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.     

Taste-olfactory convergence, and the representation of the pleasantness of flavour, in the human brain

The functional architecture of the central taste and olfactory systems in primates provides evidence that the convergence of taste and smell information onto single neurons is realized in the caudal orbitofrontal cortex (and immediately adjacent agranular insula). These higher-order association cortical areas thus support flavour processing. Much less is known, however, about homologous regions in the human cortex, or how taste-odour interactions, and thus flavour perception, are implemented in the human brain. We performed an event-related fMRI study to investigate where in the human brain these interactions between taste and odour stimuli (administered retronasally) may be realized. The brain regions that were activated by both taste and smell included parts of the caudal orbitofrontal cortex, amygdala, insular cortex and adjoining areas, and anterior cingulate cortex. It was shown that a small part of the anterior (putatively agranular) insula responds to unimodal taste and to unimodal olfactory stimuli, and that a part of the anterior frontal operculum is a unimodal taste area (putatively primary taste cortex) not activated by olfactory stimuli. Activations to combined olfactory and taste stimuli where there was little or no activation to either alone (providing positive evidence for interactions between the olfactory and taste inputs) were found in a lateral anterior part of the orbitofrontal cortex. Correlations with consonance ratings for the smell and taste combinations, and for their pleasantness, were found in a medial anterior part of the orbitofrontal cortex. These results provide evidence on the neural substrate for the convergence of taste and olfactory stimuli to produce flavour in humans, and where the pleasantness of flavour is represented in the human brain.     

On-line psychophysical data acquisition and event-related fMRI protocol optimized for the investigation of brain activation in response to gustatory stimuli

An experimental method for event-related functional magnetic resonance imaging that allows for the presentation of several chemosensory stimuli in the oral cavity during the same run, the collection of psychophysical measures (intensity or pleasantness) during the presentation of the stimuli, and the analysis of the data in an event-related fashion are described. The automatic pumps used to present taste stimuli allowed for multiple tastes to be delivered in small amounts under computer control. Psychophysical ratings of pleasantness or intensity were collected after each presentation of a taste stimulus and water, with the general labeled magnitude scale, using a joystick that controlled the movement of an arrow on the visual display. Performing these cognitive tasks required that the participant remained focused, and aided in the interpretation of the data collected. The perceived pleasantness differed across stimuli for all conditions; however, pleasantness ratings for the same stimulus displayed consistency, over the duration of the run and before each scan on separate days. Activation in response to sucrose and caffeine while the participant rated pleasantness was found in the insula, frontal operculum, rolandic operculum and orbitofrontal cortex which is consistent with previous taste fMRI studies.     

Consciousness Versus Attention

We consider paradigms attempting to prove that attention and consciousness are independent. As part of the analysis, we introduce the notion of the ‘Creativity Effects’, which allow for a more precise analysis of the interaction between conscious/attended processing and that of which there is no consciousness. Two such effects are considered, one at a high level, which allows filling in from memory of apparently stimulus-free activity when noisy stimuli are unattended. This leads to increased confidence but also increased error rate. The other is at a lower cortical level, involving as it does increasing the size of relevant neuron receptive fields by removing attention; subsequent attended processing can then lead to increased accuracy in detecting noisy stimuli. These effects are applied to certain experiments [1–3] to explain how apparently attention-free awareness arises through a process in which attention actually plays a crucial role. It also shows that at least in these experiments, consciousness and attention are not independent (as has been claimed in [4, 5] and numerous other places).     

