Umami: a delicious flavor formed by convergence of taste and olfactory pathways in the human brain

Umami taste is produced by glutamate acting on a fifth taste system. However, glutamate presented alone as a taste stimulus is not highly pleasant, and does not act synergistically with other tastes (sweet, salt, bitter and sour). We show here that when glutamate is given in combination with a consonant, savory, odour (vegetable), the resulting flavor can be much more pleasant. Moreover, we showed using functional brain imaging with fMRI that the glutamate taste and savory odour combination produced much greater activation of the medial orbitofrontal cortex and pregenual cingulate cortex than the sum of the activations by the taste and olfactory components presented separately. Supralinear effects were much less (and significantly less) evident for sodium chloride and vegetable odour. Further, activations in these brain regions were correlated with the pleasantness and fullness of the flavor, and with the consonance of the taste and olfactory components. Supralinear effects of glutamate taste and savory odour were not found in the insular primary taste cortex. We thus propose that glutamate acts by the nonlinear effects it can produce when combined with a consonant odour in multimodal cortical taste-olfactory convergence regions. We propose the concept that umami can be thought of as a rich and delicious flavor that is produced by a combination of glutamate taste and a consonant savory odour. Glutamate is thus a flavor enhancer because of the way that it can combine supralinearly with consonant odours in cortical areas where the taste and olfactory pathways converge far beyond the receptors.     

Impaired reward processing in the human prefrontal cortex distinguishes between persistent and remittent attention deficit hyperactivity disorder

Symptoms of attention deficit hyperactivity disorder (ADHD) in children often persist into adulthood and can lead to severe antisocial behavior. However, to‐date it remains unclear whether neuro‐functional abnormalities cause ADHD, which in turn can then provide a marker of persistent ADHD. Using event‐related functional magnetic resonance imaging (fMRI), we measured blood oxygenation level dependent (BOLD) signal changes in subjects during a reversal learning task in which choice of the correct stimulus led to a probabilistically determined ‘monetary’ reward or punishment. Participants were diagnosed with ADHD during their childhood (N = 32) and were paired with age, gender, and education matched healthy controls (N = 32). Reassessment of the ADHD group as adults resulted in a split between either persistent (persisters, N = 17) or remitted ADHDs (remitters, N = 15). All three groups showed significantly decreased activation in the medial prefrontal cortex (PFC) and the left striatum during punished correct responses, however only remitters and controls presented significant psycho‐physiological interaction between these fronto‐striatal reward and outcome valence networks. Comparing persisters to remitters and controls showed significantly inverted responses to punishment (P < 0.05, family‐wise error corrected) in left PFC region. Interestingly, the decreased activation shown after punishment was located in different areas of the PFC for remitters compared with controls, suggesting that remitters might have learned compensation strategies to overcome their ADHD symptoms. Thus, fMRI helps understanding the neuro‐functional basis of ADHD related behavior differences and differentiates between persistent and remittent ADHD. Hum Brain Mapp 36:4648–4663, 2015. © 2015 Wiley Periodicals, Inc.     

The neural basis of individual differences in mate poaching

This study tested the hypothesis that individual differences in the activity of the orbitofrontal cortex, a region implicated in value-based decision-making, are associated with the preference for a person with a partner, which could lead to mate poaching. During functional magnetic resonance imaging (fMRI), male participants were presented with facial photographs of (a) attractive females with a partner, (b) attractive females without a partner, (c) unattractive females with a partner, and (d) unattractive females without a partner. The participants were asked to rate the degree to which they desired a romantic relationship with each female using an 8-point scale. The participants rated attractive females higher than unattractive females, and this effect was associated with ventral striatum activation. The participants also indicated lower ratings for females with a partner than for females without a partner, and this effect was associated with parietal cortex activation. As predicted, the participants characterized by higher orbitofrontal activity demonstrated a greater willingness to engage in a romantic relationship with females who have a partner compared with females who do not have a partner. These results are the first to provide a possible neural explanation for why certain individuals are willing to engage in mate poaching.     

