Skip to main content
Download PDF

Homeostatic modulation on unconscious hedonic responses to food

BMC Research Notes volume 10, Article number: 511 (2017) Cite this article

Abstract

Objective

Hedonic/affective responses to food play a critical role in eating behavior. Previous behavioral studies have shown that hedonic responses to food are elicited consciously and unconsciously. Although the studies also showed that hunger and satiation have a modulatory effect on conscious hedonic responses to food, the effect of these homeostatic states on unconscious hedonic responses to food remains unknown.

Results

We investigated unconscious hedonic responses to food in hungry and satiated participants using the subliminal affective priming paradigm. Food images or corresponding mosaic images were presented in the left or right peripheral visual field during 33 ms. Then photographs of target faces with emotionally neutral expressions were presented, and the participants evaluated their preference for the faces. Additionally, daily eating behaviors were assessed using questionnaires. Preference for the target faces was increased by food images relative to the mosaics in the hungry, but not the satiated, state. The difference in preference ratings between the food and mosaic conditions was positively correlated with the tendency for external eating in the hungry, but not the satiated, group. Our findings suggest that homeostatic states modulate unconscious hedonic responses to food and that this phenomenon is related to daily eating behaviors.

Introduction

Hedonic or affective responses, such as liking, to food stimuli have significant effects on human life, both advantageously (e.g., facilitating survival) and disadvantageously (e.g., triggering overeating and lifestyle disease). Previous behavioral studies have shown that seeing and consuming food elicit hedonic responses, which in turn induce food intake [1,2,3,4,5,6,7,8].

A recent study has demonstrated that hedonic responses to food were elicited rapidly even without conscious awareness of the food [9] using a subliminal affective priming paradigm [10, 11]. The investigators found that the subliminal presentation of food stimuli heightened the preference for subsequent face targets more than the subliminal presentation of mosaics. These findings suggest that the unconscious hedonic responses elicited by food spill over into the hedonic evaluation of unrelated targets. Such behavioral evidence is consistent with findings from neuroimaging studies showing that brain regions that are activated in response to the sight of food, such as the amygdala and nucleus accumbens [e.g., [12]; for a review, see [13] ], are also activated in response to subliminally presented non-food affective stimuli, such as emotional facial expressions [14]. Taken together, previous behavioral and neuroimaging data suggest that hedonic responses to food are elicited both consciously and unconsciously.

However, whether the unconscious hedonic responses to food might be modulated by the homeostatic states of hunger and satiation remains unknown. This issue is important because hedonic responses to external food stimuli and homeostatic control of internal states jointly control eating behaviors [15, 16]. A previous study has tested unconscious hedonic responses to food only in hungry participants [9]; thus, the unconscious hedonic response to food in the satiated state remains unknown. In contrast, several previous studies fund that conscious hedonic responses to food are modulated by hunger and satiation [2,3,4, 17,18,19,20]; specifically, the pleasant feelings toward supraliminal food stimuli are reduced in satiated compared with hungry participants [2,3,4, 17,18,19,20]. Moreover, the rapid, automatic processes related to supraliminal food stimuli, such as attention orienting to food, are attenuated in the satiated relative to the hungry state [18, 21,22,23]. Furthermore, neuroimaging studies showed reduced amygdala activity during the observation of supraliminal food images in the satiated compared with the hungry state [24, 25]. Based on these data, we hypothesized that unconscious hedonic responses to food may be modulated by the homeostatic state such that the responses are attenuated in the satiated relative to the hungry state.

