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Consumption Of Fermented Milk Product With Probiotic Modulates Brain Activity.

K. Tillisch, J. Labus, L. Kilpatrick, Zhiguo Jiang, J. Stains, B. Ebrat, D. Guyonnet, S. Legrain-Raspaud, Beatrice Trotin, B. Naliboff, E. Mayer
Published 2013 · Medicine

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BACKGROUND & AIMS Changes in gut microbiota have been reported to alter signaling mechanisms, emotional behavior, and visceral nociceptive reflexes in rodents. However, alteration of the intestinal microbiota with antibiotics or probiotics has not been shown to produce these changes in humans. We investigated whether consumption of a fermented milk product with probiotic (FMPP) for 4 weeks by healthy women altered brain intrinsic connectivity or responses to emotional attention tasks. METHODS Healthy women with no gastrointestinal or psychiatric symptoms were randomly assigned to groups given FMPP (n = 12), a nonfermented milk product (n = 11, controls), or no intervention (n = 13) twice daily for 4 weeks. The FMPP contained Bifidobacterium animalis subsp Lactis, Streptococcus thermophiles, Lactobacillus bulgaricus, and Lactococcus lactis subsp Lactis. Participants underwent functional magnetic resonance imaging before and after the intervention to measure brain response to an emotional faces attention task and resting brain activity. Multivariate and region of interest analyses were performed. RESULTS FMPP intake was associated with reduced task-related response of a distributed functional network (49% cross-block covariance; P = .004) containing affective, viscerosensory, and somatosensory cortices. Alterations in intrinsic activity of resting brain indicated that ingestion of FMPP was associated with changes in midbrain connectivity, which could explain the observed differences in activity during the task. CONCLUSIONS Four-week intake of an FMPP by healthy women affected activity of brain regions that control central processing of emotion and sensation.
This paper references
10.1016/0165-1838(83)90129-7
Central connections of the sensory and motor nuclei of the vagus nerve.
P. Sawchenko (1983)
10.1016/0166-2236(94)90047-7
Columnar organization in the midbrain periaqueductal gray: modules for emotional expression?
R. Bandler (1994)
10.1016/0306-4522(94)90395-6
Convergence of deep somatic and visceral nociceptive information onto a discrete ventrolateral midbrain periaqueductal gray region
K. Keay (1994)
10.1136/gut.47.6.861
The neurobiology of stress and gastrointestinal disease
E. Mayer (2000)
10.1016/j.neuroimage.2004.07.020
Partial least squares analysis of neuroimaging data: applications and advances
A. McIntosh (2004)
10.1113/jphysiol.2004.063388
Postnatal microbial colonization programs the hypothalamic–pituitary–adrenal system for stress response in mice
N. Sudo (2004)
10.1016/j.neuroimage.2004.12.016
Stability of amygdala BOLD response to fearful faces over multiple scan sessions
T. Johnstone (2005)
10.1002/cne.20752
Intrinsic brain activity sets the stage for expression of motivated behavior
M. Raichle (2005)
10.1016/j.neuroimage.2005.12.050
Facial expressions and complex IAPS pictures: Common and differential networks
J. C. Britton (2006)
10.1111/j.1572-0241.2006.00734.x
Efficacy of an Encapsulated Probiotic Bifidobacterium infantis 35624 in Women with Irritable Bowel Syndrome
P. Whorwell (2006)
10.1136/gut.2005.066100
Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice
E. Verdu (2006)
10.1176/APPI.AJP.2007.07040609
Temporal stability of individual differences in amygdala reactivity.
S. Manuck (2007)
10.1093/JN/137.8.1901
Synergy between Lactobacillus paracasei and its bacterial products to counteract stress-induced gut permeability and sensitivity increase in rats.
H. Eutamene (2007)
10.3410/f.1087927.540874
Faculty Opinions recommendation of Putting feelings into words: affect labeling disrupts amygdala activity in response to affective stimuli.
K. Berridge (2007)
10.1016/j.bbi.2007.02.005
Infection-induced viscerosensory signals from the gut enhance anxiety: Implications for psychoneuroimmunology
L. Goehler (2007)
10.1038/nm1521
Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors
C. Rousseaux (2007)
10.1073/pnas.0711891105
Commensal microbiota is fundamental for the development of inflammatory pain
F. Amaral (2008)
10.1016/j.neuroimage.2008.03.009
Sex differences in brain activity during aversive visceral stimulation and its expectation in patients with chronic abdominal pain: A network analysis
J. Labus (2008)
Roles of short-chain fatty acids receptors, GPR41 and GPR43 on colonic functions.