The representation of the oral structures in the first somatosensory cortex of the cat

Applying light mechanical stimulations to the oral structures, multi-unit recordings (MUR) were performed, and receptive fields of neurons were defined in the somatosensory cortex S I of the cat. Oral representation was confirmed in the circumscribed area of the anterior coronal gyrus rostral to the facial area in the following order: the contralateral lips, the contralateral periodontal tissues such as the gingivae and periodontal membranes, the middle and ipsilateral part of the periodontal tissues, and the palate and tongue in a caudorostral direction. The representation of the lip and perioral tissues of the lower jaw was found on the medial side of the coronal gyrus, while the upper one was found on the lateral side. The same oral representation was confirmed by single-unit recording (SUR) analysis in the anterior coronal gyrus. The representation area of the contralateral, middle and ipsilateral site of the non-hairy lips and periodontal tissues was found in cytoarchitectural field, areas 3b and 2; somatic koniocortex.     

Segmentally arranged somatotopy within the face representation of human primary somatosensory cortex

Though somatotypic representation within the face in human primary somatosensory cortex (S1) to innocuous stimuli is controversial; previous work suggests that painful heat is represented based on an "onion-skin" or segmental pattern on the face. The aim of this study was to determine if face somatotopy for brush stimuli in S1 also follows this segmental representation model. Twelve healthy subjects (nine men: three women) underwent functional magnetic resonance imaging to measure blood oxygen level dependent signals during brush (1 Hz, 15 s) applied to their faces. Separate functional scans were collected for brush stimuli repetitively applied to each of five separate stimulation sites on the right side of the face. These sites were arranged in a vertical, horizontal, and circular manner encompassing the three divisions of the trigeminal nerve. To minimize inter-individual morphological differences in the post-central gyrus across subjects, cortical surface-based registration was implemented before group statistical image analysis. Based on activation foci, somatotopic activation in the post-central gyrus was detected for brush, consistent with the segmental face representation model.     

Waiting to win: elevated striatal and orbitofrontal cortical activity during reward anticipation in euthymic bipolar disorder adults

Nusslock R, Almeida JRC, Forbes EE, Versace A, Frank E, LaBarbara EJ, Klein CR, Phillips ML. Waiting to win: elevated striatal and orbitofrontal cortical activity during reward anticipation in euthymic bipolar disorder adults. Bipolar Disord 2012: 14: 249–260. © 2012 The Authors. Journal compilation © 2012 John Wiley & Sons A/S. Objective: Bipolar disorder may be characterized by a hypersensitivity to reward‐relevant stimuli, potentially underlying the emotional lability and dysregulation that characterizes the illness. In parallel, research highlights the predominant role of striatal and orbitofrontal cortical (OFC) regions in reward‐processing and approach‐related affect. We aimed to examine whether bipolar disorder, relative to healthy, participants displayed elevated activity in these regions during reward processing. Methods: Twenty‐one euthymic bipolar I disorder and 20 healthy control participants with no lifetime history of psychiatric disorder underwent functional magnetic resonance imaging (fMRI) scanning during a card‐guessing paradigm designed to examine reward‐related brain function to anticipation and receipt of monetary reward and loss. Data were collected using a 3T Siemens Trio scanner. Results: Region‐of‐interest analyses revealed that bipolar disorder participants displayed greater ventral striatal and right‐sided orbitofrontal [Brodmann area (BA) 11] activity during anticipation, but not outcome, of monetary reward relative to healthy controls (p < 0.05, corrected). Whole‐brain analyses indicated that bipolar disorder, relative to healthy, participants also displayed elevated left‐lateral OFC (BA 47) activity during reward anticipation (p < 0.05, corrected). Conclusions: Elevated ventral striatal and OFC activity during reward anticipation may represent a neural mechanism for predisposition to expansive mood and hypo/mania in response to reward‐relevant cues that characterizes bipolar disorder. Our findings contrast with research reporting blunted activity in the ventral striatum during reward processing in unipolar depressed individuals, relative to healthy controls. Examination of reward‐related neural activity in bipolar disorder is a promising research focus to facilitate identification of biological markers of the illness.     

Primary somatosensory cortex hand representation dynamically modulated by motor output

The brain’s primary motor and primary somatosensory cortices are generally viewed as functionally distinct entities. Here we show by means of magnetoencephalography with a phantom-limb patient, that movement of the phantom hand leads to a change in the response of the primary somatosensory cortex to tactile stimulation. This change correlates with the described conscious perception and suggests a greater degree of functional unification between the primary motor and somatosensory cortices than is currently realized. We suggest that this may reflect the evolution of this part of the human brain, which is thought to have occurred from an undifferentiated sensorimotor cortex.     

