Different Food Odors Control Brain Connectivity in Impulsive Children

Author(s): Benito de Celis-Alonso*, Silvia S. Hidalgo-Tobón, Eduardo Barragán-Pérez, Eduardo Castro-Sierra, Pilar Dies-Suárez, Julio Garcia, Eduardo Moreno-Barbosa, Oscar Arias-Carrión*.

Journal Name: CNS & Neurological Disorders - Drug Targets

Volume 18 , Issue 1 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Background: Impulsivity is a complex multi-dimensional combination of behaviors which include: ineffective impulse control, premature decision-making and inability to delay gratification.

Objective: The aim of this work was to explore how food odor perception and its emotional value is affected in impulsive children.

Methods: Here we compared two cohorts of impulsive and control children with ages between 10 and 16 years. Both groups underwent a functional magnetic resonance imaging experiment, in which foodrelated odor-cues were presented to all of them.

Results: Differences in regions of blood oxygen level dependent activation, as well as connectivity, were calculated. Activations were significant for all odors in the impulsive group in the temporal lobe, cerebellum, supplementary motor area, frontal cortex, medial cingulate cortex, insula, precuneus, precentral, para-hippocampal and calcarine cortices.

Conclusion: Connectivity results showed that the expected emotional reward, based on odor perceived and processed in temporal lobes, was the main cue driving responses of impulsive children. This was followed by self-consciousness, the sensation of interaction with the surroundings and feelings of comfort and happiness, modulated by the precuneus together with somatosensory cortex and cingulum. Furthermore, reduced connectivity to frontal areas as well as to other sensory integration areas (piriform cortex), combined to show different sensory processing strategies for olfactory emotional cues in impulsive children. Finally, we hypothesize that the cerebellum plays a pivotal role in modulating decision-making for impulsive children.

Keywords: Olfaction, children, impulsivity, obesity, fMRI, connectivity.