Furthermore, it remains unclear whether the relationship between unconscious hedonic responses to food and daily eating behaviors could be modulated by homeostatic states. A previous investigation of unconscious hedonic responses to food [9] has assessed daily eating behaviors using the Dutch eating behavior questionnaire (DEBQ) [26]. The DEBQ measures the tendency for external eating, restrained eating, and emotional eating toward overeating [26]. The investigators found that the unconscious preference for food was correlated positively with external eating, defined as a tendency to eat in response to external cues, such as the sight of food. However, this study did not include fed participants. A previous neuroimaging study found that external eating modulated the functional connectivity between the amygdala and nucleus accumbens during the viewing of food images [27]. Because amygdala activity is altered according to homeostatic state [24, 25], we hypothesized that the relationship between unconscious hedonic responses to food and external eating tendencies may be modulated by homeostatic state.

To test theses hypotheses, we investigated the unconscious and conscious hedonic responses to food and non-food images in hungry and satiated participants. We assessed the unconscious hedonic responses using the subliminal affective priming paradigm [28] (Fig. 1). We presented food images and corresponding mosaics during 33 ms in the inattentional peripheral visual field, followed by a mask. Target faces with neutral expressions were subsequently presented, and participants evaluated their preference for the faces. To investigate conscious hedonic responses, we supraliminally presented food and mosaic images and participants rated their preference for the images. Participants were randomly assigned to the hungry- or satiated-state condition and we tested the modulatory effect of the homeostatic state on unconscious and conscious hedonic responses to food. Moreover, we used the DEBQ and evaluated the modulatory influence of homeostatic state on the relationships between the unconscious/conscious hedonic responses and daily eating behaviors.

Fig. 1
figure 1

Schematic of the protocols under the subliminal and supraliminal presentation conditions. Photographic stimuli were used in the experiments

Full size image

Main text

Methods and Supplementary findings are presented in Additional files 1 and 2, respectively.

Findings

Preference evaluation

Under the subliminal condition, the two-way analysis of variance (ANOVA) for preference ratings for target faces (Fig. 2), with homeostatic state (hungry/satiated) and stimulus type (food/mosaic) as factors, revealed a significant main effect of homeostatic state (F(1,67) = 6.74, p < 0.05, η 2 p  = 0.09), indicating that the preference ratings for faces under the satiated condition were higher than those under the hungry condition. Furthermore, the interaction between homeostatic state and stimulus type was significant (F(1,67) = 7.19, p < 0.005, η 2 p  = 0.10), indicating that the subliminal hedonic effects of food differed between homeostatic states. The main effect of stimulus type was not significant (F(1,67) = 1.84, p > 0.1).

Fig. 2
figure 2

Mean (± standard error) preference ratings under the subliminal (left) and supraliminal (right) presentation conditions. Asterisks indicate significant simple main effects (*p < 0.05; **p < 0.005; ***p < 0.001)

Full size image

Follow-up analyses of the interaction revealed a significant simple main effect of stimulus type under the hungry (F(1,67) = 8.15, p < 0.005), but not under the satiated (F(1,67) = 0.87, p > 0.1), condition, indicating that the preference ratings for faces primed by food images were higher than those primed by mosaics under the hungry, but not the satiated, condition. The simple main effect of homeostatic state was significant for the food and mosaic stimuli (F(1,134) = 4.77, p < 0.05; F(1,134) = 8.73, p < 0.005, respectively) confirming the main effect of homeostatic state.

Under the supraliminal condition, the two-way ANOVA for preference ratings for food and mosaic stimuli (Fig. 2) revealed a significant main effect of stimulus type (F(1,67) = 267.73, p < 0.001, η 2 p  = 0.80), indicating that the preference ratings for food were higher than those for the mosaics. More importantly, the interaction between homeostatic state and stimulus type was significant (F(1,67) = 14.25, p < 0.001, η 2 p  = 0.18), indicating that the preferential ratings for food versus mosaics differed between homeostatic states. The main effect of homeostatic state was not significant (F(1,67) = 1.84, p > 0.1).