H. Tazoe (2008)
10.1017/S0007114509990882
Fermented milk containing Bifidobacterium lactis DN-173 010 improves gastrointestinal well-being and digestive symptoms in women reporting minor digestive symptoms: a randomised, double-blind, parallel, controlled study
D. Guyonnet (2009)
10.1111/j.1365-2982.2009.01280.x
Lactobacillus farciminis treatment attenuates stress‐induced overexpression of Fos protein in spinal and supraspinal sites after colorectal distension in rats
A. Ait-Belgnaoui (2009)
10.1038/nri2515
The gut microbiota shapes intestinal immune responses during health and disease
J. Round (2009)
10.1038/nrgastro.2009.35
Principles and clinical implications of the brain–gut–enteric microbiota axis
S. Rhee (2009)
10.1016/j.rdc.2009.05.006
Abnormal pain modulation in patients with spatially distributed chronic pain: fibromyalgia.
R. Staud (2009)
10.1111/j.1365-2036.2008.03853.x
Clinical trial: the effects of a fermented milk product containing Bifidobacterium lactis DN‐173 010 on abdominal distension and gastrointestinal transit in irritable bowel syndrome with constipation
A. Agrawal (2009)
10.1111/j.1751-2980.2008.00366.x
Fermented milk containing Bifidobacterium lactis DN‐173 010 improved self‐reported digestive comfort amongst a general population of adults. A randomized, open‐label, controlled, pilot study
D. Guyonnet (2009)
10.1186/1757-4749-1-6
A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome
A. Rao (2009)
10.1073/pnas.0906186106
Prestimulus functional connectivity determines pain perception in humans
M. Ploner (2009)
10.1159/000268126
The Role of Pathogenic Microbes and Commensal Bacteria in Irritable Bowel Syndrome
S. Collins (2010)
10.1016/j.psychres.2008.05.006
The NimStim set of facial expressions: Judgments from untrained research participants
N. Tottenham (2009)
A randomized, doubleblind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome
(2009)
10.1111/j.1365-2982.2010.01520.x
The probiotic Bifidobacterium infantis 35624 displays visceral antinociceptive effects in the rat
D. McKernan (2010)
10.1016/j.bbr.2010.03.042
Intrinsic functional connectivity of the periaqueductal gray, a resting fMRI study
J. Kong (2010)
10.1053/j.gastro.2010.01.053
Short-chain fatty acids regulate the enteric neurons and control gastrointestinal motility in rats.
R. Soret (2010)
10.1172/JCI43766
Central modulation of pain.
M. Ossipov (2010)
10.1016/j.neuroscience.2010.04.072
I know the pain you feel—how the human brain's default mode predicts our resonance to another's suffering
A. Otti (2010)
10.1017/S0007114510004319
Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects
M. Messaoudi (2010)
10.1073/pnas.1000092107
Epithelial crosstalk at the microbiota–mucosal interface
J. Wells (2010)
10.1016/j.autneu.2009.07.007
Gut chemosensing: Interactions between gut endocrine cells and visceral afferents
H. Raybould (2010)
10.1007/s00213-010-1983-8
A single dose of mirtazapine modulates neural responses to emotional faces in healthy people
N. Rawlings (2010)
10.1126/scitranslmed.3002701
The Impact of a Consortium of Fermented Milk Strains on the Gut Microbiome of Gnotobiotic Mice and Monozygotic Twins
N. McNulty (2011)
10.1136/gutjnl-2011-300253
The balancing act: endogenous modulation of pain in functional gastrointestinal disorders
C. Wilder-Smith (2011)
10.3109/00365521.2011.584895
Dose-response effect of Bifidobacterium lactis HN019 on whole gut transit time and functional gastrointestinal symptoms in adults
Philip A Waller (2011)
10.1523/JNEUROSCI.4099-11.2011
The Placebo Effect: Advances from Different Methodological Approaches
K. Meissner (2011)
10.1016/j.nurt.2009.07.009
Preclinical and early clinical investigations related to monoaminergic pain modulation
K. Bannister (2009)
10.1007/s11010-011-1126-5
Antinociceptive effect of VSL#3 on visceral hypersensitivity in a rat model of irritable bowel syndrome: a possible action through nitric oxide pathway and enhance barrier function
C. Dai (2012)
10.1002/ana.22537
Altered functional magnetic resonance imaging resting‐state connectivity in periaqueductal gray networks in migraine
C. Mainero (2011)
10.1371/journal.pone.0023035
Intestinal Microbiota in Healthy Adults: Temporal Analysis Reveals Individual and Common Core and Relation to Intestinal Symptoms
J. Jalanka-Tuovinen (2011)
10.4161/gmic.2.4.16108
Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers
M. Messaoudi (2011)
10.1053/j.gastro.2011.04.052
The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice.
