Neural Correlates Underlying Social-Cue-Induced Value Change.

As humans are social beings, human behavior and cognition are fundamentally shaped by information provided by peers, making human subjective value for rewards prone to be manipulated by perceived social information. Even subtle nonverbal social information, such as others' eye gazes, can influence value assignment, such as food value. In this study, we investigate the neural underpinnings of how gaze cues modify participants' food value (both genders) by means of functional magnetic resonance imaging. During the gaze-cuing task, food items were repeatedly presented either while others looked at them or while they were ignored by others. We determined participants' food values by assessing their willingness to pay before and after a standard gaze-cuing training. Results revealed that participants were willing to pay significantly more for food items that were attended to by others compared with the unattended to food items. Neural data showed that differences in subjective values between the two conditions were accompanied by enhanced activity in the inferior frontal gyrus, middle temporal gyrus, and caudate after food items were attended to. Furthermore, the functional connectivity between the caudate and the angular gyrus precisely predicted the individual differences in the preference shift. Our results unveil the key neural mechanism underlying the influence of social cues on the subjective value of food and highlight the crucial role of social context in shaping subjective value for food rewards in human.SIGNIFICANCE STATEMENT We investigated how social information like others' gaze toward foods affects individuals' food value. We found that individuals more often choose food items that were looked at by another person compared with food items that were ignored. Using neuroimaging, we showed that this increased value for attended to food items was associated with higher brain activity in the inferior frontal gyrus, middle temporal gyrus, and caudate. Furthermore, functional connectivity between the caudate and the angular gyrus was associated with individual differences in values for food items that were attended to by others versus being ignored. These findings provide novel insights into how the brain integrates social information into food value and could suggest possible interventions like using gaze cuing to promote healthier food choices.

Neural correlates of changing food choices while bypassing values.

Current theories suggest that altering choices requires value modification. To investigate this, normal-weight female participants' food choices and values were tested before and after an approach-avoidance training (AAT), while neural activity was recorded during the choice task using functional magnetic resonance imaging (fMRI). During AAT, participants consistently approached low- while avoiding high-calorie food cues. AAT facilitated low-calorie food choices, leaving food values unchanged. Instead, we observed a shift in indifference points, indicating the decreased contribution of food values in food choices. Training-induced choice shifts were associated with increased activity in the posterior cingulate cortex (PCC). In contrast, the medial PFC activity was not changed. Additionally, PCC gray matter density predicted individual differences in training-induced functional changes, suggesting anatomic predispositions to training impact. Our findings demonstrate neural mechanisms underlying choice modulation independent of valuation-related processes, which has substantial theoretical significance for decision-making frameworks and translational implications for health-related decisions resilient to value shifts.

Eating to dare - Nutrition impacts human risky decision and related brain function.

Macronutrient composition modulates plasma amino acids that are precursors of neurotransmitters and can impact brain function and decisions. Neurotransmitter serotonin has been shown to regulate not only food intake, but also economic decisions. We investigated whether an acute nutrition-manipulation inducing plasma tryptophan fluctuation affects brain function, thereby affecting risky decisions. Breakfasts differing in carbohydrate/protein ratios were offered to test changes in risky decision-making while metabolic and neural dynamics were tracked. We identified that a high-carbohydrate/protein breakfast increased plasma tryptophan/LNAA (large neutral amino acids) ratio which mapped to individual risk propensity changes. The nutrition-manipulation and tryptophan/LNAA fluctuation effects on risk propensity changes were further modulated by individual differences in body fat mass. Using fMRI, we further identified activation in the parietal lobule during risk-processing, of which activities 1) were sensitive to the tryptophan/LNAA fluctuation, 2) were modulated by individual's body fat mass, and 3) predicted the risk propensity changes in decision-making. Our results provide evidence for a personalized nutrition-driven modulation on human risky decision and its metabolic and neural mechanisms.

Altered intrinsic connectivity distribution in internet gaming disorder and its associations with psychotherapy treatment outcomes.

