Neural correlates of affective influence on choice

The Journal of …, 2011

Self-control is a key aspect of adaptive decision-making. Self-control allows us to pursue a deliberate, long-term goal (for instance, to be healthy) by overcoming more automatic and immediate stimulus-response tendencies that conflict with that goal (to eat a sugary snack). Conversely, impaired self-control in decision-making has been linked to addiction and obesity (for review, see , highlighting the enormous impact of this issue on public health as well as the importance of research on the neurobiological mechanisms of selfcontrol in decision-making.

Behavioral and Brain Functions, 2008

Background: In most studies on human reward processing, reward intensity has been manipulated on an objective scale (e.g., varying monetary value). Everyday experience, however, teaches us that objectively equivalent rewards may differ substantially in their subjective incentive values. One factor influencing incentive value in humans is branding. The current study explores the hypothesis that individual brand preferences modulate activity in reward areas similarly to objectively measurable differences in reward intensity. Methods: A wheel-of-fortune game comprising an anticipation phase and a subsequent outcome evaluation phase was implemented. Inside a 3 Tesla MRI scanner, 19 participants played for chocolate bars of three different brands that differed in subjective attractiveness. Results: Parametrical analysis of the obtained fMRI data demonstrated that the level of activity in anatomically distinct neural networks was linearly associated with the subjective preference hierarchy of the brands played for. During the anticipation phases, preference-dependent neural activity has been registered in premotor areas, insular cortex, orbitofrontal cortex, and in the midbrain. During the outcome phases, neural activity in the caudate nucleus, precuneus, lingual gyrus, cerebellum, and in the pallidum was influenced by individual preference. Conclusion: Our results suggest a graded effect of differently preferred brands onto the incentive value of objectively equivalent rewards. Regarding the anticipation phase, the results reflect an intensified state of wanting that facilitates action preparation when the participants play for their favorite brand. This mechanism may underlie approach behavior in real-life choice situations.

Journal of Neuroscience, 2011

The ability of human subjects to choose between disparate kinds of rewards suggests that the neural circuits for valuing different reward types must converge. Economic theory suggests that these convergence points represent the subjective values (SVs) of different reward types on a common scale for comparison. To examine these hypotheses and to map the neural circuits for reward valuation we had food and water-deprived subjects make risky choices for money, food, and water both in and out of a brain scanner. We found that risk preferences across reward types were highly correlated; the level of risk aversion an individual showed when choosing among monetary lotteries predicted their risk aversion toward food and water. We also found that partially distinct neural networks represent the SVs of monetary and food rewards and that these distinct networks showed specific convergence points. The hypothalamic region mainly represented the SV for food, and the posterior cingulate cortex mainly represented the SV for money. In both the ventromedial prefrontal cortex (vmPFC) and striatum there was a common area representing the SV of both reward types, but only the vmPFC significantly represented the SVs of money and food on a common scale appropriate for choice in our data set. A correlation analysis demonstrated interactions across money and food valuation areas and the common areas in the vmPFC and striatum. This may suggest that partially distinct valuation networks for different reward types converge on a unified valuation network, which enables a direct comparison between different reward types and hence guides valuation and choice.

Neuropsychologia, 2004

We examined neural activations during decision-making using fMRI paired with the wheel of fortune task, a newly developed two-choice decision-making task with probabilistic monetary gains. In particular, we assessed the impact of high-reward/risk events relative to low-reward/risk events on neural activations during choice selection and during reward anticipation. Seventeen healthy adults completed the study. We found, in line with predictions, that (i) the selection phase predominantly recruited regions involved in visuo-spatial attention (occipito-parietal pathway), conflict (anterior cingulate), manipulation of quantities (parietal cortex), and preparation for action (premotor area), whereas the anticipation phase prominently recruited regions engaged in reward processes (ventral striatum); and (ii) high-reward/risk conditions relative to low-reward/risk conditions were associated with a greater neural response in ventral striatum during selection, though not during anticipation. Following an a priori ROI analysis focused on orbitofrontal cortex, we observed orbitofrontal cortex activation (BA 11 and 47) during selection (particularly to high-risk/reward options), and to a more limited degree, during anticipation. These findings support the notion that (1) distinct, although overlapping, pathways subserve the processes of selection and anticipation in a two-choice task of probabilistic monetary reward; (2) taking a risk and awaiting the consequence of a risky decision seem to affect neural activity differently in selection and anticipation; and thus (3) common structures, including the ventral striatum, are modulated differently by risk/reward during selection and anticipation. Published by Elsevier Ltd.