Depicting the inner and outer nose: The representation of the nose and the nasal mucosa on the human primary somatosensory cortex (SI)

The nose is important not only for breathing, filtering air, and perceiving olfactory stimuli. Although the face and hands have been mapped, the representation of the internal and external surface of the nose on the primary somatosensory cortex (SI) is still poorly understood. To fill this gap functional magnetic resonance imaging (fMRI) was used to localize the nose and the nasal mucosa in the Brodman areas (BAs) 3b, 1, and 2 of the human postcentral gyrus (PG). Tactile stimulation during fMRI was applied via a customized pneumatically driven device to six stimulation sites: the alar wing of the nose, the lateral nasal mucosa, and the hand (serving as a reference area) on the left and right side of the body. Individual representations could be discriminated for the left and right hand, for the left nasal mucosa and left alar wing of the nose in BA 3b and BA 1 by comparing mean activation maxima and Euclidean distances. Right‐sided nasal conditions and conditions in BA 2 could further be separated by different Euclidean distances. Regarding the alar wing of the nose, the results concurred with the classic sensory homunculus proposed by Penfield and colleagues. The nasal mucosa was not only determined an individual and bilateral representation, its position on the somatosensory cortex is also situated closer to the caudal end of the PG compared to that of the alar wing of the nose and the hand. As SI is commonly activated during the perception of odors, these findings underscore the importance of the knowledge of the representation of the nasal mucosa on the primary somatosensory cortex, especially for interpretation of results of functional imaging studies about the sense of smell. Hum Brain Mapp 35:4751–4766, 2014. © 2014 Wiley Periodicals, Inc .     

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.     

Neural correlates of idiographic goal priming in depression: goal-specific dysfunctions in the orbitofrontal cortex

We used functional magnetic resonance imaging (fMRI) to determine whether depressed (vs non-depressed) adults showed differences in cortical activation in response to stimuli representing personal goals. Drawing upon regulatory focus theory as well as previous research, we predicted that depressed patients would manifest attenuated left orbitofrontal cortex (OFC) activation in response to their own promotion goals as well as exaggerated right OFC activation in response to their own prevention goals. Unmedicated adults with major depression (n = 22) and adults with no history of affective disorder (n = 14) completed questionnaires and a personal goal interview. Several weeks later, they were scanned during a judgment task which (unknown to them) included stimuli representing their promotion and prevention goals. Both groups showed similar patterns of task-related activation. Consistent with predictions, patients showed significantly decreased left OFC and increased right OFC activation compared to controls on trials in which they were exposed incidentally to their promotion and prevention goals, respectively. The results suggest that depression involves dysfunction in processing two important types of personal goals. The findings extend models of the etiology of depression to incorporate cognitive and motivational processes underlying higher order goal representation and ultimately may provide an empirical basis for treatment matching.     

Active and passive touch differentially activate somatosensory cortex in texture perception

The neural mechanisms behind active and passive touch are not yet fully understood. Using fMRI we investigated the brain correlates of these exploratory procedures using a roughness categorization task. Participants either actively explored a surface (active touch) or the surface was moved under the participant's stationary finger (passive touch). The stimuli consisted of three different grades of sandpaper which participants were required to categorize as either coarse, medium, or fine. Exploratory procedure did not affect performance although the coarse and fine surfaces were more easily categorized than the medium surface. An initial whole brain analysis revealed activation of sensory and cognitive areas, including post‐central gyrus and prefrontal cortical areas, in line with areas reported in previous studies. Our main analysis revealed greater activation during active than passive touch in the contralateral primary somatosensory region but no effect of stimulus roughness. In contrast, activation in the parietal operculum (OP) was significantly affected by stimulus roughness but not by exploration procedure. Active touch also elicited greater and more distributed brain activity compared with passive touch in areas outside the somatosensory region, possibly due to the motor component of the task. Our results reveal that different cortical areas may be involved in the processing of surface exploration and surface texture, with exploration procedures affecting activations in the primary somatosensory cortex and stimulus properties affecting relatively higher cortical areas within the somatosensory system. Hum Brain Mapp, 2011. © 2010 Wiley‐Liss, Inc.     