P. Bercik (2011)
10.1016/j.bbi.2010.11.010
Abdominal pain in Irritable Bowel Syndrome: A review of putative psychological, neural and neuro-immune mechanisms
S. Elsenbruch (2011)
10.1136/gutjnl-2011-301501
An irritable bowel syndrome subtype defined by species-specific alterations in faecal microbiota
I. Jeffery (2011)
10.1007/s10620-011-1730-y
Effects of Bifidobacterium infantis 35624 on Post-Inflammatory Visceral Hypersensitivity in the Rat
Anthony C Johnson (2011)
10.1111/j.1365-2982.2010.01620.x
Reduced anxiety‐like behavior and central neurochemical change in germ‐free mice
K. M. Neufeld (2011)
10.1111/j.1365-2982.2011.01796.x
The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut–brain communication
P. Bercik (2011)
10.1073/pnas.1010529108
Normal gut microbiota modulates brain development and behavior
R. D. Heijtz (2011)
10.1371/journal.pone.0027633
Personality Is Reflected in the Brain's Intrinsic Functional Architecture
Jonathan S. Adelstein (2011)
10.1038/nrn3071
Gut feelings: the emerging biology of gut–brain communication
E. Mayer (2011)
10.1073/pnas.1102999108
Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve
J. Bravo (2011)
10.1111/j.1365-2982.2010.01664.x
The microbiome‐gut‐brain axis: from bowel to behavior
J. Cryan (2011)
10.1096/fj.10-177980
Probiotics stimulate enterocyte migration and microbial diversity in the neonatal mouse intestine
Geoffrey A. Preidis (2012)
10.1016/j.neuroimage.2011.11.095
Neuroimaging of the periaqueductal gray: State of the field
C. Linnman (2012)
10.1038/nrn3346
Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour
J. Cryan (2012)
10.1126/science.1223490
Interactions Between the Microbiota and the Immune System
L. Hooper (2012)
10.1016/j.pain.2011.11.006
Sex similarities and differences in pain-related periaqueductal gray connectivity
C. Linnman (2012)
10.1111/j.1601-183X.2012.00786.x
Linking variability in brain chemistry and circuit function through multimodal human neuroimaging
P. Fisher (2012)
10.1126/science.1223813
Host-Gut Microbiota Metabolic Interactions
J. Nicholson (2012)
10.1371/journal.pone.0031951
Histamine Derived from Probiotic Lactobacillus reuteri Suppresses TNF via Modulation of PKA and ERK Signaling
Carissa M Thomas (2012)
10.1113/jphysiol.2011.219691
Role of innate immunity and the microbiota in liver fibrosis: crosstalk between the liver and gut
E. Seki (2012)
10.1021/pr200938v
Gut microbiota modulate the metabolism of brown adipose tissue in mice.