Mixture Perception of rORI7 Agonists with Similar Odors

The straight-chain aldehyde hexanal has a distinct ??green-grassy?? smell quite different from the similar ??citrus-waxy??-smelling homologues heptanal to undecanal (Kittel et al., Chemosens Percept 1:235?C241, 2008). Two prior studies demonstrated the absence of cross-adaptation between hexanal and three other homologues (Kurtz et al., Chemosens Percept 3:149?C155, 2010) but a significant mixture suppression between the dissimilar-smelling odorants hexanal and octanal (Kurtz et al., Chemosens Percept 4:186?C194, 2009). In contrast, this study of similar-smelling octanal and decanal showed little mixture suppression. In contrast to the hexanal and octanal adaptation, data from Kurtz et al. (Chemosens Percept 3:149?C155, 2010) showed a significant cross-adaptation between octanal and decanal. The differences observed between mixture suppression and adaptation suggest that these two phenomena are processed separately.     

Identification of human gustatory cortex by activation likelihood estimation

Over the last two decades, neuroimaging methods have identified a variety of taste-responsive brain regions. Their precise location, however, remains in dispute. For example, taste stimulation activates areas throughout the insula and overlying operculum, but identification of subregions has been inconsistent. Furthermore, literature reviews and summaries of gustatory brain activations tend to reiterate rather than resolve this ambiguity. Here, we used a new meta-analytic method [activation likelihood estimation (ALE)] to obtain a probability map of the location of gustatory brain activation across 15 studies. The map of activation likelihood values can also serve as a source of independent coordinates for future region-of-interest analyses. We observed significant cortical activation probabilities in: bilateral anterior insula and overlying frontal operculum, bilateral mid dorsal insula and overlying Rolandic operculum, and bilateral posterior insula/parietal operculum/postcentral gyrus, left lateral orbitofrontal cortex (OFC), right medial OFC, pregenual anterior cingulate cortex (prACC) and right mediodorsal thalamus. This analysis confirms the involvement of multiple cortical areas within insula and overlying operculum in gustatory processing and provides a functional "taste map" which can be used as an inclusive mask in the data analyses of future studies. In light of this new analysis, we discuss human central processing of gustatory stimuli and identify topics where increased research effort is warranted.     

Uses and Abuses of Patient Reported Outcome Measures (PROMs): Potential Iatrogenic Impact of PROMs Implementation and How It Can Be Mitigated

Having been a national advocate for the use of patient reported outcome measures (PROMs) in Child and Adolescent Mental Health Services (CAMHS) in the UK for the last decade, I have become increasingly concerned that unless the potential iatrogenic impact of widespread policy requirement for use of PROMs (Department of Health, Children and Young People’s Health Outcomes Strategy, 2012) is recognised and addressed their real potential benefits (Sapyta et al., J Clin Psychol 61(2):145–153, 2005) may never be realized. Drawing on examples from PROMs implementation in CAMHS in the UK (Wolpert et al., J Ment Health 21(2):165–173, 2012a; Child Adolesc Mental Health 17(3):129–130, 2012b). I suggest key ways forward if PROMs are to support best clinical practice rather than undermine it.     

Selective attention to affective value alters how the brain processes taste stimuli

How does selective attention to affect influence sensory processing? In an fMRI investigation, when subjects were instructed to remember and rate the pleasantness of a taste stimulus, 0.1 m monosodium glutamate, activations were greater in the medial orbitofrontal and pregenual cingulate cortex than when subjects were instructed to remember and rate the intensity of the taste. When the subjects were instructed to remember and rate the intensity, activations were greater in the insular taste cortex. An interaction analysis showed that this dissociation of taste processing, depending on whether attention to pleasantness or intensity was relevant, was highly significant (P < 0.0002). Thus, depending on the context in which tastes are presented and whether affect is relevant, the brain responds to a taste differently. These findings show that, when attention is paid to affective value, the brain systems engaged to represent the sensory stimulus of taste are different from those engaged when attention is directed to the physical properties of a stimulus such as its intensity. This differential biasing of brain regions engaged in processing a sensory stimulus, depending on whether the cognitive demand is for affect‐related vs. more sensory‐related processing, may be an important aspect of cognition and attention. This has many implications for understanding the effects not only of taste but also of other sensory stimuli.     