[1]
Kalenscher TT, Ohmann O. The neuroscience of impulsive and self-controlled decisions. Int J Psychophysiol 2006; 62(2): 203-11.
[2]
Evenden JL. Varieties of impulsivity. Psychopharmacology 1999; 146(4): 348-61.
[3]
McDonald V. Networks underlying trait impulsivity: Evidence from voxel-based lesion-symptom mapping. Hum Brain Mapp 2017; 38(2): 656-65.
[4]
Whelan R. Adolescent impulsivity phenotypes characterized by distinct brain networks. Nat Neurosci 2012; 15(6): 920-5.
[5]
Crone EA. Executive functions in adolescence: Inferences from brain and behavior. Dev Sci 2009; 12(6): 825-30.
[6]
Neville KR, Lewis BH. The synaptic organization of the brain. olfactory cortex. 5th Ed. 2004: Oxford Univeristy Press.
[7]
Bear MF, Connors BW, Paradiso MA. Neuroscience exploring the brain. 3rd Ed. 2007: Lippincot williams & Wilkins.
[8]
Kose S. Neural correlates of impulsive aggressive behavior in subjects with a history of alcohol dependence. Behav Neurosci 2015; 129(2): 183-96.
[9]
Rusnakova S. The executive functions in frontal and temporal lobes: A flanker task intracerebral recording study. J Clin Neurophysiol 2011; 28(1): 30-5.
[10]
Waxman SE. A systematic review of impulsivity in eating disorders. Eur Eat Disord Rev 2009; 17(6): 408-25.
[11]
Fahy T, Eisler I. Impulsivity and eating disorders. Br J Psychiatry 1993; 162: 193-7.
[12]
Perry JL, Carroll ME. The role of impulsive behavior in drug abuse. Psychopharmacology 2008; 200(1): 1-26.
[13]
Dick DM. Understanding the construct of impulsivity and its relationship to alcohol use disorders. Addict Biol 2010; 15(2): 217-26.
[14]
Potenza MN, de Wit H. Control yourself: Alcohol and impulsivity. Alcohol Clin Exp Res 2010; 34(8): 1303-5.
[15]
Hodgins DC, Holub A. Components of impulsivity in gambling disorder. Int J Ment Health Addict 2015; 13(6): 699-711.
[16]
Chamorro J. Impulsivity in the general population: A national study. J Psychiatr Res 2012; 46(8): 994-1001.
[17]
Palili A. Inattention, hyperactivity, impulsivity-epidemiology and correlations: A nationwide greek study from birth to 18 years. J Child Neurol 2011; 26(2): 199-204.
[18]
Best M, Williams JM, Coccaro EF. Evidence for a dysfunctional prefrontal circuit in patients with an impulsive aggressive disorder. Proc Natl Acad Sci USA 2002; 99(12): 8448-53.
[19]
Yeomans MR. Olfactory influences on appetite and satiety in humans. Physiol Behav 2006; 89(1): 10-4.
[20]
Tetley A, Brunstrom J, Griffiths P. Individual differences in food-cue reactivity. The role of BMI and everyday portion-size selections. Appetite 2009; 52(3): 614-20.
[21]
Heinz A. Alcohol craving and relapse prediction: Imaging studies, in advances in the neuroscience of addiction, C.M. Kuhn and G.F. Koob, Editors. 2010: Boca Raton (FL).
[22]
Bragulat V. Food-related odor probes of brain reward circuits during hunger: A pilot FMRI study. Obesity (Silver Spring) 2010; 18(8): 1566-71.
[23]
Burton AC. Previous cocaine self-administration disrupts reward expectancy encoding in ventral striatum. Neuropsychopharmacology 2018; 43(12): 2350-60.
[24]
Cortese BM. The fMRI BOLD response to unisensory and multisensory smoking cues in nicotine-dependent adults. Psychiatry Res 2015; 234(3): 321-7.
[25]
Eiler WJ. Ventral frontal satiation-mediated responses to food aromas in obese and normal-weight women. Am J Clin Nutr 2014; 99(6): 1309-18.
[26]
Cyders MA. Negative urgency and ventromedial prefrontal cortex responses to alcohol cues: FMRI evidence of emotion-based impulsivity. Alcohol Clin Exp Res 2014; 38(2): 409-17.
[27]
Biswal BB. Resting state fMRI: A personal history. Neuroimage 2012; 62(2): 938-44.
[28]
Chodkowski BA, Cowan RL, Niswender KD. Imbalance in resting state functional connectivity is associated with eating behaviors and adiposity in children. Heliyon 2016; 2(1): e00058.
[29]
Inuggi A. Brain functional connectivity changes in children that differ in impulsivity temperamental trait. Front Behav Neurosci 2015; 6(8): 156.
[30]
Kollndorfer K. Recovery of olfactory function induces neuroplasticity effects in patients with smell loss. Neural Plast 2014; 2014: 140419.
[31]
Kollndorfer K. Effects of chronic peripheral olfactory loss on functional brain networks. Neuroscience 2015; 310: 589-99.
[32]
Larsen JK, Hermans RC, Engels RC. Food intake in response to food-cue exposure. Examining the influence of duration of the cue exposure and trait impulsivity. Appetite 2012; 58(3): 907-13.
[33]
Ogawa S. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 1990; 87(24): 9868-72.
[34]
Xu T. Network analysis of functional brain connectivity in borderline personality disorder using resting-state fMRI. Neuroimage Clin 2016; 11: 302-15.
[35]
Faul FG. *Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 2007; 39(2): 175-91.
[36]
Newman JP, Widom CS, Nathan S. Passive avoidance in syndromes of disinhibition: Psychopathy and extraversion. J Pers Soc Psychol 1985; 48(5): 1316-27.
[37]
Yechiam E. A formal cognitive model of the go/no-go discrimination task: Evaluation and implications. Psychol Assess 2006; 18(3): 239-49.
[38]
Kindlon DE, Mezzacappa J, Earls F. Psychometric properties of impulsivity measures: Temporal stability, validity and factor structure. J Child Psychol Psychiatry 1995; 36(4): 645-61.
[39]
Jonkman LM, Lansbergen M, Stauder JE. Developmental differences in behavioral and event-related brain responses associated with response preparation and inhibition in a go/nogo task. Psychophysiology 2003; 40(5): 752-61.
[40]
Menon V. Error-related brain activation during a Go/NoGo response inhibition task. Hum Brain Mapp 2001; 12(3): 131-43.
[41]