Follow-up analyses of the interaction revealed a significant simple main effect of stimulus type under the hungry and satiated conditions (F(1,67) = 202.75, p < 0.001; F(1,67) = 79.227, p < 0.001, respectively), indicating that the preference ratings for food were higher than those for mosaics in both homeostatic states. The simple main effect of homeostatic state was also significant for the food and mosaic stimuli (F(1,134) = 8.75, p < 0.001; F(1,134) = 4.40, p < 0.005, respectively), indicating that the preference for food stimuli was decreased in the satiated state and the preference for mosaic stimuli was decreased in the hungry state.

Relationship between food preference and daily eating behaviors

We calculated the correlation coefficients between the food preference (differences in preference ratings between the food and mosaic conditions) and the DEBQ scores under the subliminal and supraliminal conditions (Additional file 3: Table S1). Consistent with our hypothesis, the correlation coefficients between the food preference under the subliminal condition and external eating scores differed for the different homeostatic states (Fig. 3). They were significant in the hungry state (r = 0.34, p < 0.05), but not in the satiated state (r = − 0.19, p > 0.1). To statistically test this difference, we performed a multiple regression analysis with the external eating score, homeostatic state, and the interaction between them as independent variables and the food preference under the subliminal condition as the dependent variable and confirmed the significant interaction (β = 0.26, t(52) = 2.08, p < 0.05). We conducted a series of explorative regression analyses and found no other significant interaction between homeostatic state and DEBQ score (t(52) < 1.60, p > 0.1).

Fig. 3
figure 3

A scatterplot with a regression line showing food preference scores under the subliminal condition as a function of external eating tendencies. An asterisk indicates a significant correlation (*p < 0.05)

Full size image

Discussion

Our findings revealed a modulatory effect of homeostatic state (hunger versus satiation) on preference ratings for food and mosaic images under the supraliminal condition, such that participants in the satiated group showed a decreased preference for food and increased preference for mosaics relative to those in the hungry group. This pattern corroborates previous findings that the satiated state is associated with a decreased preference for food and increased preference for non-food items [3, 4, 19].

More importantly, our findings under the subliminal condition revealed that compared with the hungry state, satiation attenuated the unconscious hedonic responses to food (interaction between homeostatic state and stimulus type) and heightened the overall preference for faces (main effect of homeostatic state). Our findings are consistent with those of previous studies using supraliminal stimuli [2,3,4, 17,18,19,20]. Furthermore, our findings do not contradict those of neuroimaging studies showing that less amygdala activity was elicited by supraliminal presentation of food stimuli in the satiated state than in the hungry state [24, 25]. Moreover, a recent neuroimaging study [29] found that amygdala activity elicited by the supraliminal presentation of food stimuli was modulated by hypothalamic input in hungry, but not satiated, participants. The hypothalamus is known to be involved in homeostatic regulation via communication with the somatic system [30]. Our study extends previous findings related to conscious hedonic responses by providing the first evidence that unconscious hedonic responses to food are modulated by homeostatic states.

Furthermore, our correlational analyses revealed that the positive association between the food preference and external eating under the subliminal condition was weaker in the satiated compared with the hungry participants. Our finding is consistent with those in previous neuroimaging studies showing that (1) amygdala activity is related to the unconscious hedonic processing of non-food stimuli [14], (2) amygdala functional connectivity is modulated by external eating tendencies [27], and (3) food-related amygdala activity is altered in response to homeostatic state [24, 25]. Because the external eating score is an indicator of the tendency for eating to be elicited by external stimuli [26], our behavioral findings indicate that externally driven daily eating behaviors are associated with unconscious hedonic responses specifically when individuals are hungry.

Our study has several practical implications. First, our findings suggest that hunger and satiation may influence unconscious hedonic responses to food and daily eating behaviors related to overeating. Because healthy eating behaviors, such as consuming a low-calorie diet, require suppressing unconscious hedonic responses and externally-driven overeating behaviors, our findings may provide behavioral strategies for dieting. For example, we recommend that people eat before visiting food-abundant environments, such as supermarkets and convenience stores, to reduce the unconscious hedonic processing of food and subsequent overeating.

