditioning studies, repeated experience of odors with sweet and sour tastes result in enhanced ratings of sensory quality of the paired taste for the odor on its own. More recent studies also report increased pleasantness ratings for odors paired with sucrose for participants who like sweet tastes, and conversely decreased liking and increased bitterness for quinine-paired odors. When odors were experienced in combination with sucrose when hungry, liking was not increased if tested sated, suggesting that expression of acquired liking for odors depends on current motivational state. Other studies report sensory-specific satiety is seen with food-related odors. Overall, these studies suggest that once an odor is experienced in a food-related context, that odor acquires the ability to modify both preparatory and satiety-related components of ingestion.