Di Marco B. Neuro-inflammatory mechanisms in developmental disorders associated with intellectual disability and autism spectrum disorder: A neuro- immune perspective. CNS Neurol Disord Drug Targets 2016; 15(4): 448-63.
[42]
Doty RL. University of pennsylvania smell identification test: A rapid quantitative olfactory function test for the clinic. Laryngoscope 1984; 94(2 Pt 1): 176-8.
[43]
Wolz I. Subjective craving and event-related brain response to olfactory and visual chocolate cues in binge-eating and healthy individuals. Sci Rep 2017; 7: 41736.
[44]
Schulte EM, Avena NM, Gearhardt AN. Which foods may be addictive? The roles of processing, fat content, and glycemic load. PLoS One 2015; 10(2): e0117959.
[45]
Hellman TM. Small, Characterization of the odor properties of 101 petrochemicals using sensory methods. J Air Pollut Control Assoc 1974; 24(10): 979-82.
[46]
Dravnieks AT, Masurat S, Lamm RA. Hedonics of odors and odor descriptors. J Air Pollut Control Assoc 1984; 34(7): 4.
[47]
Schulze P. Preprocessing of emotional visual information in the human piriform cortex. Sci Rep 2017; 7(1): 9191.
[48]
Distel H. Perception of everyday odors-correlation between intensity, familiarity and strength of hedonic judgement. Chem Senses 1999; 24(2): 191-9.
[49]
Guerrero AC. Strategies for tonal and atonal musical interpretation in blind and normally sighted children: An fMRI study. Brain Behav 2016; 6(4): e00450.
[50]
Alonso BC. A multi-methodological MR resting state network analysis to assess the changes in brain physiology of children with ADHD. PLoS One 2014; 9(6): e99119.
[51]
Power JD. Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage 2014; 84: 320-41.
[52]
Mazaika PK, Whitfield S, Cooper JC. Detection and repair of transient artifacts in fMRI data. Neuroimage 2005; 26: e36.
[53]
Mersov AM. Estimating the sample size required to detect an arterial spin labelling magnetic resonance imaging perfusion abnormality in voxel-wise group analyses. J Neurosci Methods 2015; 245: 169-77.
[54]
Mainland, J. and M. Sobel, The Sniff Is Part of the Olfactory Percep. Chem Senses 2006; 31: 15.
[55]
Sobel N. Odorant-induced and sniff-induced activation in the cerebellum of the human. J Neurosci 1998; 18(21): 8990-9001.
[56]
Oh TS. Hypothalamic AMP-activated protein kinase as a regulator of food intake and energy balance. CNS Neurol Disord Drug Targets 2016; 15(8): 13.
[57]
Sun Y. Preventive and protective roles of dietary Nrf2 activators against central nervous system diseases. CNS Neurol Disord Drug Targets 2017; 16(3): 326-38.
[58]
Caballero-Villarraso J. Interrelationships among gut microbiota and host: Paradigms, role in neurodegenerative diseases and future prospects. CNS Neurol Disord Drug Targets 2017; 16(8): 945-64.
[59]
Andrews-Hanna JR. Cognitive control in adolescence: Neural underpinnings and relation to self-report behaviors. PLoS One 2011; 6(6): e21598.
[60]
Zhang S, Li CS. Functional connectivity mapping of the human precuneus by resting state fMRI. Neuroimage 2012; 59(4): 3548-62.
[61]
Margulies DS. Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci USA 2009; 106(47): 20069-74.
[62]
Utevsky AV, Smith DV, Scott A. Precuneus is a functional core of the default-mode network. J Neurosci 2014; 34(3): 8.
[63]
Ul Huque AE, Poliakoff RJ. Effects of learning on somatosensory decision-making and experiences. J Exp Psychol Gen 2017; 146(11): 1631-48.
[64]
Borich MR. Understanding the role of the primary somatosensory cortex: Opportunities for rehabilitation. Neuropsychologia 2015; 79(Pt B): 246-55.
[65]
Sato W. The structural neural substrate of subjective happiness. Sci Rep 2015; 5: 16891.
[66]
Mouly AM, Sullivan R. Memory and plasticity in the olfactory system: From infancy to adulthood, in the neurobiology of olfaction. A. Menini, Editor. 2010: Boca Raton (FL).
[67]
Desai M. Olfactory abnormalities in temporal lobe epilepsy. J Clin Neurosci 2015; 22(10): 1614-8.
[68]
Berridge KC, Kringelbach ML. Affective neuroscience of pleasure: Reward in humans and animals. Psychopharmacology 2008; 199(3): 457-80.
[69]
Neubert FX. Connectivity reveals relationship of brain areas for reward-guided learning and decision making in human and monkey frontal cortex. Proc Natl Acad Sci USA 2015; 112(20): E2695-704.
[70]
Gottfried JA. Central mechanisms of odour object perception. Nat Rev Neurosci 2010; 11(9): 628-41.
[71]
Jiao Z. Functional connectivity analysis of brain default mode networks using hamiltonian path CNS Neurol Disord Drug Target 2017 16(1): 44-50.
[72]
Leech R, Sharp DJ. The role of the posterior cingulate cortex in cognition and disease. Brain 2014; 137(Pt 1): 12-32.
[73]
Brewer JA, Garrison KA, Whitfield-Gabrieli S. What about the “self” is processed in the posterior cingulate cortex? Front Hum Neurosci 2013; 7: 647.
[74]
Moers-Hornikx VM. Cerebellar nuclei are involved in impulsive behaviour. Behav Brain Res 2009; 203(2): 256-63.
[75]
Blackwood N. The cerebellum and decision making under uncertainty. Brain Res Cogn Brain Res 2004; 20(1): 46-53.
[76]
Schmahmann JD. The cerebellum and cognition. International Review of Neurobiology, ed. S.J. Bradley, A. Adron Harris, and P. jenner. Vol. 41. 1997, San Diego: Academic Press.
[77]
Small DM. Flavor processing: More than the sum of its parts. Neuroreport 1997; 22(8): 4.
[78]
Savic I. Processing of odorous signals in humans. Brain Res Bull 2001; 54(3): 307-12.
[79]
O’Reilly JX. Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cereb Cortex 2010; 20(4): 953-65.


Rights & PermissionsPrintExport Cite as


Article Details

VOLUME: 18
ISSUE: 1
Year: 2019
Page: [63 - 77]
Pages: 15
DOI: 10.2174/1871527317666181105105113
Price: $58

Article Metrics

PDF: 26
HTML: 2
PRC: 1