Journal of Cognitive Neuroscience

Craving of unhealthy food is a common target of self-regulation, but the neural systems underlying this process are understudied. In the present study, participants used cognitive reappraisal to regulate their desire to consume idiosyncratically craved or not craved energy- dense foods, and neural activity during regulation was compared to each other and to activity during passive viewing of energy-dense foods. Regulation of both food types elicited activation in classic top-down self-regulation regions including the dorsolateral prefrontal, inferior frontal, and dorsal anterior cingulate cortices. This main effect of regulation was qualified by an interaction such that activation in these regions was significantly greater during reappraisal of craved (versus not craved) foods, and several regions, including the dorsolateral prefrontal, inferior frontal, medial frontal, and dorsal anterior cingulate cortices, were uniquely active during regulation of personally-craved foods. Body mass index significantly negatively correlated with regulation-related activation in the right dorsolateral prefrontal cortex, thalamus, and bilateral dorsal anterior cingulate cortex, and with activity in nucleus accumbens during passive viewing of craved (versus neutral, low energy density) foods. These results suggest that several of the brain regions involved in the self-regulation of food craving are similar to other kinds of affective self-regulation, and that others are sensitive to the self-relevance of the regulation target.

PLOS ONE, 2016

Taking into account how people value the healthiness and tastiness of food at both the behavioral and brain levels may help to better understand and address overweight and obesity-related issues. Here, we investigate whether brain activity in those areas involved in self-control may increase significantly when individuals with a high body-mass index (BMI) focus their attention on the taste rather than on the health benefits related to healthy food choices. Under such conditions, BMI is positively correlated with both the neural responses to healthy food choices in those brain areas associated with gustation (insula), reward value (orbitofrontal cortex), and self-control (inferior frontal gyrus), and with the percent of healthy food choices. By contrast, when attention is directed towards health benefits, BMI is negatively correlated with neural activity in gustatory and reward-related brain areas (insula, inferior frontal operculum). Taken together, these findings suggest that those individuals with a high BMI do not necessarily have reduced capacities for self-control but that they may be facilitated by external cues that direct their attention toward the tastiness of healthy food. Thus, promoting the taste of healthy food in communication campaigns and/or food packaging may lead to more successful self-control and healthy food behaviors for consumers with a higher BMI, an issue which needs to be further researched.

Current Opinion in Clinical Nutrition & Metabolic Care, 2018

Purpose of review The dominant view in the literature is that increased neural reactivity to high-caloric palatable foods in the mesocorticolimbic system is a stable-specific characteristic of obese people. In this review, we argue that this viewpoint may not be justified, and we propose that the neural response to food stimuli is dynamic, and in synchrony with the current motivational and cognitive state of an individual. We will further motivate why a clear mental task in the scanner is a necessity for drawing conclusions from neural activity, and why multivariate approaches to functional MRI (fMRI) data-analysis may carry the field forward. Recent findings From the reviewed literature we draw the conclusions that: neural food-cue reactivity depends strongly on cognitive factors such as the use of cognitive regulation strategies, task demands, and focus of attention; neural activity in the mesocorticolimbic system is not proportionate to the hedonic value of presented food stimuli; and multivariate approaches to fMRI data-analysis have shown that hedonic value can be decoded from multivoxel patterns of neural activity. Summary Future research should take the dynamic nature of food-reward processing into account and take advantage from state-of-the-art multivariate approaches to fMRI data-analysis.