Second, because images of faces were the target stimuli under the subliminal condition, our results imply that being satiated unconsciously enhances the general preference for people. Thus, the consumption of food during meetings, on romantic dates, or in various other situations may unconsciously heighten emotionally positive interactions.

Limitations

Our study has several limitations. First, we used a between-subjects experimental design to examine the effect of homeostatic state. Although this design allowed us to investigate the participants’ naïve responses (without contextual referencing) under the subliminal condition [31], it did not allow us to assess whether changes in homeostatic states could modulate unconscious hedonic responses, as well as the association between unconscious hedonic responses and external eating tendencies, in individual participants as would a within-subjects design. Further studies using a within-subjects design are warranted to complement and extend our findings.

Second, we only assessed daily eating behaviors using the DEBQ and did not measure actual food intake behaviors. The relationship between the DEBQ scores and actual food intake behaviors are controversial; some investigators have reported convergence between these measures [e.g., [32]] while others have not [e.g., [33]]. The relationship between unconscious homeostatic–hedonic interaction and actual food intake behaviors is an interesting topic for future research.

Abbreviations

ANOVA:

analysis of variance

DEBQ:

Dutch eating behavior questionnaire

References

  1. Blechert J, Meule A, Busch NA, Ohla K. Food-pics: an image database for experimental research on eating and appetite. Front Psychol. 2014;5:617.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Finlayson G, King N, Blundell JE. Is it possible to dissociate ‘liking’ and ‘wanting’ for foods in humans? a novel experimental procedure. Physiol Behav. 2007;90:36–42.

    Article  CAS  PubMed  Google Scholar 

  3. Jiang T, Soussignan R, Rigaud D, Martin S, Royet JP, Brondel L, Schaal B. Alliesthesia to food cues: heterogeneity across stimuli and sensory modalities. Physiol Behav. 2008;95:464–70.

    Article  CAS  PubMed  Google Scholar 

  4. Lemmens SG, Schoffelen PF, Wouters L, Born JM, Martens MJ, Rutters F, Westerterp-Plantenga MS. Eating what you like induces a stronger decrease of ‘wanting’ to eat. Physiol Behav. 2009;98:318–25.

    Article  CAS  PubMed  Google Scholar 

  5. Nisbett RE. Taste, deprivation, and weight determinants of eating behavior. J Personal Soc Psychol. 1968;10:107–16.

    Article  CAS  Google Scholar 

  6. Rodriguez S, Fernandez MC, Cepeda-Benito A, Vila J. Subjective and physiological reactivity to chocolate images in high and low chocolate cravers. Biol Psychol. 2005;70:9–18.

    Article  PubMed  Google Scholar 

  7. Sørensen LB, Møller P, Flint A, Martens M, Raben A. Effect of sensory perception of foods on appetite and food intake: a review of studies on humans. Int J Obes Relat Metab Disord. 2003;7:1152–66.

    Article  Google Scholar 

  8. Yeomans MR, Blundell JE, Leshem M. Palatability: response to nutritional need or need-free stimulation of appetite? Br J Nutr. 2004;92:Suppl 1:S3–14.

    Article  CAS  PubMed  Google Scholar 

  9. Sato W, Sawada R, Kubota Y, Toichi M, Fushiki T. Unconscious affective responses to food. PLoS ONE. 2016;11:e0160956.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Murphy ST, Zajonc RB. Affect, cognition, and awareness: affective priming with optimal and suboptimal stimulus exposures. J Personal Soc Psychol. 1993;64:723–39.

    Article  CAS  Google Scholar 

  11. Eastwood JD, Smilek D. Functional consequences of perceiving facial expressions of emotion without awareness. Conscious Cogn. 2005;14:565–84.

    Article  PubMed  Google Scholar 

  12. Killgore WD, Young AD, Femia LA, Bogorodzki P, Rogowska J, Yurgelun-Todd DA. Cortical and limbic activation during viewing of high- versus low-calorie foods. Neuroimage. 2003;19:1381–94.

