Neural circuits for cognitive appetite control in healthy and obese individuals: an fMRI study

Jetro J Tuulari, Henry K Karlsson, Jussi Hirvonen, Paulina Salminen, Pirjo Nuutila, Lauri Nummenmaa, Jetro J Tuulari, Henry K Karlsson, Jussi Hirvonen, Paulina Salminen, Pirjo Nuutila, Lauri Nummenmaa

Abstract

The mere sight of foods may activate the brain's reward circuitry, and humans often experience difficulties in inhibiting urges to eat upon encountering visual food signals. Imbalance between the reward circuit and those supporting inhibitory control may underlie obesity, yet brain circuits supporting volitional control of appetite and their possible dysfunction that can lead to obesity remain poorly specified. Here we delineated the brain basis of volitional appetite control in healthy and obese individuals with functional magnetic resonance imaging (fMRI). Twenty-seven morbidly obese women (mean BMI = 41.4) and fourteen age-matched normal-weight women (mean BMI = 22.6) were scanned with 1.5 Tesla fMRI while viewing food pictures. They were instructed to inhibit their urge to eat the foods, view the stimuli passively or imagine eating the foods. Across all subjects, a frontal cortical control circuit was activated during appetite inhibition versus passive viewing of the foods. Inhibition minus imagined eating (appetite control) activated bilateral precunei and parietal cortices and frontal regions spanning anterior cingulate and superior medial frontal cortices. During appetite control, obese subjects had lower responses in the medial frontal, middle cingulate and dorsal caudate nuclei. Functional connectivity of the control circuit was increased in morbidly obese versus control subjects during appetite control, which might reflect impaired integrative and executive function in obesity.

Trial registration: ClinicalTrials.gov NCT01373892.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Experimental design and trial structure.
Fig 1. Experimental design and trial structure.
Fig 2. Regional brain activations across all…
Fig 2. Regional brain activations across all subjects.
Brain regions showing stronger responses during inhibition minus passive viewing condition (A), imaginary eating minus passive viewing condition (B) and inhibition condition minus imaginary eating (C). The data are thresholded at p

Fig 3. Regional differences in brain activations…

Fig 3. Regional differences in brain activations between normal-weight and obese subjects.

Brain regions showing…

Fig 3. Regional differences in brain activations between normal-weight and obese subjects.
Brain regions showing stronger activation in normal-weight versus morbidly obese subjects in inhibition minus passive viewing (A), imaginary eating minus passive viewing (B) and inhibition minus versus imaginary eating (C) contrasts. The data in C are thresholded at p

Fig 4. Functional connectivity (PPI) across all…

Fig 4. Functional connectivity (PPI) across all subjects.

The data are thresholded at p

Fig 4. Functional connectivity (PPI) across all subjects.
The data are thresholded at p

Fig 5. Differences in functional connectivity (PPI)…

Fig 5. Differences in functional connectivity (PPI) in obese versus normal-weight individuals.

The data are…

Fig 5. Differences in functional connectivity (PPI) in obese versus normal-weight individuals.
The data are thresholded at p
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References
    1. Wynne K, Stanley S, McGowan B, Bloom S (2005) Appetite control. J Endocrinol 184: 291–318. - PubMed
    1. Nummenmaa L, Hirvonen J, Hannukainen J, Immonen H, Lindroos M, et al. (2012) Dorsal striatum and its limbic connectivity mediate abnormal anticipatory reward processing in obesity. PLoS ONE 7: e31089–e31089. 10.1371/journal.pone.0031089 - DOI - PMC - PubMed
    1. Swinburn B, Sacks G, Hall K, McPherson K, Finegood D, et al. (2011) The global obesity pandemic: Shaped by global drivers and local environments. Lancet (London, England) 378: 804–814. 10.1016/S0140-6736(11)60813-1 - DOI - PubMed
    1. Volkow N, Wang G, Tomasi D, Baler R (2013) The addictive dimensionality of obesity. Biol Psychiatry 73: 811–818 10.1016/j.biopsych.2012.12.020 - DOI - PMC - PubMed
    1. Koob G, Volkow N (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35: 217–238. 10.1038/npp.2009.110 - DOI - PMC - PubMed
Show all 32 references
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Grant support
This study was financially supported by the Academy of Finland (grants #256147 and #251125 to LN), the Sigrid Juselius Foundation, the University Hospital of Turku and the University of Turku (grant 10463 to JJT). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Fig 3. Regional differences in brain activations…
Fig 3. Regional differences in brain activations between normal-weight and obese subjects.
Brain regions showing stronger activation in normal-weight versus morbidly obese subjects in inhibition minus passive viewing (A), imaginary eating minus passive viewing (B) and inhibition minus versus imaginary eating (C) contrasts. The data in C are thresholded at p

Fig 4. Functional connectivity (PPI) across all…

Fig 4. Functional connectivity (PPI) across all subjects.