Alterations in brain connectivity have been implicated in internet gaming disorder (IGD). However, little is known about alterations in whole-brain connectivity and their associations with long-term treatment outcomes. Here, we used a relatively new analytic approach, intrinsic connectivity distribution (ICD) analysis, to examine brain connectivity in 74 IGD participants and 41 matched healthy controls (HCs) and conducted post hoc seed-based resting-state functional connectivity (rsFC) analyses based on the ICD findings. We also examined how these findings related to outcomes involving a craving behavioral intervention (CBI) for IGD. IGD participants showed less whole-brain connectivity in the left angular gyrus and ventromedial prefrontal cortex (vmPFC) compared with HC participants. Seed-based rsFC analyses revealed that the left angular gyrus in the IGD group showed less connectivity with areas involved in the default-mode network and greater connectivity with areas in the salience and executive control networks. CBI was associated with improved connectivity within regions in the default-mode network and regions across the default-mode and salience networks. ICD-identified connectivity differences in the left angular gyrus and vmPFC were related to changes in craving and severity of addiction 6 months after the intervention. The findings suggest that IGD is associated with alterations in brain connectivity that may be sensitive to interventions. Thus, the findings have implications for understanding mechanisms underlying CBI effects and for further treatment development.

Impact of nutrition on social decision making.

Food intake is essential for maintaining homeostasis, which is necessary for survival in all species. However, food intake also impacts multiple biochemical processes that influence our behavior. Here, we investigate the causal relationship between macronutrient composition, its bodily biochemical impact, and a modulation of human social decision making. Across two studies, we show that breakfasts with different macronutrient compositions modulated human social behavior. Breakfasts with a high-carbohydrate/protein ratio increased social punishment behavior in response to norm violations compared with that in response to a low carbohydrate/protein meal. We show that these macronutrient-induced behavioral changes in social decision making are causally related to a lowering of plasma tyrosine levels. The findings indicate that, in a limited sense, "we are what we eat" and provide a perspective on a nutrition-driven modulation of cognition. The findings have implications for education, economics, and public policy, and emphasize that the importance of a balanced diet may extend beyond the mere physical benefits of adequate nutrition.

Disentangling neural representations of value and salience in the human brain.

A large body of evidence has implicated the posterior parietal and orbitofrontal cortex in the processing of value. However, value correlates perfectly with salience when appetitive stimuli are investigated in isolation. Accordingly, considerable uncertainty has remained about the precise nature of the previously identified signals. In particular, recent evidence suggests that neurons in the primate parietal cortex signal salience instead of value. To investigate neural signatures of value and salience, here we apply multivariate (pattern-based) analyses to human functional MRI data acquired during a noninstrumental outcome-prediction task involving appetitive and aversive outcomes. Reaction time data indicated additive and independent effects of value and salience. Critically, we show that multivoxel ensemble activity in the posterior parietal cortex encodes predicted value and salience in superior and inferior compartments, respectively. These findings reinforce the earlier reports of parietal value signals and reconcile them with the recent salience report. Moreover, we find that multivoxel patterns in the orbitofrontal cortex correlate with value. Importantly, the patterns coding for the predicted value of appetitive and aversive outcomes are similar, indicating a common neural scale for appetite and aversive values in the orbitofrontal cortex. Thus orbitofrontal activity patterns satisfy a basic requirement for a neural value signal.

Effects of cognitive bias modification training on neural signatures of alcohol approach tendencies in male alcohol-dependent patients.

Alcohol-dependent patients have been shown to faster approach than avoid alcohol stimuli on the Approach Avoidance Task (AAT). This so-called alcohol approach bias has been associated with increased brain activation in the medial prefrontal cortex and nucleus accumbens. Cognitive bias modification (CBM) has been used to retrain the approach bias with the clinically relevant effect of decreasing relapse rates one year later. The effects of CBM on neural signatures of approach/avoidance tendencies remain hitherto unknown. In a double-blind placebo-controlled design, 26 alcohol-dependent in-patients were assigned to a CBM or a placebo training group. Both groups performed the AAT for three weeks: in CBM training, patients pushed away 90 percent of alcohol cues; this rate was 50 percent in placebo training. Before and after training, patients performed the AAT offline, and in a 3 T magnetic resonance imaging scanner. The relevant neuroimaging contrast for the alcohol approach bias was the difference between approaching versus avoiding alcohol cues relative to soft drink cues: [(alcohol pull > alcohol push) > (soft drink pull > soft drink push)]. Before training, both groups showed significant alcohol approach bias-related activation in the medial prefrontal cortex. After training, patients in the CBM group showed stronger reductions in medial prefrontal cortex activation compared with the placebo group. Moreover, these reductions correlated with reductions in approach bias scores in the CBM group only. This suggests that CBM affects neural mechanisms involved in the automatic alcohol approach bias, which may be important for the clinical effectiveness of CBM.