    Article  PubMed  Google Scholar 

  13. Carnell S, Gibson C, Benson L, Ochner CN, Geliebter A. Neuroimaging and obesity: current knowledge and future directions. Obes Rev. 2012;13:43–56.

    Article  CAS  PubMed  Google Scholar 

  14. Suslow T, Kugel H, Ohrmann P, Stuhrmann A, Grotegerd D, Redlich R, et al. Neural correlates of affective priming effects based on masked facial emotion: an fMRI study. Psychiatry Res. 2013;211:239–45.

    Article  PubMed  Google Scholar 

  15. Cabanac M. Physiological role of pleasure. Science. 1971;173:1103–7.

    Article  CAS  PubMed  Google Scholar 

  16. Schachter S. Obesity and eating. Internal and external cues differentially affect the eating behavior of obese and normal subjects. Science. 1968;161:751–6.

    Article  CAS  PubMed  Google Scholar 

  17. Cameron JD, Goldfield GS, Finlayson G, Blundell JE, Doucet E. Fasting for 24 hours heightens reward from food and food-related cues. PLoS ONE. 2014;9:e85970.

    Article  PubMed  PubMed Central  Google Scholar 

  18. di Pellegrino G, Magarelli S, Mengarelli F. Food pleasantness affects visual selective attention. Q J Exp Psychol. 2011;64:560–71.

    Article  Google Scholar 

  19. Stoeckel LE, Cox JE, Cook EW 3rd, Weller RE. Motivational state modulates the hedonic value of food images differently in men and women. Appetite. 2007;48:139–44.

    Article  PubMed  Google Scholar 

  20. Rolls ET, Rolls BJ, Rowe EA. Sensory-specific and motivation-specific satiety for the sight and taste of food and water in man. Physiol Behav. 1983;30:185–92.

    Article  CAS  PubMed  Google Scholar 

  21. Castellanos EH, Charboneau E, Dietrich MS, Park S, Bradley BP, Mogg K, Cowan RL. Obese adults have visual attention bias for food cue image: evidence for altered reward system function. Int J Obes. 2009;33:1063–73.

    Article  CAS  Google Scholar 

  22. Gearhardt AN, Treat TA, Hollingworth A, Corbin WR. The relationship between eating-related individual differences and visual attention to foods high in added fat and sugar. Eat Behav. 2012;13:371–4.

    Article  PubMed  Google Scholar 

  23. Giel KE, Friederich H-C, Teufel M, Hautzinger M, Enck P, Zipfel S. Attentional processing of food pictures in individuals with anorexia nervosa—An eye-tracking study. Biol Psychiatry. 2011;69:661–7.

    Article  PubMed  Google Scholar 

  24. Führer D, Zysset S, Stumvoll M. Brain activity in hunger and satiety: an exploratory visually stimulated FMRI study. Obesity. 2008;16:945–50.

    Article  PubMed  Google Scholar 

  25. Goldstone AP, Prechtl de Hernandez CG, Beaver JD, Muhammed K, Croese C, Bell G, et al. Fasting biases brain reward systems towards high-calorie foods. Eur J Neurosci. 2009;30:1625–35.

    Article  PubMed  Google Scholar 

  26. van Strien T, Frijters JER, Bergers GPA, Defares PB. The Dutch eating behavior questionnaire (DEBQ) for assessment of restrained, emotional, and external eating behavior. Int J Eat Disord. 1986;5:295–315.

    Article  Google Scholar 

  27. Passamonti L, Rowe JB, Schwarzbauer C, Ewbank MP, von dem Hagen E, Calder AJ. Personality predicts the brain’s response to viewing appetizing foods: the neural basis of a risk factor for overeating. J Neurosci. 2009;29:43–51.