Emotional self-reference: brain structures involved in the processing of words describing one's own emotions

The present functional magnetic resonance imaging study investigated the role of emotion-related (e.g., amygdala) and self-related brain structures (MPFC in particular) in the processing of emotional words varying in stimulus reference. Healthy subjects (N = 22) were presented with emotional (pleasant or unpleasant) or neutral words in three different conditions: (1) self (e.g., my fear), (2) other (e.g., his fear) and (3) no reference (e.g., the fear). Processing of unpleasant words was associated with increased amygdala and also insula activation across all conditions. Pleasant stimuli were specifically associated with increased activation of amygdala and insula when related to the self (vs. other and no reference). Activity in the MPFC (vMPFC in particular) and anterior cingulate cortex (ACC) was preferentially increased during processing of self-related emotional words (vs. other and no reference). These results demonstrate that amygdala activation in response to emotional stimuli is modulated by stimulus reference and that brain structures implicated in emotional and self-related processing might be important for the subjective experience of one's own emotions.     

Individual Variability in the Awareness of Odors: Demographic Parameters and Odor Identification Ability

Human chemosensation can be strongly influenced by how much attention people pay to chemosensory stimuli (e.g., Marks and Wheeler in Chem Senses 23:19?C29, 1998; Prescott et al. in Chem Senses 29:331?C340, 2004). In a recent study, a scale has been devised (i.e., the Odor Awareness Scale; OAS; see Smeets et al. in Chem Senses 33:725?C734, 2008) to investigate the level of awareness people have of the available odorants in the environment. Here, we explored whether a variant (Italian version) of the OAS could be used to discriminate between different groups of participants in terms of olfactory abilities (i.e., performance in an odor identification task) and/or personal/demographic characteristics (e.g., gender, age, etc.). Ninety-eight participants underwent this study that was composed of a personal detail questionnaire, the OAS, and a deep investigation of odor identification ability based on a large variety of odor stimuli. During 6 testing sessions, a total of 72 odor stimuli were evaluated: 36 aromas in vapor phase presented in vials and 36 chemical compounds in hydroalcoholic solutions. The results did not indicate any relationships between the participants?? declared awareness of odors and the real performance in the identification test. However, differences in the awareness of odors were found as a function of a number of personal factors such as, for example, gender (with females showing higher scores than males) or age (with younger collecting lower scores than older participants). In conclusion, we could not predict from modified OAS scores the participants?? specific ability to identify odors. Nevertheless, we could extend the scale??s characterization by highlighting different connections between OAS scores and individual parameters.     

Neural correlates of evaluative compared with passive tasting

We used functional magnetic resonance imaging to test the hypothesis that the nature of the neural response to taste varies as a function of the task the subject is asked to perform. Subjects received sweet, sour, salty and tasteless solutions passively and while evaluating stimulus presence, pleasantness and identity. Within the insula and overlying operculum the location of maximal response to taste vs. tasteless varied as a function of task; however, the primary taste cortex (anterior dorsal insula/frontal operculum – AIFO), as well as a more ventral region of anterior insula, responded to taste vs. tasteless irrespective of task. Although the response here did not depend upon task, preferential connectivity between AIFO and the amygdala (bilaterally) was observed when subjects tasted passively compared with when they performed a task. This suggests that information transfer between AIFO and the amygdala is maximal during implicit processing of taste. In contrast, a region of the left lateral orbitofrontal cortex (OFC) responded preferentially to taste and to tasteless when subjects evaluated pleasantness, and was preferentially connected to earlier gustatory relays (caudomedial OFC and AIFO) when a taste was present. This suggests that processing in the lateral OFC organizes the retrieval of gustatory information from earlier relays in the service of computing perceived pleasantness. These findings show that neural encoding of taste varies as a function of task beyond that of the initial cortical representation.     