Journal of Cognitive Neuroscience, 2014

Craving of unhealthy food is a common target of self-regulation, but the neural systems underlying this process are understudied. In the present study, participants used cognitive reappraisal to regulate their desire to consume idiosyncratically craved or not craved energydense foods, and neural activity during regulation was compared to each other and to activity during passive viewing of energy-dense foods. Regulation of both food types elicited activation in classic top-down self-regulation regions including the dorsolateral prefrontal, inferior frontal, and dorsal anterior cingulate cortices. This main effect of regulation was qualified by an interaction such that activation in these regions was significantly greater during reappraisal of craved (versus not craved) foods, and several regions, including the dorsolateral prefrontal, inferior frontal, medial frontal, and dorsal anterior cingulate cortices, were uniquely active during regulation of personally-craved foods. Body mass index significantly negatively correlated with regulation-related activation in the right dorsolateral prefrontal cortex, thalamus, and bilateral dorsal anterior cingulate cortex, and with activity in nucleus accumbens during passive viewing of craved (versus neutral, low energy density) foods. These results suggest that several of the brain regions involved in the self-regulation of food craving are similar to other kinds of affective self-regulation, and that others are sensitive to the self-relevance of the regulation target.

International journal of obesity (2005), 2012

Objective:In this study, we investigate the brain mechanisms of the conscious regulation of the desire for food using functional magnetic resonance imaging. Further, we examine associations between hemodynamic responses and participants' cognitive restraint of eating (CRE), as well as their susceptibility to uncontrolled eating.Subjects:Seventeen non-vegetarian, right-handed, female Caucasian participants (age: 20-30 years, mean 25.3 years±3.1 s.d.; BMI: 20.2-31.2 kg m(-2), mean 25.1±3.5 s.d.).Measurements:During scanning, our participants viewed pictures of food items they had pre-rated according to tastiness and healthiness. Participants were either allowed to admit to the desire for the food (ADMIT) or they were instructed to downregulate their desire using a cognitive reappraisal strategy, that is, thinking of negative long-term health-related and social consequences (REGULATE).Results:Comparing the hemodynamic responses of the REGULATE with the ADMIT condition, we observed...

2014

Food advertisements often promote choices that are driven by inferences about the hedonic pleasures of eating a particular food. Given the individual and public health consequences of obesity, it is critical to address unanswered questions about the specific neural systems underlying these hedonic inferences. For example, although regions such as the orbitofrontal cortex (OFC) are frequently observed to respond more to pleasant food images than less hedonically pleasing stimuli, one important hedonic brain region in particular has largely remained conspicuously absent among human studies of hedonic response to food images. Based on rodent research demonstrating that activity in the ventral pallidum underlies the hedonic pleasures experienced upon eating food rewards, one might expect that activity in this important 'hedonic hotspot' might also track inferred food pleasantness. To date, however, no human studies have assessed this question. We thus asked human subjects to undergo fMRI and make item-by-item ratings of how pleasant it would be to eat particular visually perceived foods. Activity in the ventral pallidum was strongly modulated with pleasantness inferences. Additionally, activity within a region of the orbitofrontal cortex that tracks the pleasantness of tastes was also modulated with inferred pleasantness. Importantly, the reliability of these findings is demonstrated by their replication when we repeated the experiment at a new site with new subjects. These two experiments demonstrate that the ventral pallidum, in addition to the OFC, plays a central role in the moment-to-moment hedonic inferences that influence food-related decision-making.

2010

Tracking the hemodynamic responses to reward and punishment in the striatum. J Neurophysiol 84: 3072-3077, 2000. Research suggests that the basal ganglia complex is a major component of the neural circuitry that mediates reward-related processing. However, human studies have not yet characterized the response of the basal ganglia to an isolated reward, as has been done in animals. We developed an event-related functional magnetic resonance imaging paradigm to identify brain areas that are activated after presentation of a reward. Subjects guessed whether the value of a card was higher or lower than the number 5, with monetary rewards as an incentive for correct guesses. They received reward, punishment, or neutral feedback on different trials. Regions in the dorsal and ventral striatum were activated by the paradigm, showing differential responses to reward and punishment. Activation was sustained following a reward feedback, but decreased below baseline following a punishment feedback.