    Article  CAS  PubMed  Google Scholar 

  28. Sato W, Aoki S. Right hemispheric dominance in processing of unconscious negative emotion. Brain Cogn. 2006;62:261–6.

    Article  PubMed  Google Scholar 

  29. Sun X, Kroemer NB, Veldhuizen MG, Babbs AE, de Araujo IE, Gitelman DR, et al. Basolateral amygdala response to food cues in the absence of hunger is associated with weight gain susceptibility. J Neurosci. 2015;35:7964–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Berthoud HR. Interactions between the “cognitive” and “metabolic” brain in the control of food intake. Physiol Behav. 2007;91:486–98.

    Article  CAS  PubMed  Google Scholar 

  31. Charness G, Gneezy U, Kuhn MA. Experimental methods: between-subject and within-subject design. J Econ Behav Organ. 2012;81:1–8.

    Article  Google Scholar 

  32. van Strien T, Peter Herman C, Anschutz D. The predictive validity of the DEBQ-external eating scale for eating in response to food commercials while watching television. Int J Eat Disord. 2012;45:257–62.

    Article  PubMed  Google Scholar 

  33. Jansen A, Nederkoorn C, Roefs A, Bongers P, Teugels T, Havermans R. The proof of the pudding is in the eating: is the DEBQ-external eating scale a valid measure of external eating? Int J Eat Disord. 2011;44:164–8.

    PubMed  Google Scholar 

Download references

Authors’ contributions

Conceived and designed the experiments: WS, RS, YK, MT, and TF. Performed the experiments: WS and RS. Analyzed the data: WS. Wrote the paper: WS, RS, YK, and TF. All authors read and approved the final manuscript.

Acknowledgements

The authors thank Ms. Kazusa Minemoto for her technical support and our anonymous reviewers for their helpful advice.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

The dataset supporting the conclusions of this article is included within Additional file 4.

Consent for publication

Not applicable.

Ethics approval and consent to participate

This study was ethically approved by the Ethics Committee of the Graduate School of Medicine, Kyoto University (R0256), and was conducted in accordance with the approved guidelines. Written informed consent was obtained from all participants after the experimental procedure was fully explained.

Funding

This study was supported by grants from the Project of the NARO Bio-oriented Technology Research Advancement Institution (Integration research for agriculture and interdisciplinary fields, Japan) and the Research Complex Program from Japan Science and Technology Agency.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Author information

Authors and Affiliations

  1. Department of Neurodevelopmental Psychiatry, Habilitation and Rehabilitation, Graduate School of Medicine, Kyoto University, 53 Shogoin-Kawaharacho, Sakyo, Kyoto, 606-8507, Japan

    Wataru Sato & Reiko Sawada

  2. Health and Medical Services Center, Shiga University, 1-1-1 Baba, Hikone, Shiga, 522-8522, Japan

    Yasutaka Kubota

  3. Faculty of Human Health Science, Graduate School of Medicine, Kyoto University, 53 Shogoin-Kawaharacho, Sakyo-ku, Kyoto, 606-8507, Japan

    Motomi Toichi

  4. The Organization for Promoting Neurodevelopmental Disorder Research, 40 Shogoin-Sannocho, Sakyo, Kyoto, 606-8392, Japan

    Motomi Toichi

  5. Faculty of Agriculture, Ryukoku University, 1-5 Seta Oe-Cho Koya, Ohtsu, Shiga, 520-2194, Japan

    Tohru Fushiki

Authors
  1. Wataru Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Reiko Sawada
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yasutaka Kubota
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Motomi Toichi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tohru Fushiki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wataru Sato.

Additional files

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sato, W., Sawada, R., Kubota, Y. et al. Homeostatic modulation on unconscious hedonic responses to food. BMC Res Notes 10, 511 (2017). https://doi.org/10.1186/s13104-017-2835-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s13104-017-2835-y

Keywords

BMC Research Notes

ISSN: 1756-0500

Contact us