Prediction error and somatosensory insula activation in women recovered from anorexia nervosa

BackgroundPrevious research in patients with anorexia nervosa showed heightened brain response during a taste reward conditioning task and heightened sensitivity to rewarding and punishing stimuli. Here we tested the hypothesis that individuals recovered from anorexia nervosa would also experience greater brain activation during this task as well as higher sensitivity to salient stimuli than controls.MethodsWomen recovered from restricting-type anorexia nervosa and healthy control women underwent fMRI during application of a prediction error taste reward learning paradigm.ResultsTwenty-four women recovered from anorexia nervosa (mean age 30.3 ± 8.1 yr) and 24 control women (mean age 27.4 ± 6.3 yr) took part in this study. The recovered anorexia nervosa group showed greater left posterior insula activation for the prediction error model analysis than the control group (family-wise error– and small volume–corrected p < 0.05). A group × condition analysis found greater posterior insula response in women recovered from anorexia nervosa than controls for unexpected stimulus omission, but not for unexpected receipt. Sensitivity to punishment was elevated in women recovered from anorexia nervosa.LimitationsThis was a cross-sectional study, and the sample size was modest.ConclusionAnorexia nervosa after recovery is associated with heightened prediction error–related brain response in the posterior insula as well as greater response to unexpected reward stimulus omission. This finding, together with behaviourally increased sensitivity to punishment, could indicate that individuals recovered from anorexia nervosa are particularly responsive to punishment. The posterior insula processes somatosensory stimuli, including unexpected bodily states, and greater response could indicate altered perception or integration of unexpected or maybe unwanted bodily feelings. Whether those findings develop during the ill state or whether they are biological traits requires further study.     

A salty‐congruent odor enhances saltiness: Functional magnetic resonance imaging study

Excessive intake of dietary salt (sodium chloride) may increase the risk of chronic diseases. Accordingly, various strategies to reduce salt intake have been conducted. This study aimed to investigate whether a salty‐congruent odor can enhance saltiness on the basis of psychophysical (Experiment 1) and neuroanatomical levels (Experiment 2). In Experiment 1, after receiving one of six stimulus conditions: three odor conditions (odorless air, congruent, or incongruent odor) by two concentrations (low or high) of either salty or sweet taste solution, participants were asked to rate taste intensity and pleasantness. In Experiment 2, participants received the same stimuli during the functional magnetic resonance imaging scan. In Experiment 1, compared with an incongruent odor and/or odorless air, a congruent odor enhanced not only taste intensity but also either pleasantness of sweetness or unpleasantness of saltiness. In Experiment 2, a salty‐congruent combination of odor and taste produced significantly higher neuronal activations in brain regions associated with odor–taste integration (e.g., insula, frontal operculum, anterior cingulate cortex, and orbitofrontal cortex) than an incongruent combination and/or odorless air with taste solution. In addition, the congruent odor‐induced saltiness enhancement was more pronounced in the low‐concentrated tastant than in the high‐concentrated one. In conclusion, this study demonstrates the congruent odor‐induced saltiness enhancement on the basis of psychophysical and neuroanatomical results. These findings support an alternative strategy to reduce excessive salt intake by adding salty‐congruent aroma to sodium reduced food. However, there are open questions regarding the salty‐congruent odor‐induced taste unpleasantness. Hum Brain Mapp, 2013. © 2011 Wiley Periodicals, Inc.     

The Relationship between Sensory Sensitivity and Autistic Traits in the General Population

Individuals with Autism Spectrum Disorders (ASDs) tend to have sensory processing difficulties (Baranek et al. in J Child Psychol Psychiatry 47:591–601, 2006). These difficulties include over- and under-responsiveness to sensory stimuli, and problems modulating sensory input (Ben-Sasson et al. in J Autism Dev Disorders 39:1–11, 2009). As those with ASD exist at the extreme end of a continuum of autistic traits that is also evident in the general population, we investigated the link between ASD and sensory sensitivity in the general population by administering two questionnaires online to 212 adult participants. Results showed a highly significant positive correlation (r = .775, p < .001) between number of autistic traits and the frequency of sensory processing problems. These data suggest a strong link between sensory processing and autistic traits in the general population, which in turn potentially implicates sensory processing problems in social interaction difficulties.     

