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Elevated energy intake is correlated with hyperresponsivity in attentional, gustatory, and reward brain regions while anticipating palatable food receipt.

ABSTRACT: Obese compared with lean individuals show greater attention-, gustatory-, and reward-region responsivity to food cues but reduced reward-region responsivity during food intake. However, to our knowledge, research has not tested whether an objectively measured caloric intake is positively associated with neural responsivity independent of excess adipose tissue.We tested the hypothesis that objectively measured energy intake, which accounts for basal needs and the percentage of body fat, correlates positively with the neural response to anticipated palatable food intake but negatively with a response to food intake in healthy-weight adolescents.Participants (n = 155; mean ± SD age: 15.9 ± 1.1 y) completed functional magnetic resonance imaging scans while anticipating and receiving palatable food compared with a tasteless solution, a doubly labeled water assessment of energy intake, and assessments of resting metabolic rate and body composition.Energy intake correlated positively with activation in the lateral visual and anterior cingulate cortices (visual processing and attention), frontal operculum (primary gustatory cortex) when anticipating palatable food, and greater striatal activation when anticipating palatable food in a more-sensitive region of interest analysis. Energy intake was not significantly related to neural responsivity during palatable food intake.Results indicate that objectively measured energy intake that accounts for basal needs and adipose tissue correlates positively with activity in attentional, gustatory, and reward regions when anticipating palatable food. Although hyperresponsivity of these regions may increase risk of overeating, it is unclear whether this is an initial vulnerability factor or a result of previous overeating. This trial was registered at clinicaltrials.gov as NCT01807572.

SUBMITTER: Burger KS

PROVIDER: S-EPMC3652919 | biostudies-literature | 2013 Jun

REPOSITORIES: biostudies-literature

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Elevated energy intake is correlated with hyperresponsivity in attentional, gustatory, and reward brain regions while anticipating palatable food receipt.

Burger Kyle S KS Stice Eric E

The American journal of clinical nutrition 20130417 6

<h4>Background</h4>Obese compared with lean individuals show greater attention-, gustatory-, and reward-region responsivity to food cues but reduced reward-region responsivity during food intake. However, to our knowledge, research has not tested whether an objectively measured caloric intake is positively associated with neural responsivity independent of excess adipose tissue.<h4>Objective</h4>We tested the hypothesis that objectively measured energy intake, which accounts for basal needs and ...[more]

PMID: 23595877

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Project description:Background: Both an elevated brain-reward-region response to palatable food and elevated weight variability have been shown to predict future weight gain.Objective: We examined whether the brain-reward response to food is related to future weight variability.Design: A total of 162 healthy-weight adolescents, who were aged 14-18 y at baseline, were enrolled in the study and were assessed annually over a 3-y follow-up period with 127 participants completing the final 3-y follow-up assessment. With the use of functional magnetic resonance imaging, we tested whether the neural responses to a cue that signaled an impending milkshake receipt and the receipt of the milkshake predicted weight variability over the follow-up period. Weight variability was modeled with a root mean squared error method to reflect fluctuations in weight independent of the net weight change.Results: Elevated activation in the medial prefrontal cortex and supplementary motor area, cingulate gyrus, cuneus and occipital gyrus, and insula in response to milkshake receipt predicted greater weight variability. Greater activation in the precuneus and middle temporal gyrus predicted lower weight variability.Conclusions: From our study data, we suggest that the elevated activation of reward and emotional-regulation brain regions (medial prefrontal cortex, cingulate cortex, and insula) and lower activation in self-reference regions (precuneus) in response to milkshake receipt predict weight variability over 3 y of follow-up. The fact that the reward response in the current study emerged in response to high-calorie palatable food receipt suggests that weight variability may be a measure of propensity periods of a positive energy balance and should be examined in addition to measures of the net weight change. With our collective results, we suggest that weight variability and its brain correlates should be added to other variables that are predictive of weight gain to inform the design of obesity-preventive programs in adolescents. This trial was registered at clinicaltrials.gov as NCT01807572.

