Human protein status modulates brain reward responses to food cues.
BACKGROUND
Protein is indispensable in the human diet, and its intake appears tightly regulated. The role of sensory attributes of foods in protein intake regulation is far from clear.


OBJECTIVE
We investigated the effect of human protein status on neural responses to different food cues with the use of functional magnetic resonance imaging (fMRI). The food cues varied by taste category (sweet compared with savory) and protein content (low compared with high). In addition, food preferences and intakes were measured.


METHODS
We used a randomized crossover design whereby 23 healthy women [mean ± SD age: 22 ± 2 y; mean ± SD body mass index (in kg/m(2)): 22.5 ± 1.8] followed two 16-d fully controlled dietary interventions involving consumption of either a low-protein diet (0.6 g protein · kg body weight(-1) · d(-1), ~7% of energy derived from protein, approximately half the normal protein intake) or a high-protein diet (2.2 g protein · kg body weight(-1) · d(-1), ~25% of energy, approximately twice the normal intake). On the last day of the interventions, blood oxygen level-dependent (BOLD) responses to odor and visual food cues were measured by using fMRI. The 2 interventions were followed by a 1-d ad libitum phase, during which a large array of food items was available and preference and intake were measured.


RESULTS
When exposed to food cues (relative to the control condition), the BOLD response was higher in reward-related areas (orbitofrontal cortex, striatum) in a low-protein state than in a high-protein state. Specifically, BOLD was higher in the inferior orbitofrontal cortex in response to savory food cues. In contrast, the protein content of the food cues did not modulate the BOLD response. A low protein state also increased preferences for savory food cues and increased protein intake in the ad libitum phase as compared with a high-protein state.


CONCLUSIONS
Protein status modulates brain responses in reward regions to savory food cues. These novel findings suggest that dietary protein status affects taste category preferences, which could play an important role in the regulation of protein intake in humans. This trial was registered at www.trialregister.nl/trialreg/admin/rctview.asp?TC=3288 as NTR3288.
From the Division of Human Nutrition, Wageningen University, Wageningen, Netherlands (SG-R,PAMS, EvdH, SB, and CdG); the Image Sciences Institute, University Medical Center Utrecht, Utrecht, Netherlands (PAMS); and the Institute of Psychological Sciences, University of Leeds, Leeds, United Kingdom (GF).
Sanne
S
Griffioen-Roose
From the Division of Human Nutrition, Wageningen University, Wageningen, Netherlands (SG-R,PAMS, EvdH, SB, and CdG); the Image Sciences Institute, University Medical Center Utrecht, Utrecht, Netherlands (PAMS); and the Institute of Psychological Sciences, University of Leeds, Leeds, United Kingdom (GF).
Paul Am
PA
Smeets
From the Division of Human Nutrition, Wageningen University, Wageningen, Netherlands (SG-R,PAMS, EvdH, SB, and CdG); the Image Sciences Institute, University Medical Center Utrecht, Utrecht, Netherlands (PAMS); and the Institute of Psychological Sciences, University of Leeds, Leeds, United Kingdom (GF).
Emmy
E
van den Heuvel
From the Division of Human Nutrition, Wageningen University, Wageningen, Netherlands (SG-R,PAMS, EvdH, SB, and CdG); the Image Sciences Institute, University Medical Center Utrecht, Utrecht, Netherlands (PAMS); and the Institute of Psychological Sciences, University of Leeds, Leeds, United Kingdom (GF).
Sanne
S
Boesveldt
From the Division of Human Nutrition, Wageningen University, Wageningen, Netherlands (SG-R,PAMS, EvdH, SB, and CdG); the Image Sciences Institute, University Medical Center Utrecht, Utrecht, Netherlands (PAMS); and the Institute of Psychological Sciences, University of Leeds, Leeds, United Kingdom (GF).
Graham
G
Finlayson
From the Division of Human Nutrition, Wageningen University, Wageningen, Netherlands (SG-R,PAMS, EvdH, SB, and CdG); the Image Sciences Institute, University Medical Center Utrecht, Utrecht, Netherlands (PAMS); and the Institute of Psychological Sciences, University of Leeds, Leeds, United Kingdom (GF).
Cees
C
de Graaf
D015992:Body Mass Index; D001835:Body Weight; D001921:Brain / Q000502:physiology*; D002755:Choice Behavior / Q000502:physiology; D018592:Cross-Over Studies; D003463:Cues; D018753:Diet, Protein-Restricted; D004040:Dietary Carbohydrates / Q000008:administration & dosage; D004041:Dietary Fats / Q000008:administration & dosage; D004044:Dietary Proteins / Q000008:administration & dosage*; D002149:Energy Intake; D005247:Feeding Behavior / Q000523:psychology*; D005260:Female; D005518:Food Preferences / Q000523:psychology*; D064368:Healthy Volunteers; D006801:Humans; D008279:Magnetic Resonance Imaging; D009474:Neurons / Q000502:physiology; D009752:Nutritional Status; D012201:Reward; D013649:Taste; D055815:Young Adult
D004040:Dietary Carbohydrates; D004041:Dietary Fats; D004044:Dietary Proteins