Incongruent Contextual Information Intrudes on Short-term Olfactory Memory

Both name and source information provide a context for the perceptual evaluation of odorants (Herz, J Exp Psychol 132(4): 595?C606, 2003) that may also affect memory (Lyman and McDaniel, J Exp Psychol 16(4): 656?C664, 1986). The current study asked whether appropriate information about the context in which an odor source is found would affect short-term memory for the odor. Fifty-four participants were presented with pairs of olfactory stimuli and visual contextual information that either matched each other or did not. There were two types of visual stimuli, either a pictorial representation of a contextual location for an odor source or a written representation of the name of that location. Stimulus presentation was followed by a verbal interference task (Peterson and Peterson, J Exp Psychol 58: 193?C198, 1959). A recognition test for the olfactory stimuli conducted immediately afterwards revealed that participants who had been presented with visual representations of non-matching odor source contexts were more likely to falsely remember odors appropriate to the visual context. These findings suggest that participants either relied heavily on encoding of the visually presented source contextual information, to the detriment of memory, for olfactory stimuli or suffered from the semantic-based memory error of misattribution.     

Diffusion and Extrusion Shape Standing Calcium Gradients During Ongoing Parallel Fiber Activity in Dendrites of Purkinje Neurons

Synaptically induced calcium transients in dendrites of Purkinje neurons (PNs) play a key role in the induction of plasticity in the cerebellar cortex (Ito, Physiol Rev 81:1143?C1195, 2001). Long-term depression at parallel fiber?CPN synapses can be induced by stimulation paradigms that are associated with long-lasting (>1?min) calcium signals. These signals remain strictly localized (Eilers et al., Learn Mem 3:159?C168, 1997), an observation that was rather unexpected, given the high concentration of the mobile endogenous calcium-binding proteins parvalbumin and calbindin in PNs (Fierro and Llano, J Physiol (Lond) 496:617?C625, 1996; Kosaka et al., Exp Brain Res 93:483?C491, 1993). By combining two-photon calcium imaging experiments in acute slices with numerical computer simulations, we found that significant calcium diffusion out of active branches indeed takes places. It is outweighed, however, by rapid and powerful calcium extrusion along the dendritic shaft. The close interplay of diffusion and extrusion defines the spread of calcium between active and inactive dendritic branches, forming a steep gradient in calcium with drop ranges of ~13???m (interquartile range, 10?C18???m).     

The Walking Corsi Test (WalCT): standardization of the topographical memory test in an Italian population

Selective visuo-spatial memory deficits can seriously affect many aspects of daily life; for example, an individual may not remember where he put an object or which path he took to reach his destination. In general, visuo-spatial memory is assessed through pen-and-paper tests that mainly assess memory components in peripersonal space. Recent studies (Piccardi et al. in Exp Brain Res 206:171–177, 2010; Piccardi et al. in Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 18:362–384, 2011) have shown that brain-damaged patients selectively fail on navigation memory tasks but not on other tests of visuo-spatial memory ability. These findings underline the need for a standardized test that measures memory in navigation separately from other types of visuo-spatial memory. Here, we report the validation of the Walking Corsi Test (WalCT: Piccardi et al. in Neurosci Lett 432:127–131, 2008) on 289 individuals aged 15–86 years. The WalCT is a new instrument that assesses topographical memory in real environments and reproduces on a large-scale version the Corsi Block-Tapping Test (CBT: Corsi in Unpublished doctoral dissertation, McGill University, Montreal, 1972). The WalCT has been used in clinical practice and has proven sensitive in detecting navigational memory deficits even in individuals who have no other memory impairments (Piccardi et al. in Exp Brain Res 206:171–177, 2010; Piccardi et al. in Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 18:362–384, 2011; Bianchini et al. in Neuropsychologia 48:1563–1573, 2010 ).     

