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Patterns of brain structural connectivity differentiate normal weight from overweight subjects

Authors :
Jennifer S. Labus
Benjamin M. Ellingson
Claudia P. Sanmiguel
John D. Van Horn
Kirsten Tillisch
Connor Fling
Emeran A. Mayer
Aubrey D. Love
Davis C. Woodworth
Arpana Gupta
Source :
NeuroImage: Clinical, Vol 7, Iss C, Pp 506-517 (2015), NeuroImage : Clinical, Gupta, A; Mayer, EA; Sanmiguel, CP; Van Horn, JD; Woodworth, D; Ellingson, BM; et al.(2015). Patterns of brain structural connectivity differentiate normal weight from overweight subjects. NEUROIMAGE-CLINICAL, 7, 506-517. doi: 10.1016/j.nicl.2015.01.005. UCLA: Retrieved from: http://www.escholarship.org/uc/item/5k58f6kq
Publication Year :
2015
Publisher :
Elsevier, 2015.

Abstract

Background Alterations in the hedonic component of ingestive behaviors have been implicated as a possible risk factor in the pathophysiology of overweight and obese individuals. Neuroimaging evidence from individuals with increasing body mass index suggests structural, functional, and neurochemical alterations in the extended reward network and associated networks. Aim To apply a multivariate pattern analysis to distinguish normal weight and overweight subjects based on gray and white-matter measurements. Methods Structural images (N = 120, overweight N = 63) and diffusion tensor images (DTI) (N = 60, overweight N = 30) were obtained from healthy control subjects. For the total sample the mean age for the overweight group (females = 32, males = 31) was 28.77 years (SD = 9.76) and for the normal weight group (females = 32, males = 25) was 27.13 years (SD = 9.62). Regional segmentation and parcellation of the brain images was performed using Freesurfer. Deterministic tractography was performed to measure the normalized fiber density between regions. A multivariate pattern analysis approach was used to examine whether brain measures can distinguish overweight from normal weight individuals. Results 1. White-matter classification: The classification algorithm, based on 2 signatures with 17 regional connections, achieved 97% accuracy in discriminating overweight individuals from normal weight individuals. For both brain signatures, greater connectivity as indexed by increased fiber density was observed in overweight compared to normal weight between the reward network regions and regions of the executive control, emotional arousal, and somatosensory networks. In contrast, the opposite pattern (decreased fiber density) was found between ventromedial prefrontal cortex and the anterior insula, and between thalamus and executive control network regions. 2. Gray-matter classification: The classification algorithm, based on 2 signatures with 42 morphological features, achieved 69% accuracy in discriminating overweight from normal weight. In both brain signatures regions of the reward, salience, executive control and emotional arousal networks were associated with lower morphological values in overweight individuals compared to normal weight individuals, while the opposite pattern was seen for regions of the somatosensory network. Conclusions 1. An increased BMI (i.e., overweight subjects) is associated with distinct changes in gray-matter and fiber density of the brain. 2. Classification algorithms based on white-matter connectivity involving regions of the reward and associated networks can identify specific targets for mechanistic studies and future drug development aimed at abnormal ingestive behavior and in overweight/obesity.<br />Highlights • Multivariate analysis can be used to classify overweight from normal weight individuals. • Anatomical connectivity achieved 97% accuracy in the classification algorithm. • Greater connectivity was observed in extended reward and somatosensory regions. • Morphological gray-matter achieved 69% accuracy in the classification algorithm. • Lower morphological values were observed in regions of the extended reward network.

Subjects

Subjects :
Male
HC
VIP, variable importance in projection
sgACC, subgenual anterior cingulate cortex
FACT, fiber assignment by continuous tracking
general linear model
variable importance in projection
Brain mapping
CT, cortical thickness
0302 clinical medicine
MC, mean curvature
GLM, general linear model
sgACC
dlPFC, dorsolateral prefrontal cortex
negative predictive value
gray matter volume
repetition time
FOV
TE, echo time
0303 health sciences
ANOVA
Brain
Regular Article
diffusion tensor imaging
anterior cingulate cortex
Diffusion Tensor Imaging
NPV, negative predictive value
Neurology
DTI
GMV, gray matter volume
Biomedical Imaging
sparse partial least squares for discrimination Analysis
posterior parietal cortex
FACT
ventral tegmental area
mean curvature
aMCC
sPLS-DA, sparse partial least squares for discrimination Analysis
lcsh:Computer applications to medicine. Medical informatics
Basic Behavioral and Social Science
Classification algorithm
NPV
03 medical and health sciences
SA
Clinical Research
diffusion-weighted MRIs
Humans
Risk factor
HAD, hospital anxiety and Depression Scale
Morphological gray-matter
healthy control
Reward network
surface area
sPLS-DA
medicine.disease
Obesity
VIP
false-discovery rate
Neurology (clinical)
DTI, diffusion tensor imaging
Anatomical white-matter connectivity
GLM
Neuroscience
Body mass index
030217 neurology & neurosurgery
SPSS
PPC, posterior parietal cortex
TR
BMI, body mass index
DWI
Overweight
FOV, field of view
lcsh:RC346-429
Computer-Assisted
aMCC, anterior mid cingulate cortex
Neural Pathways
MC
hospital anxiety and Depression Scale
ANOVA, analysis of variance
2. Zero hunger
dorsolateral prefrontal cortex
Brain Mapping
OFG, orbitofrontal gyrus
GMV
ACC, anterior cingulate cortex
HC, healthy control
Magnetic Resonance Imaging
TR, repetition time
lcsh:R858-859.7
Female
medicine.symptom
Psychology
field of view
dlPFC
PPC
VTA
Algorithms
CT
TE
Adult
analysis of variance
FA
orbitofrontal gyrus
OFG
Cognitive Neuroscience
body mass index
PPV
vmPFC, ventromedial prefrontal cortex
DWI, diffusion-weighted MRIs
ventromedial prefrontal cortex
echo time
VTA, ventral tegmental area
FDR
BMI
Neurochemical
vmPFC
Neuroimaging
Behavioral and Social Science
Image Interpretation, Computer-Assisted
medicine
Radiology, Nuclear Medicine and imaging
SPSS, statistical package for the social sciences
ACC
Image Interpretation
lcsh:Neurology. Diseases of the nervous system
030304 developmental biology
Nutrition
fiber assignment by continuous tracking
subgenual anterior cingulate cortex
HAD
Neurosciences
Feeding Behavior
FDR, false-discovery rate
cortical thickness
statistical package for the social sciences
anterior mid cingulate cortex
SA, surface area
PPV, positive predictive value
FA, flip angle
flip angle
Multivariate analysis
positive predictive value
Ingestive behaviors

Details

Language :
English
ISSN :
22131582
Volume :
7
Database :
OpenAIRE
Journal :
NeuroImage: Clinical
Accession number :
edsair.doi.dedup.....0a8c8d3fdf042cb85c293b036a921b17
Full Text :
https://doi.org/10.1016/j.nicl.2015.01.005.