Sunk' or unrecoverable costs impact proximal reward-based decisions across species. However, it is not known if these incurred costs elicit a long-lasting change in reward value. To address this, we identified the relative preference between different flavored food pellets in rats. Animals were then trained to experience the initially preferred reward after short delays and the initially less preferred reward after long delays. This training regimen enhanced the preference for the initially less desirable food reward. We probed whether this change in subjective preference involved dopamine signaling or the orbital frontal cortex (OFC) given that these neural systems contribute to reward valuation. Systemic dopamine receptor antagonism attenuated anticipatory responding during training sessions but did not prevent the change in reward preference elicited by incurred temporal costs. OFC lesions had no effect on anticipatory responding during training or on the change in reward preference. These findings collectively illustrate that the neural systems involved with economic assessments of reward value are not contributing to changes in subjective preference.

European Journal of Neuroscience, 2008

Representing the affective value of a reward on a continuous scale may occur separately from making a binary, for example yes vs no, decision about whether to choose the reward. To investigate whether these are separable processes, we used functional magnetic resonance imaging to measure activations produced by pleasant warm, unpleasant cold, and affectively complex combinations of these stimuli applied to the hand. On some trials the affective value was rated on a continuous scale, and on different trials a yes-no decision was made about whether the stimulus should be repeated in future. Decision-making contrasted with just rating the affective stimuli revealed activations in the medial prefrontal cortex area 10, implicating this area in binary decision-making. Activations related to the pleasantness ratings and which were not influenced when a binary decision was made were found in the pregenual cingulate and parts of the orbitofrontal cortex, implicating these regions in the continuous representation of affective value. When a decision was yes vs. no, effects were found in the dorsal cingulate cortex, agranular (anterior) insula and ventral tegmental area, implicating these areas in initiating actions to obtain goals.

European Journal of Neuroscience, 2004

The motivation to eat in humans is a complex process influenced by intrinsic mechanisms relating to the hunger and satiety cascade, and extrinsic mechanisms based on the appetitive incentive value of individual foods, which can themselves induce desire. This study was designed to investigate the neural basis of these two factors contributing to the control of motivation to eat within the same experimental design using positron emission tomography. Using a novel counterbalanced approach, participants were scanned in two separate sessions, once after fasting and once after food intake, in which they imagined themselves in a restaurant and considered a number of items on a menu, and were asked to choose their most preferred. All items were tailored to each individual and varied in their incentive value. No actual foods were presented. In response to a hungry state, increased activation was shown in the hypothalamus, amygdala and insula cortex as predicted, as well as the medulla, striatum and anterior cingulate cortex. Satiety, in contrast, was associated with increased activation in the lateral orbitofrontal and temporal cortex. Only activity in the vicinity of the amygdala and orbitofrontal cortex was observed in response to the processing of extrinsic appetitive incentive information. These results suggest that the contributions of intrinsic homeostatic influences, and extrinsic incentive factors to the motivation to eat, are somewhat dissociable neurally, with areas of convergence in the amygdala and orbitofrontal cortex. The findings of this study have implications for research into the underlying mechanisms of eating disorders.

Cognitive Neuroscience, 2012

Most neuropsychological research using food as a reward uses single-bid auctions. We wished to determine whether focal brain lesions would affect the ability and motivation to win snack food items in a computerized auction allowing multiple bids. This allowed us to assess participants' abilities under more complex conditions. We enrolled 154 male penetrating traumatic brain injury (pTBI) veterans, mean age 58, from the Vietnam Head Injury Study registry, and 53 male uninjured veterans, mean age 59. We used voxel-based lesion symptom mapping (VLSM) to identify effects of brain lesions on the ability to win items and on participants' answers to statements regarding their level of motivation and evaluation of how well they performed. Number of items won was not significantly associated with any lesions; however, lesions in gustatory cortex (GC) affected motivation and self-evaluation. Our findings provide further evidence of the primary GC's role in motivation for food and drink.