Reward-related activity in the human motor cortex

The human primary motor cortex (M1) participates in motor learning and response selection, functions that rely on feedback on the success of behavior (i.e. reward). To investigate the possibility that behavioral contingencies alter M1 activity in humans, we tested intracortical inhibition with single and paired (subthreshold/suprathreshold) transcranial magnetic stimulation during a slot machine simulation that delivered variable money rewards for three-way matches and required no movement. A two-way match before the third barrel had stopped (increased reward expectation) was associated with more paired-pulse inhibition than no match. Receiving a large reward on the preceding trial augmented this effect. A control task that manipulated attention to the same stimuli produced no changes in excitability. The origin of this reward-related activity is not clear, although dopaminergic ventral tegmental area neurons project to M1, where they are thought to inhibit output neurons and could be the source of the finding. Transcranial magnetic stimulation of M1 may be useful as a quantitative measure of reward-related activity.     

Orbito‐frontal cortex mechanism of inhibition of return in current and remitted depression

Deficient inhibition of return (IOR) for emotional materials is an important cognitive biomarker of depression. However, its neural mechanism and role in depression remission remain largely unknown. Using functional magnetic resonance imaging (fMRI), this study observed the neural foundation of inhibition of return in individuals with current (n = 30) and remitted (n = 27) depression and in healthy controls (n = 33), by using a cue‐target task. The results showed that individuals with remitted depression (RMD) possessed a nonavoidant attention model for sad faces, which indicated a cue validity and was correlated with enhanced task‐ and resting‐state activation and function connectivity in orbitofrontal cortex (OFC). The patients with major depressive disorder (MDD), in contrast, displayed an IOR effect for all faces, which indicated a strategy of attention avoidance due to the high cognitive burden in the cue‐target task, and was correlated with decreased resting‐state activation and function connectivity in OFC. Moreover, the hippocampus, a less‐known cortex in IOR, showed a contrary model, that is, lower activation in depression remission and higher task‐ and resting‐state activation in depressive episodes. The results suggest the OFC mechanism of the IOR effect in remitted depression and the hippocampus mechanism of the IOR effect in depressive episodes, which offer potential biomarkers for the clinical treatment of depression.     

Deficits in inferior frontal cortex activation in euthymic bipolar disorder patients during a response inhibition task

Townsend JD, Bookheimer SY, Foland‐Ross LC, Moody TD, Eisenberger NI, Fischer JS, Cohen MS, Sugar CA, Altshuler LL. Deficits in inferior frontal cortex activation in euthymic bipolar disorder patients during a response inhibition task.
Bipolar Disord 2012: 14: 442–450. © 2012 The Authors. Journal compilation © 2012 John Wiley & Sons A/S. Objectives: The inferior frontal cortical–striatal network plays an integral role in response inhibition in normal populations. While inferior frontal cortex (IFC) impairment has been reported in mania, this study explored whether this dysfunction persists in euthymia. Methods: Functional magnetic resonance imaging (fMRI) activation was evaluated in 32 euthymic patients with bipolar I disorder and 30 healthy subjects while performing the Go/NoGo response inhibition task. Behavioral data were collected to evaluate accuracy and response time. Within‐group and between‐group comparisons of activation were conducted using whole‐brain analyses to probe significant group differences in neural function. Results: Both groups activated bilateral IFC. However, between‐group comparisons showed a significantly reduced activation in this brain region in euthymic patients with bipolar disorder compared to healthy subjects. Other frontal and basal ganglia regions involved in response inhibition were additionally significantly reduced in bipolar disorder patients, in both the medicated and the unmedicated subgroups. No areas of greater activation were observed in bipolar disorder patients versus healthy subjects. Conclusions: Bipolar disorder patients, even during euthymia, have a persistent reduction in activation of brain regions involved in response inhibition, suggesting that reduced activation in the orbitofrontal cortex and striatum is not solely related to the state of mania. These findings may represent underlying trait abnormalities in bipolar disorder.     

Face representation in the human secondary somatosensory cortex.

