Morten L. Kringelbach

The human orbitofrontal cortex : Linking reward to hedonic experience

Hedonic experience is arguably at the heart of what makes us human. In recent neuroimaging studies of the cortical networks that mediate hedonic experience in the human brain, the orbitofrontal cortex has emerged as the strongest candidate for linking food and other types of reward to hedonic experience. The orbitofrontal cortex is among the least understood regions of the human brain, but has been proposed to be involved in sensory integration, in representing the affective value of reinforcers, and in decision making and expectation. Here, the functional neuroanatomy of the human orbitofrontal cortex is described and a new integrated model of its functions proposed, including a possible role in the mediation of hedonic experience.

Affective neuroscience of pleasure: reward in humans and animals

IntroductionPleasure and reward are generated by brain circuits that are largely shared between humans and other animals.DiscussionHere, we survey some fundamental topics regarding pleasure mechanisms and explicitly compare humans and animals.ConclusionTopics surveyed include liking, wanting, and learning components of reward; brain coding versus brain causing of reward; subjective pleasure versus objective hedonic reactions; roles of orbitofrontal cortex and related cortex regions; subcortical hedonic hotspots for pleasure generation; reappraisals of dopamine and pleasure-electrode controversies; and the relation of pleasure to happiness.

Translational principles of deep brain stimulation

Deep brain stimulation (DBS) has shown remarkable therapeutic benefits for patients with otherwise treatment-resistant movement and affective disorders. This technique is not only clinically useful, but it can also provide new insights into fundamental brain functions through direct manipulation of both local and distributed brain networks in many different species. In particular, DBS can be used in conjunction with non-invasive neuroimaging methods such as magnetoencephalography to map the fundamental mechanisms of normal and abnormal oscillatory synchronization that underlie human brain function. The precise mechanisms of action for DBS remain uncertain, but here we give an up-to-date overview of the principles of DBS, its neural mechanisms and its potential future applications.

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.

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.

Pleasure Systems in the Brain

Pleasure is mediated by well-developed mesocorticolimbic circuitry and serves adaptive functions. In affective disorders, anhedonia (lack of pleasure) or dysphoria (negative affect) can result from breakdowns of that hedonic system. Human neuroimaging studies indicate that surprisingly similar circuitry is activated by quite diverse pleasures, suggesting a common neural currency shared by all. Wanting for reward is generated by a large and distributed brain system. Liking, or pleasure itself, is generated by a smaller set of hedonic hot spots within limbic circuitry. Those hot spots also can be embedded in broader anatomical patterns of valence organization, such as in a keyboard pattern of nucleus accumbens generators for desire versus dread. In contrast, some of the best known textbook candidates for pleasure generators, including classic pleasure electrodes and the mesolimbic dopamine system, may not generate pleasure after all. These emerging insights into brain pleasure mechanisms may eventually facilitate better treatments for affective disorders.

Towards a functional neuroanatomy of pleasure and happiness

The pursuit of happiness is a preoccupation for many people. Yet only the pursuit can be promised, not happiness itself. Can science help? We focus on the most tractable ingredient, hedonia or positive affect. A step toward happiness might be gained by improving the pleasures and positive moods in daily life. The neuroscience of pleasure and reward provides relevant insights, and we discuss how specific hedonic mechanisms might relate to happiness or the lack thereof. Although the neuroscience of happiness is still in its infancy, further advances might be made through mapping overlap between brain networks of hedonic pleasure with others, such as the brains default network, potentially involved in the other happiness ingredient, eudaimonia or life meaning and engagement.

Neural correlates of rapid reversal learning in a simple model of human social interaction.

Humans and other primates spend much of their time engaged in social interactions where a crucial ability is to decode face expressions and act accordingly. This rapid reversal learning has been proposed to be important in the relative evolutionary success of primates. Here we provide the first neuroimaging evidence that the ability to change behaviour based on face expression in a model of social interactions is not reflected in the activity in the fusiform face area, but is specifically correlated with activity in the orbitofrontal and anterior cingulate/paracingulate cortices. These brain regions are particularly involved in reversal learning, such that the activations described occurred specifically at the time of reversal, and were also found when different face expressions other than angry were used to cue reversal. The evidence that the orbitofrontal and anterior cingulate/paracingulate cortices are specifically activated at the time of reversal is important for understanding changes in affect and emotional processing in patients with lesions to these brain regions.

FOOD FOR THOUGHT: HEDONIC EXPERIENCE BEYOND HOMEOSTASIS IN THE HUMAN BRAIN

Food intake is an essential human activity regulated by homeostatic and hedonic systems in the brain which has mostly been ignored by the cognitive neurosciences. Yet, the study of food intake integrates fundamental cognitive and emotional processes in the human brain, and can in particular provide evidence on the neural correlates of the hedonic experience central to guiding behaviour. Neuroimaging experiments provide a novel basis for the further exploration of the brain systems involved in the conscious experience of pleasure and reward, and thus provide a unique method for studying the hedonic quality of human experience. Recent neuroimaging experiments have identified some of the regions involved in the cortical networks mediating hedonic experience in the human brain, with the evidence suggesting that the orbitofrontal cortex is the perhaps strongest candidate for linking food and other kinds of reward to hedonic experience. Based on the reviewed literature, a model is proposed to account for the roles of the different parts of the orbitofrontal cortex in this hedonic network.

A specific and rapid neural signature for parental instinct.

Darwin originally pointed out that there is something about infants which prompts adults to respond to and care for them, in order to increase individual fitness, i.e. reproductive success, via increased survivorship of ones own offspring. Lorenz proposed that it is the specific structure of the infant face that serves to elicit these parental responses, but the biological basis for this remains elusive. Here, we investigated whether adults show specific brain responses to unfamiliar infant faces compared to adult faces, where the infant and adult faces had been carefully matched across the two groups for emotional valence and arousal, as well as size and luminosity. The faces also matched closely in terms of attractiveness. Using magnetoencephalography (MEG) in adults, we found that highly specific brain activity occurred within a seventh of a second in response to unfamiliar infant faces but not to adult faces. This activity occurred in the medial orbitofrontal cortex (mOFC), an area implicated in reward behaviour, suggesting for the first time a neural basis for this vital evolutionary process. We found a peak in activity first in mOFC and then in the right fusiform face area (FFA). In mOFC the first significant peak (p<0.001) in differences in power between infant and adult faces was found at around 130 ms in the 10–15 Hz band. These early differences were not found in the FFA. In contrast, differences in power were found later, at around 165 ms, in a different band (20–25 Hz) in the right FFA, suggesting a feedback effect from mOFC. These findings provide evidence in humans of a potential brain basis for the “innate releasing mechanisms” described by Lorenz for affection and nurturing of young infants. This has potentially important clinical applications in relation to postnatal depression, and could provide opportunities for early identification of families at risk.