Different representations of pleasant and unpleasant odours in the human brain

Odours are important in emotional processing; yet relatively little is known about the representations of the affective qualities of odours in the human brain. We found that three pleasant and three unpleasant odours activated dissociable parts of the human brain. Pleasant but not unpleasant odours were found to activate a medial region of the rostral orbitofrontal cortex. Further, there was a correlation between the subjective pleasantness ratings of the six odours given during the investigation with activation of a medial region of the rostral orbitofrontal cortex. In contrast, a correlation between the subjective unpleasantness ratings of the six odours was found in regions of the left and more lateral orbitofrontal cortex. Moreover, a double dissociation was found with the intensity ratings of the odours, which were not correlated with the BOLD signal in the orbitofrontal cortex, but were correlated with the signal in medial olfactory cortical areas including the pyriform and anterior entorhinal cortex. Activation was also found in the anterior cingulate cortex, with a middle part of the anterior cingulate activated by both pleasant and unpleasant odours, and a more anterior part of the anterior cingulate cortex showing a correlation with the subjective pleasantness ratings of the odours. Thus the results suggest that there is a hedonic map of the sense of smell in brain regions such as the orbitofrontal cortex, and these results have implications for understanding the psychiatric and related problems that follow damage to these brain areas.     

Cerebral blood flow changes associated with attribution of emotional valence to pleasant, unpleasant, and neutral visual stimuli in a PET study of normal subjects.

OBJECTIVE: To assist in the development of a model for the psychopathology of emotions, the present study sought to identify the neural circuits associated with the evaluation of visual stimuli for emotional valence. METHOD: Seventeen healthy individuals were shown three sets of emotionally laden pictures carrying pleasant, unpleasant, and neutral content. While subjects evaluated the picture set for emotional valence, regional cerebral blood flow was measured with the use of [15O] water positron emission tomography. Subjective ratings of the emotional valence of the picture sets were recorded. Data were analyzed by comparing the images acquired during the neutral condition with the unpleasant and pleasant image sets and the unpleasant and pleasant conditions with each other. RESULTS: Processing of pleasant stimuli was associated with increased blood flow in the dorsal-lateral, orbital, and medial frontal cortex relative to the unpleasant condition and in the cingulate, precuneus, and visual cortex relative to the neutral condition. Evaluation of unpleasant stimuli activated the amygdala, visual cortex, and cerebellum relative to the pleasant condition and the nucleus accumbens, precuneus, and visual cortex relative to the neutral condition. CONCLUSIONS: Observing and assigning emotional value to unpleasant stimuli produced activations in subcortical limbic regions, whereas evaluation of pleasant stimuli produced activations in cortical limbic areas. These findings are consistent with the notion of a subcortical and archaic danger recognition system and a system detecting pleasantness in events and situations that is phylogenetically younger, involving primarily the prefrontal cortex.     

Brain activity during expectancy of emotional stimuli: an fMRI study

We studied the neural activation associated with the expectancy of emotional stimuli using whole brain fMRI. Fifteen healthy subjects underwent fMRI scanning during which they performed a warned reaction task using emotional pictures carrying pleasant, unpleasant, or neutral content. The task involved an expected or unexpected condition. Data were analyzed by comparing the images acquired under the different conditions. In the expected condition, compared with the unexpected condition, significant activation was observed in the medial, inferior and dorsolateral prefrontal cortex. Whereas the expectancy of pleasant stimuli produced activation in the left dorsolateral and left medial prefrontal cortex as well as in the right cerebellum, the expectancy of unpleasant stimuli produced activation in the right inferior and right medial prefrontal cortex, the right amygdala, the left anterior cingulate cortex, and bilaterally in the visual cortex. These results suggest that the expectancy of emotional stimuli is mediated by the prefrontal area including the medial, inferior, and dorsolateral prefrontal cortex. Furthermore, our data suggest that left frontal activation is associated with the expectancy of pleasant stimuli and that right frontal activation is associated with the expectancy of unpleasant stimuli. Finally, our findings suggest that the amygdala and anterior cingulate cortex may play an important role in the expectancy of unpleasant stimuli and that the input of this negative information is modulated by these specific brain areas.     