Adaptive coding of reward prediction errors is gated by striatal coupling.

To efficiently represent all of the possible rewards in the world, dopaminergic midbrain neurons dynamically adapt their coding range to the momentarily available rewards. Specifically, these neurons increase their activity for an outcome that is better than expected and decrease it for an outcome worse than expected, independent of the absolute reward magnitude. Although this adaptive coding is well documented, it remains unknown how this rescaling is implemented. To investigate the adaptive coding of prediction errors and its underlying rescaling process, we used human functional magnetic resonance imaging (fMRI) in combination with a reward prediction task that involved different reward magnitudes. We demonstrate that reward prediction errors in the human striatum are expressed according to an adaptive coding scheme. Strikingly, we show that adaptive coding is gated by changes in effective connectivity between the striatum and other reward-sensitive regions, namely the midbrain and the medial prefrontal cortex. Our results provide evidence that striatal prediction errors are normalized by a magnitude-dependent alteration in the interregional connectivity within the brain's reward system.

Neural integration of risk and effort costs by the frontal pole: only upon request.

Rewards in real life are rarely received without incurring costs and successful reward harvesting often involves weighing and minimizing different types of costs. In the natural environment, such costs often include the physical effort required to obtain rewards and potential risks attached to them. Costs may also include potential risks. In this study, we applied fMRI to explore the neural coding of physical effort costs as opposed to costs associated with risky rewards. Using an incentive-compatible valuation mechanism, we separately measured the subjective costs associated with effortful and risky options. As expected, subjective costs of options increased with both increasing effort and increasing risk. Despite the similar nature of behavioral discounting of effort and risk, distinct regions of the brain coded these two cost types separately, with anterior insula primarily processing risk costs and midcingulate and supplementary motor area (SMA) processing effort costs. To investigate integration of the two cost types, we also presented participants with options that combined effortful and risky elements. We found that the frontal pole integrates effort and risk costs through functional coupling with the SMA and insula. The degree to which the latter two regions influenced frontal pole activity correlated with participant-specific behavioral sensitivity to effort and risk costs. These data support the notion that, although physical effort costs may appear to be behaviorally similar to other types of costs, such as risk, they are treated separately at the neural level and are integrated only if there is a need to do so.

Loneliness is associated with more trust but worse trustworthiness expectations.

Subjective feelings of loneliness emerge due to unsatisfactory social relationships, representing a major risk for mental and physical well-being. Despite its social nature, evidence on how loneliness affects social behaviours and expectations is lacking. Using Bayesian analyses and economic games, we show in three different studies that lonelier individuals trusted their partners to a greater extent despite less favourable trustworthiness expectations, showing a greater discrepancy between their trusting behaviours and their expectations of others' trustworthiness. Such discrepancy was reversed in extravert individuals who also reported to be less lonely. These results provide evidence on two opposing effects of loneliness as a motivator for social connections and promoter of social withdrawal, and demonstrate the moderating role of personality traits. This work contributes to a better understanding of how loneliness impacts social behaviour and social expectations, with important downstream clinical implications for varying health conditions associated with heightened feelings of loneliness.

Weight loss impacts risky decisions in obesity.

