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Clinical Article
Imaging study of real-time fMRI neurofeedback training based on the nucleus ambiguus to improve obesity
QIAO Qi  ZHOU Jing  HE Junya  LI Xin  ZHOU Yang  SUN Yongbing  LI Zhonglin  ZOU Zhi  WU Xiaoling  LI Hao  LI Yongli 

Cite this article as: QIAO Q, ZHOU J, HE J Y, et al. Imaging study of real-time fMRI neurofeedback training based on the nucleus ambiguus to improve obesity[J]. Chin J Magn Reson Imaging, 2024, 15(10): 56-61. DOI:10.12015/issn.1674-8034.2024.10.010.


[Abstract] Objective Exploring the role of functional magnetic resonance imaging neurofeedback (rtfMRI-NF) to modulate bilateral nucleus ambiguus to improve obesity.Materials and Methods A total of 24 obese patients from December 2022 to December 2023 were recruited as study subjects. A 3-week rtfMRI-NF training intervention was conducted on the obese subjects, the Barratt Impulsiveness Scale Version 11 (BIS-11), three-factor eating questionnaire (TFEQ) with its three subscales: Uncontrolled Eating (UE), Cognitive Restriction (CR), and Emotional Eating (EE), the Food Grade Rating Scale, and resting-state functional magnetic resonance imaging datawere collected before and after the intervention. Paired-samples t-tests were used to compare changes in clinical scales before and after the subjects' intervention. Paired-sample t-tests were used to analyse the functional connectivity (FC) values of the obese subjects before and after the 3-week rtfMRI-NF intervention using SPM12 software. Pearson's correlation analysis was performed between the FC values of the statistically significant differences in brain regions and the scores of the clinical scales.Results BIS-11, TFEQ-UE, TFEQ-EE, and food grade scores decreased and TFEQ-CR scores increased after the intervention in obese patients (P<0.05). FC values of the left nucleus ambiguus with the left middle temporal gyrus decreased and those with the left middle frontal gyrus increased after the intervention in obese subjects (P<0.05, GRF-corrected). FC values of the right nucleus ambiguus with the right cerebellum and the right inferior frontal gyrus increased and FC values with the left precuneus decreased (P<0.05, GRF corrected). FC values in the right nucleus ambiguus-right cerebellar area 8 were negatively correlated with TFEQ-UE scores after intervention (r=-0.549, P=0.008), and FC values in the right nucleus ambiguus-left precuneus were positively correlated with BIS-11 scores (r=0.658, P<0.001).Conclusions The rtfMRI-NF intervention may ameliorate poor eating habits in obese patients by altering functional connectivity of the nucleus ambiguus with distributed brain regions of cognitive control, attentional bias, and emotional memory.
[Keywords] obesity;magnetic resonance imaging;real-time functional magnetic resonance imaging of neurofeedback;resting-state functional magnetic resonance imaging;nucleus ambiguus;functional connectivity

QIAO Qi1   ZHOU Jing2   HE Junya3   LI Xin3   ZHOU Yang1   SUN Yongbing1   LI Zhonglin1   ZOU Zhi1   WU Xiaoling4   LI Hao5   LI Yongli2*  

1 Medical Imaging Department, Zhengzhou University People's Hospital/Henan Provincial People's Hospital, Zhengzhou 450003, China

2 Health Management Department, Zhengzhou University People's Hospital/Henan Provincial People's Hospital, Zhengzhou 450003, China

3 Medical Imaging Department, Henan University People's Hospital/Henan Provincial People's Hospital, Zhengzhou 450003, China

4 Nuclear Medicine Department, Zhengzhou University People's Hospital/Henan Provincial People's Hospital, Zhengzhou 450003, China

5 Health Management Department, Fuwai Central China Cardiovascular Hospital, Zhengzhou 450003, China

Corresponding author: LI Y L, E-mail: shyliyongli@126.com

Conflicts of interest   None.

Received  2024-07-05
Accepted  2024-10-10
DOI: 10.12015/issn.1674-8034.2024.10.010
Cite this article as: QIAO Q, ZHOU J, HE J Y, et al. Imaging study of real-time fMRI neurofeedback training based on the nucleus ambiguus to improve obesity[J]. Chin J Magn Reson Imaging, 2024, 15(10): 56-61. DOI:10.12015/issn.1674-8034.2024.10.010.