Wednesday July 5, 200615:00–17:00Hall 5CDiscussion Group SessionEpilepsy and the emotional brain

¹ A. Papanicolaou (   ¹ The University of Texas Medical School, USA )
Affective valence–specific spatiotemporal brain activation profiles: an MEG study
Regions of the brain involved in the generation of affect in response to picture sets rated as extremely unpleasant(disgusting and/or fearful), pleasant(sexually arousing), and affectively neutral, as well as the order of activation of each region, were investigated using magnetoencephalography (MEG) in a group of sixteen young normal adult male volunteers. We found spatiotemporal maps consisting of two basic components: An early one involving activation in the occipital and basal aspects of the temporal cortex, related to the perception of the stimuli was common to all three affect conditions. The second, later component, involving activation of the cingulate gyrus, the prefrontal cortex and the temporal lobes, differentiated the pleasant and unpleasant conditions, featuring more activity over right hemisphere structures during the unpleasant condition. These activation patterns are consistent with the notion of hemispheric specialization for affective valence and they demonstrate the utility of the MEG method in exploring both the structures involved in the generation of affective responses and the temporal order of their activation.     

Expecting unpleasant stimuli – An fMRI study

Expecting forthcoming events and preparing adequate responses are important cognitive functions that help the individual to deal with the environment. The emotional valence of an event is decisive for the resulting action. Revealing the underlying mechanisms may help to understand the dysfunctional information processing in depression and anxiety that are associated with negative expectation of the future. We were interested in selective brain activity during the expectation of unpleasant visual stimuli. Twelve healthy female subjects were biased to expect and then perceive emotionally unpleasant, pleasant or neutral stimuli during functional magnetic resonance imaging. Expecting unpleasant stimuli relative to expecting pleasant and neutral stimuli resulted in activation of mainly cingulate cortex, insula, prefrontal areas, thalamus, hypothalamus and striatum. While certain areas were also active during subsequent presentation of the emotional stimuli, distinct regions of the anterior cingulate gyrus and the thalamus were solely active during expectation of the unpleasant stimuli. The identified areas may reflect a network for internal adaptation and preparation processes in order to react adequately to expected unpleasant events. They are known as well to be altered in depression. Disorders of this network may be relevant for psychiatric disorders such as depression.     

Expecting unpleasant stimuli--an fMRI study

Expecting forthcoming events and preparing adequate responses are important cognitive functions that help the individual to deal with the environment. The emotional valence of an event is decisive for the resulting action. Revealing the underlying mechanisms may help to understand the dysfunctional information processing in depression and anxiety that are associated with negative expectation of the future. We were interested in selective brain activity during the expectation of unpleasant visual stimuli. Twelve healthy female subjects were biased to expect and then perceive emotionally unpleasant, pleasant or neutral stimuli during functional magnetic resonance imaging. Expecting unpleasant stimuli relative to expecting pleasant and neutral stimuli resulted in activation of mainly cingulate cortex, insula, prefrontal areas, thalamus, hypothalamus and striatum. While certain areas were also active during subsequent presentation of the emotional stimuli, distinct regions of the anterior cingulate gyrus and the thalamus were solely active during expectation of the unpleasant stimuli. The identified areas may reflect a network for internal adaptation and preparation processes in order to react adequately to expected unpleasant events. They are known as well to be altered in depression. Disorders of this network may be relevant for psychiatric disorders such as depression.     

Neural mechanisms involved in odor pleasantness and intensity judgments

Olfactory processing in the human brain was examined using positron emission tomography. Twelve normal volunteers were scanned while smelling pairs of odors: they were asked to judge which odor was more pleasant in one condition, and which was more intense in a second condition; they also were scanned while sniffing an odorless stimulus. As in prior studies, greater cerebral blood flow was found in the right orbitofrontal cortex during both pleasantness and intensity judgments as compared to baseline. Cerebellar activity was also seen, but contrary to expectations no activity was detected in the primary olfactory (piriform) cortex. Only the pleasantness judgment elicited additional activity within the hypothalamus, suggesting that this structure may be involved in affective processing that requires access to information about internal state.     

Gustatory and olfactory function in patients with unipolar and bipolar depression

Although the crucial distinction between unipolar depressive disorder and bipolar disorder is the presence of mania (or hypomania) in the course of the latter, significant differences between unipolar and bipolar depression have also been found in clinical studies. The primary aim of the present investigation was to assess pleasantness/unpleasantness ratings of chemosensory stimuli in depressed patients, including subjects with unipolar and bipolar depression. Sensory aspects (thresholds and identification abilities) of gustatory and olfactory function were also assessed. There were no major differences between a depression group, as a whole, and healthy controls in terms of gustatory and olfactory thresholds and identification abilities. Similarly, pleasantness ratings of various gustatory and olfactory stimuli did not differ between the control and depression group. Gustatory and olfactory thresholds and identification abilities did not differ between individuals with unipolar and bipolar depression. Bipolar patients tended to rate less gustatory stimuli as unpleasant and more olfactory stimuli as pleasant compared to unipolar patients. The present results suggest that: i) depression is not associated with any major deficit in sensory aspects of gustatory and olfactory function or altered hedonic ratings of chemosensory stimuli; ii) hedonic responses to chemosensory stimuli tend to be increased in bipolar as compared to unipolar depressed patients.     