BACKGROUND & AIMS: Risky decision making is shaped by individual psychological and metabolic state. Individuals with obesity show not only altered risk behavior, but also metabolic and psychological abnormalities. The aim of the present study was to investigate whether a substantial weight loss in individuals with severe obesity will 1) normalize their metabolic and psychological state and 2) will change their pattern of decision guidance. METHODS: We assessed the effect of glycated hemoglobin (HbA1c) and mood on risk behavior in individuals with obesity (n = 62, 41 women; BMI, 46.5 ± 4.8 kg/m2; age, 44.9 ± 14.7 years) before and after 10-weeks weight loss intervention. RESULTS: Results showed that this intervention reduced participants' risk behavior, which was significantly predicted by their changes in BMI. Before intervention, mood, but not HbA1c significantly predicted decisions. After the weight loss, mood no longer, but HbA1c significantly predicted decisions. CONCLUSION: Our findings shed light on the psychological and metabolic mechanisms underlying altered risky decision making in severe obesity and can inform the development of strategies in the context of weight loss interventions.

How glitter relates to gold: similarity-dependent reward prediction errors in the human striatum.

Optimal choices benefit from previous learning. However, it is not clear how previously learned stimuli influence behavior to novel but similar stimuli. One possibility is to generalize based on the similarity between learned and current stimuli. Here, we use neuroscientific methods and a novel computational model to inform the question of how stimulus generalization is implemented in the human brain. Behavioral responses during an intradimensional discrimination task showed similarity-dependent generalization. Moreover, a peak shift occurred, i.e., the peak of the behavioral generalization gradient was displaced from the rewarded conditioned stimulus in the direction away from the unrewarded conditioned stimulus. To account for the behavioral responses, we designed a similarity-based reinforcement learning model wherein prediction errors generalize across similar stimuli and update their value. We show that this model predicts a similarity-dependent neural generalization gradient in the striatum as well as changes in responding during extinction. Moreover, across subjects, the width of generalization was negatively correlated with functional connectivity between the striatum and the hippocampus. This result suggests that hippocampus-striatal connections contribute to stimulus-specific value updating by controlling the width of generalization. In summary, our results shed light onto the neurobiology of a fundamental, similarity-dependent learning principle that allows learning the value of stimuli that have never been encountered.

Positively biased processing of self-relevant social feedback.

Receiving social feedback such as praise or blame for one's character traits is a key component of everyday human interactions. It has been proposed that humans are positively biased when integrating social feedback into their self-concept. However, a mechanistic description of how humans process self-relevant feedback is lacking. Here, participants received feedback from peers after a real-life interaction. Participants processed feedback in a positively biased way, i.e., they changed their self-evaluations more toward desirable than toward undesirable feedback. Using functional magnetic resonance imaging we investigated two feedback components. First, the reward-related component correlated with activity in ventral striatum and in anterior cingulate cortex/medial prefrontal cortex (ACC/MPFC). Second, the comparison-related component correlated with activity in the mentalizing network, including the MPFC, the temporoparietal junction, the superior temporal sulcus, the temporal pole, and the inferior frontal gyrus. This comparison-related activity within the mentalizing system has a parsimonious interpretation, i.e., activity correlated with the differences between participants' own evaluation and feedback. Importantly, activity within the MPFC that integrated reward-related and comparison-related components predicted the self-related positive updating bias across participants offering a mechanistic account of positively biased feedback processing. Thus, theories on both reward and mentalizing are important for a better understanding of how social information is integrated into the human self-concept.

Connectivity-based parcellation of the human orbitofrontal cortex.

The primate orbitofrontal cortex (OFC) is involved in reward processing, learning, and decision making. Research in monkeys has shown that this region is densely connected with higher sensory, limbic, and subcortical regions. Moreover, a parcellation of the monkey OFC into two subdivisions has been suggested based on its intrinsic anatomical connections. However, in humans, little is known about any functional subdivisions of the OFC except for a rather coarse medial/lateral distinction. Here, we used resting-state fMRI in combination with unsupervised clustering techniques to investigate whether OFC subdivisions can be revealed based on their functional connectivity profiles with other brain regions. Examination of different cluster solutions provided support for a parcellation into two parts as observed in monkeys, but it also highlighted a much finer hierarchical clustering of the orbital surface. Specifically, we identified (1) a medial, (2) a posterior-central, (3) a central, and (4-6) three lateral clusters spanning the anterior-posterior gradient. Consistent with animal tracing studies, these OFC clusters were connected to other cortical regions such as prefrontal, temporal, and parietal cortices but also subcortical areas in the striatum and the midbrain. These connectivity patterns provide important implications for identifying specific functional roles of OFC subdivisions for reward processing, learning, and decision making. Moreover, this parcellation schema can provide guidance to report results in future studies.

