Obesity-specific Circuits in the Human Brain: Exploration by Dynamic Brain Self-reference (dynBSR)

Abstract

In the last decade many efforts have been made in order to identify brain regions that may be abnormal in obese subjects. Most of the lines of research have examined links between brain circuits, behavioral processing, and overweight. We introduce here a novel analysis to the brain mapping, ‘dynamic Brain Self-Reference’ (dynBSR), based on the electrical response evoked during passively viewing a simple stimulus. Hypothetically, it should be possible to monitor both task-related networks and task-irrelevant networks during a mental state with low cognitive demand, as shown previously by others using fMRI and establishing the latter as the neural correlates of an ‘inherent’ brain activation pattern. However, this fact has been usually ignored. Our results showed that a distinct set of interconnected brain regions including, frontal areas (middle, inferior, orbitofrontal, and dorsolateral), dorsal/ventral striatum, thalamus, superior temporal region, insula cortex, post-central gyrus, left supramarginal gyrus, and parietal regions, whose activities seem to be tonically maintained, displays cohesive functional state in obesity during passively viewing a simple stimulus. This organized network is maintained in a dynamic equilibrium with the transient activation of the right supramarginal gyrus. These brain areas have been previously implicated in the regulation of taste, reward, and behavioral processing and most of them have also structural abnormalities regarding normal-weight subjects. Although exploratory, the most important result here is that the evaluation of the visual-evoked responses with dynBSR provides a foundation for investigating the brain circuits in obesity, and becomes the first attempt, to our knowledge, to imply task-irrelevant networks in these individuals.