Affective picture perception: gender differences in visual cortex?

Activity in extrastriate visual cortex is greater when people view emotional relative to neutral pictures. Prior brain imaging and psychophysiological work has further suggested a bias for men to react more strongly to pleasant pictures, and for women to react more strongly to unpleasant pictures. Here we investigated visual cortical activity using fMRI in 28 men and women during picture viewing. Men and women showed reliably greater visual cortical reactivity during both pleasant and unpleasant pictures, relative to neutral, consistent with the view that the motivational relevance of visual stimuli directs attention and enhances elaborative perceptual processing. However, men did show greater extrastriate activity than women specifically during erotic picture perception, possibly reflecting a gender-specific visual mechanism for sexual selection.     

Tagging cortical networks in emotion: A topographical analysis

Viewing emotional pictures is associated with heightened perception and attention, indexed by a relative increase in visual cortical activity. Visual cortical modulation by emotion is hypothesized to reflect re‐entrant connectivity originating in higher‐order cortical and/or limbic structures. The present study used dense‐array electroencephalography and individual brain anatomy to investigate functional coupling between the visual cortex and other cortical areas during affective picture viewing. Participants viewed pleasant, neutral, and unpleasant pictures that flickered at a rate of 10 Hz to evoke steady‐state visual evoked potentials (ssVEPs) in the EEG. The spectral power of ssVEPs was quantified using Fourier transform, and cortical sources were estimated using beamformer spatial filters based on individual structural magnetic resonance images. In addition to lower‐tier visual cortex, a network of occipito‐temporal and parietal (bilateral precuneus, inferior parietal lobules) structures showed enhanced ssVEP power when participants viewed emotional (either pleasant or unpleasant), compared to neutral pictures. Functional coupling during emotional processing was enhanced between the bilateral occipital poles and a network of temporal (left middle/inferior temporal gyrus), parietal (bilateral parietal lobules), and frontal (left middle/inferior frontal gyrus) structures. These results converge with findings from hemodynamic analyses of emotional picture viewing and suggest that viewing emotionally engaging stimuli is associated with the formation of functional links between visual cortex and the cortical regions underlying attention modulation and preparation for action. Hum Brain Mapp, 2012. © 2011 Wiley Periodicals, Inc.     

Amygdala activation during reading of emotional adjectives--an advantage for pleasant content

This event-related functional magnetic resonance imaging (fMRI)study investigated brain activity elicited by emotional adjectivesduring silent reading without specific processing instructions.Fifteen healthy volunteers were asked to read a set of randomlypresented high-arousing emotional (pleasant and unpleasant)and low-arousing neutral adjectives. Silent reading of emotionalin contrast to neutral adjectives evoked enhanced activationsin visual, limbic and prefrontal brain regions. In particular,reading pleasant adjectives produced a more robust activationpattern in the left amygdala and the left extrastriate visualcortex than did reading unpleasant or neutral adjectives. Moreover,extrastriate visual cortex and amygdala activity were significantlycorrelated during reading of pleasant adjectives. Furthermore,pleasant adjectives were better remembered than unpleasant andneutral adjectives in a surprise free recall test conductedafter scanning. Thus, visual processing was biased towards pleasantwords and involved the amygdala, underscoring recent theoreticalviews of a general role of the human amygdala in relevance detectionfor both pleasant and unpleasant stimuli. Results indicate preferentialprocessing of pleasant information in healthy young adults andcan be accounted for within the framework of appraisal theory.     