Value of freedom to choose encoded by the human brain.

Humans and animals value the opportunity to choose by preferring alternatives that offer more rather than fewer choices. This preference for choice may arise not only from an increased probability of obtaining preferred outcomes but also from the freedom it provides. We used human neuroimaging to investigate the neural basis of the preference for choice as well as for the items that could be chosen. In each trial, participants chose between two options, a monetary amount option and a "choice option." The latter consisted of a number that corresponded to the number of everyday items participants would subsequently be able to choose from. We found that the opportunity to choose from a larger number of items was equivalent to greater amounts of money, indicating that participants valued having more choice; moreover, participants varied in the degree to which they valued having the opportunity to choose, with some valuing it more than the increased probability of obtaining preferred items. Neural activations in the mid striatum increased with the value of the opportunity to choose. The same region also coded the value of the items. Conversely, activation in the dorsolateral striatum was not related to the value of the items but was elevated when participants were offered more choices, particularly in those participants who overvalued the opportunity to choose. These data suggest a functional dissociation of value representations within the striatum, with general representations in mid striatum and specific representations of the value of freedom provided by the opportunity to choose in dorsolateral striatum.

The neural code of reward anticipation in human orbitofrontal cortex.

An optimal choice among alternative behavioral options requires precise anticipatory representations of their possible outcomes. A fundamental question is how such anticipated outcomes are represented in the brain. Reward coding at the level of single cells in the orbitofrontal cortex (OFC) follows a more heterogeneous coding scheme than suggested by studies using functional MRI (fMRI) in humans. Using a combination of multivariate pattern classification and fMRI we show that the reward value of sensory cues can be decoded from distributed fMRI patterns in the OFC. This distributed representation is compatible with previous reports from animal electrophysiology that show that reward is encoded by different neural populations with opposing coding schemes. Importantly, the fMRI patterns representing specific values during anticipation are similar to those that emerge during the receipt of reward. Furthermore, we show that the degree of this coding similarity is related to subjects' ability to use value information to guide behavior. These findings narrow the gap between reward coding in humans and animals and corroborate the notion that value representations in OFC are independent of whether reward is anticipated or actually received.

Soyoung Q. Park.

Soyoung Q. Park combines cognitive neuroscience and metabolism research. Sharing her enthusiasm for using a holistic and transcultural approach, she discusses with Neuron how understanding multiple perspectives surrounding a scientific question and the various methods that can be applied to answering it supports the study of complex research topics, benefiting academia and society.

Potential mechanisms and modulators of food intake during pregnancy.

Dietary choice during pregnancy is crucial not only for fetal development, but also for long-term health outcomes of both mother and child. During pregnancy, dramatic changes in endocrine, cognitive, and reward systems have been shown to take place. Interestingly, in different contexts, many of these mechanisms play a key role in guiding food intake. Here, we review how food intake may be impacted as a function of pregnancy-induced changes across species. We first summarize changes in endocrine and metabolic signaling in the course of pregnancy. Then, we show how these may be related to cognitive function and reward processing in humans. Finally, we link these to potential drivers of change in eating behavior throughout the course of pregnancy.

Neurocomputational mechanisms of biased impression formation in lonely individuals.

Social impressions are fundamental in our daily interactions with other people but forming accurate impressions of our social partners can be biased to different extents. Loneliness has previously been suggested to induce biases that hinder the formation of accurate impressions of others for successful social bonding. Here, we demonstrated that despite counterfactual evidence, negative first impressions bias information weighting, leading to less favorable trustworthiness beliefs. Lonely individuals did not only have more negative expectations of others' social behavior, but they also manifested a stronger weighting bias. Reduced orbitofrontal cortex (OFC) activity was associated with a stronger weighting bias in lonelier individuals and mediated the relationship between loneliness and this weighting bias. Importantly, stronger coupling between OFC and temporoparietal junction compensated for such effects, promoting more positive trustworthiness beliefs especially in lonelier individuals. These findings bear potential for future basic and clinical investigations on social cognition and the development of clinical symptoms linked to loneliness.