The data are thresholded at p

Fig 4. Functional connectivity (PPI) across all subjects.
The data are thresholded at p

Fig 5. Differences in functional connectivity (PPI)…

Fig 5. Differences in functional connectivity (PPI) in obese versus normal-weight individuals.

The data are…

Fig 5. Differences in functional connectivity (PPI) in obese versus normal-weight individuals.
The data are thresholded at p
Similar articles
Cited by
References
    1. Wynne K, Stanley S, McGowan B, Bloom S (2005) Appetite control. J Endocrinol 184: 291–318. - PubMed
    1. Nummenmaa L, Hirvonen J, Hannukainen J, Immonen H, Lindroos M, et al. (2012) Dorsal striatum and its limbic connectivity mediate abnormal anticipatory reward processing in obesity. PLoS ONE 7: e31089–e31089. 10.1371/journal.pone.0031089 - DOI - PMC - PubMed
    1. Swinburn B, Sacks G, Hall K, McPherson K, Finegood D, et al. (2011) The global obesity pandemic: Shaped by global drivers and local environments. Lancet (London, England) 378: 804–814. 10.1016/S0140-6736(11)60813-1 - DOI - PubMed
    1. Volkow N, Wang G, Tomasi D, Baler R (2013) The addictive dimensionality of obesity. Biol Psychiatry 73: 811–818 10.1016/j.biopsych.2012.12.020 - DOI - PMC - PubMed
    1. Koob G, Volkow N (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35: 217–238. 10.1038/npp.2009.110 - DOI - PMC - PubMed
Show all 32 references
Publication types
MeSH terms
Associated data
Related information
Grant support
This study was financially supported by the Academy of Finland (grants #256147 and #251125 to LN), the Sigrid Juselius Foundation, the University Hospital of Turku and the University of Turku (grant 10463 to JJT). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM

NCBI Literature Resources

MeSH PMC Bookshelf Disclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

Follow NCBI
Fig 4. Functional connectivity (PPI) across all…
Fig 4. Functional connectivity (PPI) across all subjects.
The data are thresholded at p

Fig 5. Differences in functional connectivity (PPI)…

Fig 5. Differences in functional connectivity (PPI) in obese versus normal-weight individuals.

The data are…

Fig 5. Differences in functional connectivity (PPI) in obese versus normal-weight individuals.
The data are thresholded at p
Similar articles
Cited by
References
    1. Wynne K, Stanley S, McGowan B, Bloom S (2005) Appetite control. J Endocrinol 184: 291–318. - PubMed
    1. Nummenmaa L, Hirvonen J, Hannukainen J, Immonen H, Lindroos M, et al. (2012) Dorsal striatum and its limbic connectivity mediate abnormal anticipatory reward processing in obesity. PLoS ONE 7: e31089–e31089. 10.1371/journal.pone.0031089 - DOI - PMC - PubMed
    1. Swinburn B, Sacks G, Hall K, McPherson K, Finegood D, et al. (2011) The global obesity pandemic: Shaped by global drivers and local environments. Lancet (London, England) 378: 804–814. 10.1016/S0140-6736(11)60813-1 - DOI - PubMed
    1. Volkow N, Wang G, Tomasi D, Baler R (2013) The addictive dimensionality of obesity. Biol Psychiatry 73: 811–818 10.1016/j.biopsych.2012.12.020 - DOI - PMC - PubMed
    1. Koob G, Volkow N (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35: 217–238. 10.1038/npp.2009.110 - DOI - PMC - PubMed
Show all 32 references
Publication types
MeSH terms
Associated data
Related information
Grant support
This study was financially supported by the Academy of Finland (grants #256147 and #251125 to LN), the Sigrid Juselius Foundation, the University Hospital of Turku and the University of Turku (grant 10463 to JJT). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM
Fig 5. Differences in functional connectivity (PPI)…
Fig 5. Differences in functional connectivity (PPI) in obese versus normal-weight individuals.
The data are thresholded at p

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