Nonlinear relationship between emotional valence and brain activity: Evidence of separate negative and positive valence dimensions

Emotion plays a significant role in goal‐directed behavior, yet its neural basis is yet poorly understood. In several psychological models the cardinal dimensions that characterize the emotion space are considered to be valence and arousal. Here 3T functional magnetic resonance imaging (fMRI) was used to reveal brain areas that show valence‐ and arousal‐dependent blood oxygen level dependent (BOLD) signal responses. Seventeen healthy adults viewed pictures from the International Affective Picture System (IAPS) for brief 100 ms periods in a block design paradigm. In many brain regions BOLD signals correlated significantly positively with valence ratings of unpleasant pictures. Interestingly, partly in the same regions but also in several other regions BOLD signals correlated negatively with valence ratings of pleasant pictures. Therefore, there were several areas where the correlation across all pictures was of inverted U‐shape. Such correlations were found bilaterally in the dorsolateral prefrontal cortex (DLPFC), dorsomedial prefrontal cortex (DMPFC) extending to anterior cingulate cortex (ACC), and insula. Self‐rated arousal of those pictures which were evaluated to be unpleasant correlated with BOLD signal in the ACC, whereas for pleasant pictures arousal correlated positively with the BOLD signal strength in the right substantia innominata. We interpret our results to suggest a major division of brain mechanisms underlying affective behavior to those evaluating stimuli to be pleasant or unpleasant. This is consistent with the basic division of behavior to approach and withdrawal, where differentiation of hostile and hospitable stimuli is crucial. Hum Brain Mapp, 2010. © 2009 Wiley‐Liss, Inc.     

Pain influences hedonic assessment of visual inputs

It is acknowledged that the emotional state created by visual inputs can modulate the way we feel pain; however, little is known about how acute pain influences the emotional assessment of what we see. In this study healthy subjects scored affective images while receiving painful or innocuous electrical shocks. Painful stimuli did not make unpleasant images more unpleasant, but rendered pleasant pictures significantly less pleasant. Brain responses to visual inputs (64-channels electroencephalogram) mirrored behavioural results, showing pain-induced effects in the orbitofrontal cortex, the subgenual portion of the cingulate gyrus, the anterior prefrontal and the temporal cortices, exclusively during presentation of pleasant images. In addition to this specific effect on pleasant pictures, pain also produced non-specific effects upon all categories of images, engaging cerebral areas associated with attention, alertness and motor preparation (middle-cingulate, supplemental motor, prefrontal cortex). Thus, pain appears to have a dual influence on visual processing: a non-specific effect related to orienting phenomena; and a more specific action exerted on supra-modal limbic areas involved in the production of affective states. The latter correlated with changes in the subjective appraisal of visual stimuli, and may underlie not only the change in their subjective assessment but also reactive processes aimed at coping with unpleasant contexts.     

Emotionally arousing stimuli compete for attention with left hemispace

Rapid interaction of the emotional and attentional networks is critical for adaptive behavior. Here, we examined the effects of emotional stimulation on hemifield attention allocation using event-related potential and behavioral measures. Participants performed a visual-discrimination task on nonemotional targets presented randomly in the left or right hemifield. A brief task-irrelevant emotional (pleasant or unpleasant; 150-ms duration) or neutral picture was presented centrally 350 ms before the next target (150-ms duration). Unpleasant stimuli interfered with the left visual field attention capacity, slowing behavioral responses to attended left field stimuli. In keeping with the behavioral data, event-related potential responses to nonemotional attended left field stimuli were reduced over the right parietal regions when preceded by an unpleasant event. The results provide electrophysiological and behavioral evidence that unpleasant, emotionally arousing stimuli interfere with the right hemisphere-dependent attention capacity.     

Does brain electrical activity react to music?

The electrical activity of the left and right central, temporal and parietal cortex was recorded in 14 amateurs of classical music during silence, pleasant (a piece of music) and unpleasant (a recording of an infant crying) stimulation. All the subjects rated the music as a pleasant stimulation and crying as an unpleasant one. Theta relative power was significantly higher while listening to music and lower during crying. Beta relative power did not change across conditions. No interhemispheric differences in the relative power were found. Interhemispheric correlation did not change either.     

Motivated attention to cocaine and emotional cues in abstinent and current cocaine users--an ERP study