Key words

VEP - dynBSR - connectivity - neuroimage

References

• 1 Figlewicz DP. Adiposity signals and food reward: expanding the CNS roles of insulin and leptin.  Am J Physiol Regul Integr Comp Physiol. 2003;  284 R882-R892
• 2 Pannacciuli N, Del Parigi A, Chen K, Le DS, Reiman EM, Tataranni A. Brain abnormalities in human obesity: A voxel-based morphometric study.  Neuroimage. 2006;  31 1419-1125
• 3 Wang GJ, Volkow ND, Felder C, Fowler JS, Levy AV, Pappas NR, Wong CT, Zhu W, Netusil N. Enhanced resting activity of the oral somatosensory cortex in obese subjects.  NeuroReport. 2002;  13 1151-1155
• 4 Small DM, Jones-Gotman M, Zatorre RJ, Petrides M, Evans AC. Flavor processing: more than the sum of its parts.  Neuroreport. 1997;  8 3913-3917
• 5 Tataranni PA, Gautier JF, Chen K, Uecker A, Bandy D, Salbe AD, Pratley RE, Lawson M, Reiman EM, Ravussin E. Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography.  Proc Natl Acad Sci USA. 1999;  96 4569-4574
• 6 Small DM, Jones-Gotman M, Dagher A. Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers.  Neuroimage. 2003;  19 1709-1715
• 7 Odom JV, Bach M, Barber C, Brigell M, Marmor MF, Tormene AM, Holder G, Vaegan. Visual evoked potentials standard.  Doc Ophtalmol. 2004;  108 115-123
• 8 Greicius MD, Krasnow B, Reiss AL, Vinod-Menon V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis.  Proc Natl Acad Sci USA. 2003;  100 253-258
• 9 Bullier J. Integral model of visual processing.  Brain Res Rev. 2001;  36 96-107
• 10 Kötter R, Stephan KE, Palomero-Gallagher, Geyer S, Scheicher A, Zilles K. Multimodal characterization of cortical areas by multivariate analyses of receptor binding and connectivity data.  Anat Embryol. 2001;  204 333-350
• 11 Bosch-Bayard J, Valdés-Sosa P, Virues-Alba T, Aubert-Vazquez E, John ER, Harmony T, Riera-Diaz J, Trujillo-Barreto N. 3D statistical parametric mapping of EEG source spectra by means of variable resolution electromagnetic tomography (VARETA).  Clin Electroencephalogr. 2001;  32 47-61
• 12 Evans AC, Collins DL, Mills SR, Browm ED, Kelly RL, Peters TM. 3D statistical neuroanatomical model from 305 MRI volumes.  Proc. IEEE-Nuclear Sci Symp Med Imag Conf. 1993;  95 1813-1817
• 13 Holmes CJ, Hoge R, Collins L, Woods R, Toga AW, Evans AC. Enhancement of MR images using registration for signal averaging.  J Comput Assist Tomogr. 1998;  22 324-333
• 14 Fernández-Bouza A, Harmony T, Bosch J, Aubert E, Fernández T, Valdés P, Silva J, Marosi E, Martinez-Lopez M, Casian G. Source of abnormal EEG activity in the presence of brain lesions.  Clin Electroencephalogr. 1999;  30 1-7
• 15 Picton TW, Alain C, Woods DL, John MS, Scherg M, Valdes-Sosa P, Bosch-Bayard J, Trujillo NJ. Intracerebral sources of human auditory-evoked potentials.  Audiol Neurootol. 1999;  42 64-79
• 16 Prichep LS, John ER, Tom M. Localization of deep white matter lymphoma using VARETA: a case study.  Clin Electroencephalogr. 2001;  32 62-66
• 17 Müller MM, Picton TW, Valdes-Sosa P, Riera J, Teder Salejarvi WA, Hillyard SA. Effects of spatial selective attention on the steady-state visual evoked potential in the 20-28 Hz range.  Brain Res Cogn Brain Res. 1998;  6 249-261
• 18 Galán L, Biscay R, Rodriguez JL, Perez-Abalo MC, Rodríguez R. Testing topographic differences between event-related brain potencials by using non-parametric combinations of permutation tests.  Electroencephalogr Clin Neurophysiol. 1997;  102 240-247
• 19 González-Hernández JA, Pita-Alcorta C, Cedeño I, Díaz-Comas L, Figueredo-Rodriguez P. Abnormal functional asymmetry in occipital areas may prevent frontotemporal regions from achieving functional laterality during WCST performance in patients with schizophrenia.  Schizophr Res. 2003;  61 229-233
• 20 González-Hernández JA, Cedeño I, Pita-Alcorta C, Díaz-Comas L, Galán L, Figueredo-Rodriguez P. Dynamic event-related potentials and rapid source analysis reveals an intermittent short-lasting dysfrontality in schizophrenia.  Neuroimage. 2003;  19 1655-1663
• 21 Worsley KJ, Cao J, Paus T, Petrides M, Evans AC. Applications of random field theory to functional connectivity.  Hum Brain Mapp. 1998;  6 364-367
• 22 Worsley KJ, Taylor JE, Tomaiuolo F, Lerch J. Unified univariate and multivariate random field theory.  Neuroimage. 2004;  23 ((Suppl 1)) S189-S195
• 23 Gautier JF, Chen K, Uecker A, Bandy D, Frost J, Salbe AD, Pratley RE, Lawson M, Ravussin E, Reiman EM, Tataranni PA. Regions of the human brain affected during a liquid-meal taste perception in the fasting state: a positron emission tomography study.  Am J Clin Nutr. 1999;  70 806-810
• 24 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 1381-1394
• 25 González-Hernández JA, Céspedes-García Y, Campbell K, Scherbaum WA, Bosch-Bayard J, Figueredo-Rodriguez P. A pre-task resting condition neither baseline nor zero.  Neurosci Lett. 2005;  391 43-47
• 26 Del Parigi A, Chen K, Salbe AD, Gautier JF, Ravussin E, Reiman EM, Tataranni PA. Tasting a liquid meal after a prolonged fast is associated with preferential activation of the left hemisphere.  NeuroReport. 2002;  13 1141-1145
• 27 Gautier JF, Del Parigi A, Chen K, Salbe AD, Bandy D, Pratley RE, Ravussin E, Reiman EM, Tataranni PA. Effect of satiation on brain activity in obese and lean women.  Obes Res. 2001;  9 676-684
• 28 Karhunen LJ, Lappalainen RI, Vanninen EJ, Kuikka JT, Uusitupa MI. Regional cerebral blood flow during food exposure in obese and normal-weight women.  Brain. 1997;  120 1675-1684
• 29 Small DM, Zatorre RJ, Dagher A, Evans AC, Jones-Gotman M. Changes in brain activity related to eating chocolate: from pleasure to aversion.  Brain. 2001;  124 1720-1733
• 30 Corthout E, Uttl B, Ziemann U, Cowey A, Hallet M. Two periods of processing in the (circum) striate visual cortex as revealed by transcranial magnetic stimulation.  Neuropsychologia. 1999;  37 137-145
• 31 Livingstone MS, Hubel D. Segregation of form, color, movement and depth: anatomy, physiology and perception.  Science. 1998;  240 740-749
• 32 Di Russo F, Martínez A, Sereno M I, Pitzals S, Hillyard SA. Cortical sources of the early components of the visual evoked potential.  Hum Brain Mapping. 2001;  15 95-111
• 33 Di Russo F, Pitzalis S, Spitoni G, Aprile T, Patria F, Spinelli D, Hillyard SA. Identification of the neural sources of the pattern-reversal VEP.  Neuroimage. 2005;  24 874-886
• 34 Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. A default mode of brain function.  Proc Natl Acad Sci USA. 2001;  98 676-682
• 35 Shulman GL, Corbetta M, Buckner RL, Raichle ME, Fiez JA, Miezin FM, Petersen SE. Top-down modulation of early sensory cortex.  Cereb Cortex. 1997;  7 193-206

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