OBJECTIVE: To investigate the somatotopic organization of the facial skin area in the secondary somatosensory cortex (SII) in humans. METHODS: Somatosensory evoked magnetic fields following air-puff stimulation of 5 body sites, the foot, the lip and 3 points of the facial skin (forehead, cheek and mandibular angle point), were recorded. We focused on activities in SII following stimulation of these 5 sites and compared dipole locations among them. RESULTS: There was a clear somatotopic organization in SII with lip in the most lateral area, foot in the most medial area and face in an intermediate area close to the lip area. However, there was no significant difference of dipole localization in SII among the 3 areas of facial skin, similar to the overlapped somatotopic organization of facial skin areas in the primary somatosensory cortex in our previous study. CONCLUSIONS: The facial skin areas are considered to occupy a small area in SII with insufficient spatial separation to differentiate each area of facial skin even using magnetoencephalography which has a high spatial resolution. SIGNIFICANCE: This is the first systematic study of the activated regions in SII following stimulation of the facial skin.     

The orbitofrontal cortex represents advantageous choice in the Iowa gambling task

A good‐based model, the central neurobiological model of economic decision‐making, proposes that the orbitofrontal cortex (OFC) represents binary choice outcome, that is, the chosen good. A good is defined by a group of determinants characterizing the conditions in which the commodity is offered, including commodity type, cost, risk, time delay, and ambiguity. Previous studies have found that the OFC represents the binary choice outcome in decision‐making tasks involving commodity type, cost, risk, and delay. Real‐life decisions are often complex and involve uncertainty, rewards, and penalties; however, whether the OFC represents binary choice outcomes in a complex decision‐making situation, for example, Iowa gambling task (IGT), remains unclear. Here, we propose that the OFC represents binary choice outcome, that is, advantageous choice versus disadvantageous choice, in the IGT. We propose two hypotheses: first, the activity pattern in the human OFC represents an advantageous choice; and second, choice induces an OFC‐related functional network. Using functional magnetic resonance imaging and advanced machine‐learning tools, we found that the OFC represented an advantageous choice in the IGT. The OFC representation of advantageous choice was related to decision‐making performance. Choice modulated the functional connectivity between the OFC and the superior medial gyrus. In conclusion, the OFC represents an advantageous choice during the IGT. In the framework of a good‐based model, the results extend the role of the OFC to complex decision‐making situation when making a binary choice.     

Cognitive influences on the affective representation of touch and the sight of touch in the human brain

We show that the affective experience of touch and the sight of touch can be modulated by cognition, and investigate in an fMRI study where top-down cognitive modulations of bottom-up somatosensory and visual processing of touch and its affective value occur in the human brain. The cognitive modulation was produced by word labels, ‘Rich moisturizing cream’ or ‘Basic cream’, while cream was being applied to the forearm, or was seen being applied to a forearm. The subjective pleasantness and richness were modulated by the word labels, as were the fMRI activations to touch in parietal cortex area 7, the insula and ventral striatum. The cognitive labels influenced the activations to the sight of touch and also the correlations with pleasantness in the pregenual cingulate/orbitofrontal cortex and ventral striatum. Further evidence of how the orbitofrontal cortex is involved in affective aspects of touch was that touch to the forearm [which has C fiber Touch (CT) afferents sensitive to light touch] compared with touch to the glabrous skin of the hand (which does not) revealed activation in the mid-orbitofrontal cortex. This is of interest as previous studies have suggested that the CT system is important in affiliative caress-like touch between individuals.     

Somatotopic representation of the tongue in human secondary somatosensory cortex

OBJECTIVE: To clarify the somatotopic representation of the tongue secondary somatosensory cortex (SII) in humans. METHODS: Somatosensory evoked magnetic fields (SEFs) were recorded from nine subjects after stimulating four body sites, left antero (LA) and postero (LP) lateral margins of the tongue, left median nerve at the wrist (Hand), and left tibial nerve at the ankle (Foot). RESULTS: Clear neural activities were recorded from the bilateral SII in both hemispheres after the four sites were stimulated. The tongue SII for LA and LP was located close to the hand SII and significantly more anterior than the Foot SII. There was no significant difference in the location of dipoles between the LA and LP areas of the tongue SII. The mean peak latencies of the tongue SII for LA and LP were significantly shorter in the hemisphere contralateral to the stimulation than the ipsilateral hemisphere. CONCLUSIONS: The tongue areas are considered to occupy a small region in SII with insufficient spatial separation to differentiate anterior from posterior areas even using magnetoencephalography which has a higher spatial resolution than electroencephalography (EEG). SIGNIFICANCE: This is the first systematical study to clarify the activated regions in SII following stimulation of the tongue.