Renaud Mestdagh (2012)
10.1111/j.1365-2982.2011.01865.x
A marketed fermented dairy product containing Bifidobacterium lactis CNCM I‐2494 suppresses gut hypersensitivity and colonic barrier disruption induced by acute stress in rats
S. Agostini (2012)
- related periaqueductal gray connectivity
(2012)
Supplementary Table 4a
S. Bellone (2013)
Author names in bold designate shared co-first authorship
Sex similarities and differences in



This paper is referenced by
10.1016/j.pneurobio.2021.102208
From Alpha Diversity to Zzz: Interactions among sleep, the brain, and gut microbiota in the first year of life
S. Schoch (2021)
10.1016/b978-0-323-85170-1.00011-7
Food-gut microbiota interactions
K. Berding (2022)
10.1007/978-981-16-1626-6_20
Impact of Probiotics in Modulation of Gut Microbiome
R. Nourizadeh (2022)
10.1007/978-981-16-1626-6_11
Gut-Brain Axis: Probiotic Interactions and Implications for Human Mental Health
D. Gayathri (2022)
10.1016/j.pnpbp.2021.110468
Multimodal neuroimaging fusion biomarkers mediate the association between gut microbiota and cognition
Jiajia Zhu (2021)
10.1016/j.tifs.2021.12.035
Delving the role of nutritional psychiatry to mitigate the COVID-19 pandemic induced stress, anxiety and depression
M. Shabbir (2022)
10.1016/b978-0-323-85170-1.00001-4
Probiotics and the gut-brain axis
A. K. Silveira (2022)
10.1007/s00330-021-08486-5
Structural and functional neuroimaging of the effects of the gut microbiome
Rodrigo A. Montoro (2022)
10.3389/fnins.2021.613120
Interplay of Good Bacteria and Central Nervous System: Cognitive Aspects and Mechanistic Considerations
M. Salami (2021)
10.1002/0471266949.BMC297
The Gut Microbiome
Cassandra Francella (2021)
10.1016/j.bbi.2021.07.004
Kefir ameliorates specific microbiota-gut-brain axis impairments in a mouse model relevant to autism spectrum disorder
M. V. D. Wouw (2021)
10.3390/microorganisms10010091
Legumes and Legume-Based Beverages Fermented with Lactic Acid Bacteria as a Potential Carrier of Probiotics and Prebiotics
Patrycja Cichońska (2021)
10.1016/j.pnpbp.2020.110138
Emerging role of Gut-microbiota-brain axis in depression and therapeutic implication
Alper Evrensel (2020)
10.1016/j.arcmed.2021.03.002
Probiotics in Prevention and Treatment of COVID-19: Current Perspective and Future Prospects
Shilia Jacob Kurian (2021)
10.3390/nu13030927
Role of the Intestinal Microbiome, Intestinal Barrier and Psychobiotics in Depression
P. Trzeciak (2021)
10.3389/fnins.2021.804843
Interaction of Gut Microbiota and Brain Function in Patients With Chronic Insomnia: A Regional Homogeneity Study
Ying Feng (2022)
10.3390/microorganisms9061344
The Effect of Probiotics on Health Outcomes in the Elderly: A Systematic Review of Randomized, Placebo-Controlled Studies
A. N. Hutchinson (2021)
10.3390/nu13124542
A Fermented Milk Product Containing B. lactis CNCM I-2494 Improves the Tolerance of a Plant-Based Diet in Patients with Disorders of Gut–Brain Interactions
B. Nevé (2021)
10.1016/j.neubiorev.2021.06.032
The effect of probiotics on cognitive function across the human lifespan: A systematic review
J. Eastwood (2021)
10.3390/microorganisms9122518
Microorganisms as Shapers of Human Civilization, from Pandemics to Even Our Genomes: Villains or Friends? A Historical Approach
F. Rodríguez-Frías (2021)
10.1002/hbm.25419
Large‐scale functional network connectivity mediate the associations of gut microbiota with sleep quality and executive functions
Huanhuan Cai (2021)
10.1056/nejm193510312131814
Nutrition and Depression
N. Yılmaz (2021)
10.3390/foods10112639
Eating Fermented: Health Benefits of LAB-Fermented Foods
Vincenzo Castellone (2021)
10.3389/fnut.2021.790561
Bifidobacterium animalis subsp. lactis HN019 Effects on Gut Health: A Review
Jing Cheng (2021)
10.3389/fped.2021.690339
Evolution of Intestinal Microbiota of Asphyxiated Neonates Within 1 Week and Its Relationship With Neural Development at 6 Months
Xiaojiao Zhang (2021)
10.3390/ijms22062993
The Role of the Gut Microbiota in the Gut–Brain Axis in Obesity: Mechanisms and Future Implications
Jamie van Son (2021)
10.1007/s40520-021-01970-4
Dairy products and bone health
R. Rizzoli (2021)
10.3390/microorganisms9122532
Lactic Acid Bacteria-Fermentable Cereal- and Pseudocereal-Based Beverages.
M. Ziarno (2021)
10.1016/j.pnpbp.2020.110113
Microbiome and substances of abuse
M. Salavrakos (2020)
10.1021/ACSFOODSCITECH.0C00075
Dietary Influence on the Dynamics of the Human Gut Microbiome: Prospective Implications in Interventional Therapies
K. Adithya (2021)
10.1016/j.pharmthera.2021.107978
Probiotics: Potential novel therapeutics for microbiota-gut-brain axis dysfunction across gender and lifespan.
S. Snigdha (2021)
10.25259/SNI_72_2021
Targeting gut dysbiosis as a means to enhance recovery from surgical brain injury
S. Danehower (2021)
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