[1]
PAN X F, WANG L M, PAN A. Epidemiology and determinants of obesity in China[J]. Lancet Diabetes Endocrinol, 2021, 9(6): 373-392. DOI: 10.1016/S2213-8587(21)00045-0.
[2]
WANG Y P, ZANG L, MU Y M. Current status and management of obesity in China[J]. Chin J Intern Med, 2023, 62(12): 1373-1379. DOI: 10.3760/cma.j.cn112138-20231010-00197.
[3]
WANG J, WANG F, CHEN H X, et al. Comparison of the effects of intermittent energy restriction and continuous energy restriction among adults with overweight or obesity: an overview of systematic reviews and meta-analyses[J/OL]. Nutrients, 2022, 14(11): 2315 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/35684119/. DOI: 10.3390/nu14112315.
[4]
ZOU Z, LI Z L, ZHOU J, et al. Research progress on the regulation target of real-time functional magnetic resonance imaging neurofeedback[J]. Chin J Magn Reson Imag, 2020, 11(8): 684-687. DOI: 10.12015/issn.1674-8034.2020.08.022.
[5]
GNINENKO N, TRZNADEL S, DASKALOU D, et al. Functional MRI neurofeedback outperforms cognitive behavioral therapy for reducing tinnitus distress: a prospective randomized clinical trial[J/OL]. Radiology, 2024, 310(2): e231143 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/38349241/. DOI: 10.1148/radiol.231143.
[6]
MORRISSEY G, TSUCHIYAGAITO A, TAKAHASHI T, et al. Could neurofeedback improve therapist-patient communication? Considering the potential for neuroscience informed examinations of the psychotherapeutic relationship[J/OL]. Neurosci Biobehav Rev, 2024, 161: 105680 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/38641091/. DOI: 10.1016/j.neubiorev.2024.105680.
[7]
WATANABE T, SASAKI Y, SHIBATA K, et al. Advances in fMRI real-time neurofeedback: (trends in cognitive sciences 21, 997-1010, 2017)[J/OL]. Trends Cogn Sci, 2018, 22(8): 738 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/29866489/. DOI: 10.1016/j.tics.2018.05.007.
[8]
KOHL S H, VEIT R, SPETTER M S, et al. Real-time fMRI neurofeedback training to improve eating behavior by self-regulation of the dorsolateral prefrontal cortex: a randomized controlled trial in overweight and obese subjects[J/OL]. Neuroimage, 2019, 191: 596-609 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/30798010/. DOI: 10.1016/j.neuroimage.2019.02.033.
[9]
FERRARIO C R. Why did I eat that? Contributions of individual differences in incentive motivation and nucleus accumbens plasticity to obesity[J/OL]. Physiol Behav, 2020, 227: 113114 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/32777311/. DOI: 10.1016/j.physbeh.2020.113114.
[10]
STICE E, YOKUM S, ROHDE P, et al. Evidence that a novel transdiagnostic eating disorder treatment reduces reward region response to the thin beauty ideal and high-calorie binge foods[J]. Psychol Med, 2023, 53(6): 2252-2262. DOI: 10.1017/S0033291721004049.
[11]
JANSSEN L K, DUIF I, SPECKENS A E M, et al. The effects of an 8-week mindful eating intervention on anticipatory reward responses in striatum and midbrain[J/OL]. Front Nutr, 2023, 10: 1115727 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/37637944/. DOI: 10.3389/fnut.2023.1115727.
[12]
STICE E, YOKUM S. Elevated reward, emotion, and memory region response to thin models predicts eating disorder symptom persistence: a prospective functional magnetic resonance imaging study[J]. J Psychopathol Clin Sci, 2023, 132(6): 716-724. DOI: 10.1037/abn0000843.
[13]
PARSONS N, STEWARD T, CLOHESY R, et al. A systematic review of resting-state functional connectivity in obesity: Refining Current neurobiological frameworks and methodological considerations moving forward[J]. Rev Endocr Metab Disord, 2022, 23(4): 861-879. DOI: 10.1007/s11154-021-09665-x.
[14]
ZHANG P, WU G W, TANG L R, et al. Altered brain structural reorganization and hierarchical integrated processing in obesity[J/OL]. Front Neurosci, 2022, 16: 796792 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/35368267/. DOI: 10.3389/fnins.2022.796792.
[15]
GAO X Y, ZHANG M Z, YANG Z G, et al. A study on the relationship between abnormally effective connections in the nucleus accumbens and the severity of nicotine addicts[J]. Chin J Psychiatry, 2022, 55(6): 429-435. DOI: 10.3760/cma.j.cn113661-20220714-00192.
[16]
CHEN G W, LAI S S, BAO G, et al. Distinct reward processing by subregions of the nucleus accumbens[J/OL]. Cell Rep, 2023, 42(2): 112069 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/36753418/. DOI: 10.1016/j.celrep.2023.112069.
[17]
ZHANG Y, GAO J W, LI N, et al. Targeting cAMP in D1-MSNs in the nucleus accumbens, a new rapid antidepressant strategy[J]. Acta Pharm Sin B, 2024, 14(2): 667-681. DOI: 10.1016/j.apsb.2023.12.005.
[18]