Correlation Between Ventromedial Prefrontal Cortex Activation to Food Aromas and Cue-Driven Eating: An fMRI Study

Food aromas are signals associated with both food's availability and pleasure. Previous research from this laboratory has shown that food aromas under fasting conditions evoke robust activation of medial prefrontal brain regions thought to reflect reward value (Bragulat et al., Obesity (Silver Spring), 18(8): 1566?C1571, 2010). In the current study, 18 women (11 normal weight and 7 obese) underwent a 2-day imaging study (one after being fed and one while fasting). All were imaged on a 3T Siemens Trio-Tim scanner while sniffing two food (F; pasta and beef) odors, one non-food (NF; Douglas fir) odor, and an odorless control (CO). Prior to imaging, participants rated hunger and perceived odor qualities and completed the Dutch Eating Behavior Questionnaire (DEBQ) to assess "externality" (the extent to which eating is driven by external food cues). Across all participants, both food and non-food odors (compared to CO) elicited large blood oxygenation level dependent (BOLD) responses in olfactory and reward-related areas, including the medial prefrontal and anterior cingulate cortex, bilateral orbitofrontal cortex, and bilateral piriform cortex, amygdala, and hippocampus. However, food odors produced greater activation of medial prefrontal cortex, left lateral orbitofrontal cortex, and inferior insula than non-food odors. Moreover, there was a significant correlation between the (F?>?CO) BOLD response in ventromedial prefrontal cortex and ??externality?? sub-scale scores of the DEBQ, but only under the fed condition; no such correlation was present with the (NF?>?CO) response. This suggests that in those with high externality, ventromedial prefrontal cortex may inappropriately valuate external food cues in the absence of internal hunger.     

Sucrose and Non-nutritive Sweeteners Can Suppress the Bitterness of Vegetables Independent of PTC Taster Phenotype

The unpleasant bitter taste found in many nutritious vegetables may deter their consumption. While bitterness suppression by sweeteners is well-studied in the chemical and pharmacological fields (Ley Chem Percept, 1:58–77, 2008), less is known about the interaction of sweeteners with the bitterness of functional foods such as vegetables. We investigated whether sweeteners decreased the bitterness of vegetables as a step toward increasing consumption. Our secondary aim was to determine whether this effect was influenced by individual variation in bitterness perception, as assessed by phenylthiocarbamide (PTC) tasting ability. In Experiment 1, 111 college students tasted and rated plain broccoli and cauliflower, then received one with the addition of sucrose. In Experiment 2, we replaced broccoli with Brussels sprouts, which are generally perceived as highly bitter (Tepper Am J Hum Genet, 63:1271–1276, 1998), and replicated the study with 76 new participants. In Experiment 3, 224 participants tasted Brussels sprouts plain and with the addition of sucrose, saccharin, aspartame, or sucralose. In all experiments, sensitivity to PTC was also measured using suprathreshold scaling with an updated generalized labeled magnitude scale. The reported bitterness of the vegetables was significantly decreased by the addition of sweeteners in each study, all p values of <0.001. In Experiment 3, the non-nutritive sweeteners (NNS) functioned identically to sucrose in suppressing bitterness and increasing palatability. The effect of the sweeteners did not vary by the participants’ PTC taster phenotype, which was treated as a continuous variable in a linear regression analysis (all R ²?<?0.05). The addition of sweeteners to vegetables reduces the bitterness that many consumers find objectionable. This robust effect was found for vegetables that varied in their perceived bitterness and regardless of individual differences in bitterness sensitivity. Importantly, the finding that NNS are as effective as sucrose at suppressing bitterness implies that sweeteners can be incorporated into the diet without the addition of calories. Furthermore, by the principles of flavor–flavor learning sweeteners will come to condition a preference for vegetables plain.