Event-related potentials (ERPs) are a direct measure of neural activity and are ideally suited to study the time-course of attentional engagement with emotional and drug-related stimuli in addiction. In particular, the late positive potential (LPP) appears to be enhanced following cocaine-related compared with neutral stimuli in human participants with cocaine use disorders (CUD). However, previous studies have not directly compared cocaine-related with emotional stimuli while examining potential differences between abstinent and current cocaine users. The present study examined ERPs in 55 CUD (27 abstinent and 28 current users) and 29 matched healthy controls while they passively viewed pleasant, unpleasant, neutral and cocaine-related pictures. To examine the time-course of attention to these stimuli, we analysed both an early and later window in the LPP as well as the early posterior negativity (EPN), established in assessing motivated attention. Cocaine pictures elicited increased electrocortical measures of motivated attention in ways similar to affectively pleasant and unpleasant pictures in all CUD, an effect that was no longer discernible during the late LPP window for the current users. This group also exhibited deficient processing of the other emotional stimuli (early LPP window - pleasant pictures; late LPP window - pleasant and unpleasant pictures). Results were unique to the LPP and not EPN. Taken together, results support a relatively early attention bias to cocaine stimuli in cocaine-addicted individuals, further suggesting that recent cocaine use decreases such attention bias during later stages of processing but at the expense of deficient processing of other emotional stimuli.     

Correlation between extraversion and regional cerebral blood flow in response to olfactory stimuli

OBJECTIVE: Extraversion, a trait associated with individual differences in approach motivation and the experience of positive emotional states, is negatively correlated with certain psychiatric disorders, including depression and social phobia. The authors examined the correlation between extraversion and regional cerebral blood flow (rCBF) while participants were exposed to olfactory stimuli in order to further characterize individual differences in hedonic processing associated with this trait. METHOD: Twelve healthy participants were exposed to pleasant and unpleasant odors while rCBF was measured using [(15)O] water PET. The NEO Five-Factor Inventory was used to assess extraversion. Associations between extraversion scores and rCBF in each olfactory stimulus condition were assessed by correlational analysis. RESULTS: During the pleasant smell condition, extraversion was correlated with rCBF in the amygdala and occipital cortex. During the unpleasant smell condition, extraversion was correlated with rCBF in the occipital cortex and inferior temporal gyrus. CONCLUSIONS: These results provide important evidence for the biological basis of extraversion and indicate that there are systematic individual differences in patterns of brain activation in response to affective stimuli.     

Evidence of lateralized anteromedial temporal structures involvement in musical emotion processing

The right and left anteromedial temporal lobes have been shown to participate in emotion processing. The aim of the study was to further address their role in music emotion perception/recognition, and assessment by two emotional determinants, i.e., arousal (relaxing versus stimulating aspects) and valence (pleasantness degree). Epileptic patients with right or left anterior mesio-temporal resection (including the amygdala), and control subjects were presented with happy musical (chosen highly stimulating) or sad excerpts (chosen to be relaxing), that were either consonant (pleasant) or dissonant (unpleasant). The patients demonstrated an abnormal perception of dissonant music disregarding of the side of the resection; thereby confirming the role of the parahippocampal gyrus in the perception of unpleasantness. Moreover, the pleasantness of musical excerpts, in particular the happy consonant ones, was overestimated by patients with right temporal damage. In contrast, the arousal rating for happy consonant excerpts was reduced only in the group with left-resections. This modified perception of arousal might be related to the decreased ability of those patients to recognize happy and sad music. Indeed, both right and left temporal resections impaired sadness recognition, whereas happiness recognition was only reduced by the left-resections. The main result was that for the first time, the mesio-temporal structures were demonstrated to be asymmetrically involved in positive musical emotion recognition.     

Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task

Functional imaging studies consistently find that emotional stimuli activate the posterior cingulate cortex, a region that appears to have memory-related functions. However, prior imaging studies have not controlled for non-emotional stimulus features that might activate this region by engaging memory processes unrelated to emotion. This study examined whether emotional words activated the posterior cingulate cortex when these potentially confounding factors were controlled. Sixty-four pleasant and 64 unpleasant words were matched with neutral words on non-emotional features known to influence memory. Eight subjects underwent block-designed functional magnetic resonance imaging scans while evaluating the valence of these words. The posterior cingulate cortex was significantly activated bilaterally during both unpleasant and pleasant compared to neutral words. The strongest activation peak with both unpleasant and pleasant words was observed in the left subgenual cingulate cortex. Anteromedial orbital and left inferior and middle frontal cortices were also activated by both pleasant and unpleasant words. Right amygdala and auditory cortex were activated only by unpleasant words, while left frontal pole was activated only by pleasant words. The results show that activation of the posterior cingulate cortex by emotional stimuli cannot be attributed to the memory-enhancing effects of non-emotional stimulus features. The findings are consistent with the suggestion that this region may mediate interactions of emotional and memory-related processes. The results also extend prior findings that evaluating emotional words consistently activates the subgenual cingulate cortex, and suggest a means of probing this region in patients with mood disorders.     

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.