MAGNARD R, FOUYSSAC M, VACHEZ Y M, et al. Pramipexole restores behavioral inhibition in highly impulsive rats through a paradoxical modulation of frontostriatal networks[J/OL]. Transl Psychiatry, 2024, 14(1): 86 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/38336862/. DOI: 10.1038/s41398-024-02804-3.
[19]
NESELILER S, HU W, LARCHER K, et al. Neurocognitive and hormonal correlates of voluntary weight loss in humans[J/OL]. Cell Metab, 2019, 29(1): 39-49.e4 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/30344017/. DOI: 10.1016/j.cmet.2018.09.024.
[20]
RAMSAY I S, MUELLER B, MA Y Z, et al. Thalamocortical connectivity and its relationship with symptoms and cognition across the psychosis continuum[J]. Psychol Med, 2023, 53(12): 5582-5591. DOI: 10.1017/S0033291722002793.
[21]
YOKUM S, STICE E. Weight gain is associated with changes in neural response to palatable food tastes varying in sugar and fat and palatable food images: a repeated-measures fMRI study[J]. Am J Clin Nutr, 2019, 110(6): 1275-1286. DOI: 10.1093/ajcn/nqz204.
[22]
VAN GALEN K A, SCHRANTEE A, HORST K W TER, et al. Brain responses to nutrients are severely impaired and not reversed by weight loss in humans with obesity: a randomized crossover study[J]. Nat Metab, 2023, 5(6): 1059-1072. DOI: 10.1038/s42255-023-00816-9.
[23]
YANG Y K, WANG J J, QIU J, et al. Perigenual anterior cingulate cortex and its structural covariance as predictors for future body fat gain in young adults[J]. Obesity, 2023, 31(2): 446-453. DOI: 10.1002/oby.23629.
[24]
LIU Y, TAN S X, WU Y K, et al. Altered intrinsic regional spontaneous brain activity in patients with severe obesity and meibomian gland dysfunction: a resting-state functional magnetic resonance imaging study[J/OL]. Front Hum Neurosci, 2022, 16: 879513 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/35664349/. DOI: 10.3389/fnhum.2022.879513.
[25]
GRACIA-MARCO L, ESTEBAN-CORNEJO I, UBAGO-GUISADO E, et al. Lean mass index is positively associated with white matter volumes in several brain regions in children with overweight/obesity[J/OL]. Pediatr Obes, 2020, 15(5): e12604 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/31920013/. DOI: 10.1111/ijpo.12604.
[26]
SIMERLY R, DILEONE R. Cerebellar neurons that curb food consumption[J]. Nature, 2021, 600(7888): 229-230. DOI: 10.1038/d41586-021-03383-9.
[27]
LOW A Y T, GOLDSTEIN N, GAUNT J R, et al. Reverse-translational identification of a cerebellar satiation network[J]. Nature, 2021, 600(7888): 269-273. DOI: 10.1038/s41586-021-04143-5.
[28]
DOUCET G E, RASGON N, MCEWEN B S, et al. Elevated body mass index is associated with increased integration and reduced cohesion of sensory-driven and internally guided resting-state functional brain networks[J]. Cereb Cortex, 2018, 28(3): 988-997. DOI: 10.1093/cercor/bhx008.
[29]
LI Z L, WU X L, GAO H, et al. Intermittent energy restriction changes the regional homogeneity of the obese human brain[J/OL]. Front Neurosci, 2023, 17: 1201169 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/37600013/. DOI: 10.3389/fnins.2023.1201169.
[30]
ZHOU J, WU X L, XIANG T Y, et al. Dynamical alterations of brain function and gut microbiome in weight loss[J/OL]. Front Cell Infect Microbiol, 2023, 13: 1269548 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/38173792/. DOI: 10.3389/fcimb.2023.1269548.
[31]
ZHAO J, LONG Z L, LI Y, et al. Alteration of regional heterogeneity and functional connectivity for obese undergraduates: evidence from resting-state fMRI[J]. Brain Imaging Behav, 2022, 16(2): 627-636. DOI: 10.1007/s11682-021-00542-4.
[32]
DING Z N, LI P, LÜ D, et al. Association of dynamic functional connectivity with bilateral precuneus at resting-state with obsessive-compulsive disorder[J]. Chin J Psychiatry, 2022, 55(2): 106-114. DOI: 10.3760/cma.j.cn113661-20210917-00283.
[33]
MAVROGIORGOU P, BECKER S, LEE-GRIMM S I, et al. Embitterment and metacognition in obsessive-compulsive disorder[J/OL]. BMC Psychiatry, 2023, 23(1): 146 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/36890494/. DOI: 10.1186/s12888-023-04642-x.
[34]
YEUNG A W K. Brain responses to watching food commercials compared with nonfood commercials: a meta-analysis on neuroimaging studies[J]. Public Health Nutr, 2021, 24(8): 2153-2160. DOI: 10.1017/S1368980020003122.
[35]
ZHANG P, LIU Y, LV H, et al. Integration of neural reward processing and appetite-related signaling in obese females: evidence from resting-state fMRI[J]. J Magn Reson Imaging, 2019, 50(2): 541-551. DOI: 10.1002/jmri.26576.
[36]
GEARHARDT A N, YOKUM S, HARRIS J L, et al. Neural response to fast food commercials in adolescents predicts intake[J]. Am J Clin Nutr, 2020, 111(3): 493-502. DOI: 10.1093/ajcn/nqz305.

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