Project description:Background/objectivesDysfunction in reward-related aspects of feeding, and consequent overeating in humans, is a major contributor to obesity. Intrauterine undernutrition and overnutrition are among the predisposing factors, but the exact mechanism of how overeating develops is still unclear. Consummatory behavior is regulated by the medial shell (mSh) of the accumbens nucleus (Nac) through direct connections with the rostral part of the lateral hypothalamic area (LHA). Our aim was to investigate whether an altered Nac-LHA circuit may underlie hyperphagic behavior.Subjects/methodsIntrauterine protein-restricted (PR) male Wistar rats were used as models for hyperphagia. The experiments were performed using young adult control (normally nourished) and PR animals. Sweet condensed milk (SCM) served as a reward to test consumption and subsequent activation (Fos+) of Nac and LHA neurons. Expression levels of type 1 and 2 dopamine receptors (D1R, D2R) in the Nac, as well as tyrosine hydroxylase (TH) levels in the ventral tegmental area, were determined. The D1R agonist SKF82958 was injected into the mSh-Nac of control rats to test the effect of D1R signaling on SCM intake and neuronal cell activation in the LHA.ResultsA group of food reward-representing D1R+ neurons was identified in the mSh-Nac. Activation (Fos+) of these neurons was highly proportional to the consumed palatable food. D1R agonist treatment attenuated SCM intake and diminished the number of SCM-activated cells in the LHA. Hyperphagic PR rats showed increased intake of SCM, reduced D1R expression, and an impaired response to SCM-evoked neuronal activation in the mSh-Nac, accompanied by an elevated number of Fos+ neurons in the LHA compared to controls.ConclusionsSensitivity of food reward-representing neurons in the mSh-Nac determines the level of satisfaction that governs cessation of consumption, probably through connections with the LHA. D1R signaling is a key element in this function, and is impaired in obesity-prone rats.

Project description:Reward processing abnormalities have been implicated in the pathophysiology of negative symptoms such as anhedonia and avolition in schizophrenia. However, studies examining neural responses to reward anticipation and receipt have largely relied on instrumental tasks, which may confound reward processing abnormalities with deficits in response selection and execution. 25 chronic, medicated outpatients with schizophrenia and 20 healthy controls underwent functional magnetic resonance imaging using a pavlovian reward prediction paradigm with no response requirements. Subjects passively viewed cues that predicted subsequent receipt of monetary reward or non-reward, and blood-oxygen-level-dependent signal was measured at the time of cue presentation and receipt. At the group level, neural responses to both reward anticipation and receipt were largely similar between groups. At the time of cue presentation, striatal anticipatory responses did not differ between patients and controls. Right anterior insula demonstrated greater activation for nonreward than reward cues in controls, and for reward than nonreward cues in patients. At the time of receipt, robust responses to receipt of reward vs. nonreward were seen in striatum, midbrain, and frontal cortex in both groups. Furthermore, both groups demonstrated responses to unexpected versus expected outcomes in cortical areas including bilateral dorsolateral prefrontal cortex. Individual difference analyses in patients revealed an association between physical anhedonia and activity in ventral striatum and ventromedial prefrontal cortex during anticipation of reward, in which greater anhedonia severity was associated with reduced activation to money versus no-money cues. In ventromedial prefrontal cortex, this relationship held among both controls and patients, suggesting a relationship between anticipatory activity and anhedonia irrespective of diagnosis. These findings suggest that in the absence of response requirements, brain responses to reward receipt are largely intact in medicated individuals with chronic schizophrenia, while reward anticipation responses in left ventral striatum are reduced in those patients with greater anhedonia severity.

Dataset Information

Elevated energy intake is correlated with hyperresponsivity in attentional, gustatory, and reward brain regions while anticipating palatable food receipt.

Publications

Elevated energy intake is correlated with hyperresponsivity in attentional, gustatory, and reward brain regions while anticipating palatable food receipt.

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