Treating Generational Stress: Effect of Paternal Stress on Development of Memory and Extinction in Offspring Is Reversed by Probiotic Treatment

Psychological Science

Volumn 27, Issue 9, 2016, Pages 1171-1180

  Callaghan, Bridget L ^a,b,c   Cowan, Caitlin S M ^a   Richardson, Rick ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b Columbia University ^*  (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

extinction; generational effects; infantile amnesia; inheritance; maternal separation; Pavlovian conditioning; probiotic

Indexed keywords

PROBIOTIC AGENT;

AMNESIA; ANIMAL; BRAIN; DRUG EFFECTS; EPIDEMIOLOGY; FEMALE; HUMAN; JURISPRUDENCE; MALE; MATERNAL DEPRIVATION; MEMORY; MENTAL STRESS; PHYSIOLOGY; PSYCHOLOGY; RAT; SPRAGUE DAWLEY RAT;

AMNESIA; ANIMALS; BRAIN; COHORT EFFECT; FEMALE; HUMANS; MALE; MATERNAL DEPRIVATION; MEMORY; PROBIOTICS; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL; WILLS;

EID: 84986275957     PISSN: 09567976     EISSN: 14679280     Source Type: Journal    
DOI: 10.1177/0956797616653103     Document Type: Article

References (40)

1. E.BarrettR.P.RossP.W.O’TooleG.F.FitzgeraldC.Stanton (2012). γ-Aminobutyric acid production by culturable bacteria from the human intestine. Journal of Applied Microbiology, 113, 411–417.
2. N.A.BroderickN.BuchonB.Lemaitre (2014). Microbiota-induced changes in Drosophila melanogaster host gene expression and gut morphology. mBio, 5(3), Article e01117-14. doi:10.1128/mBio.01117-14
3. B.L.CallaghanS.LiR.Richardson (2014). The elusive engram: What can infantile amnesia tell us about memory?Trends in Neurosciences, 37, 47–53.
4. B.L.CallaghanR.Richardson (2011). Maternal separation results in early emergence of adult-like fear and extinction learning in infant rats. Behavioral Neuroscience, 125, 20–28.
5. B.L.CallaghanR.Richardson (2012a). Adverse rearing environments and persistent memories in rats: Removing the brakes on infant fear memory. Translational Psychiatry, 2, Article e138. doi:10.1038/tp.2012.65
6. B.L.CallaghanR.Richardson (2012b). Early-life stress affects extinction during critical periods of development: An analysis of the effects of maternal separation on extinction in adolescent rats. Stress, 15, 671–679.
7. B.L.CallaghanR.Richardson (2013). Early experiences and the development of emotional learning systems in rats. Biology of Mood & Anxiety Disorders, 3, Article 8. doi:10.1186/2045-5380-3-8
8. B.L.CallaghanR.Richardson (2014). Early emergence of adult-like fear renewal in the developing rat after chronic corticosterone treatment of the dam or the pups. Behavioral Neuroscience, 128, 594–602.
9. B.A.CampbellN.E.Spear (1972). Ontogeny of memory. Psychological Review, 79, 215–236.
10. D.K.ChitkaraM.A.L.van TilburgN.Blois-MartinW.E.Whitehead (2008). Early life risk factors that contribute to irritable bowel syndrome in adults: A systematic review. American Journal of Gastroenterology, 103, 765–774.
11. C.S.M.CowanB.L.CallaghanJ.M.KanR.Richardson (2016). The lasting impact of early-life adversity on individuals and their descendants: Potential mechanisms and hope for intervention. Genes, Brain and Behavior, 15, 155–168.
12. C.S.M.CowanB.L.CallaghanR.Richardson (2013). Acute early-life stress results in premature emergence of adult-like fear retention and extinction relapse in infant rats. Behavioral Neuroscience, 127, 703–711.
13. C.S.M.CowanB.L.CallaghanR.Richardson (2016). The effects of a probiotic formulation (Lactobacillus rhamnosus and L. helveticus) on developmental trajectories of emotional learning in stressed infant rats. Translational Psychiatry, 6, Article e823. doi:10.1038/tp.2016.94
14. J.P.CurleyR.MashoodhF.A.Champagne (2011). Epigenetics and the origins of paternal effects. Hormones and Behavior, 59, 306–314.
15. G.De PalmaP.BlennerhassettJ.LuY.DengA.J.ParkW.GreenP.. Bercik. (2015). Microbiota and host determinants of behavioural phenotype in maternally separated mice. Nature Communications, 6, Article 7735. doi:10.1038/ncomms8735
16. B.G.DiasK.J.Ressler (2014). Parental olfactory experience influences behavior and neural structure in subsequent generations. Nature Neuroscience, 17, 89–96.
17. D.M.DietzQ.LaPlantE.L.WattsG.E.HodesS.J.RussoJ.FengE.J.. Nestler (2011). Paternal transmission of stress-induced pathologies. Biological Psychiatry, 70, 408–414.
18. W.D.FellowsK.M.Rasmussen (1984). Comparison of methods for obtaining milk samples from well-nourished and malnourished rats. Physiology & Behavior, 33, 761–763.
19. L.M.FosterT.A.TompkinsW.J.Dahl (2011). A comprehensive post-market review of studies on a probiotic product containing Lactobacillus helveticus R0052 and Lactobacillus rhamnosus R0011. Beneficial Microbes, 2, 319–334.
20. T.B.FranklinH.RussigI.C.WeissJ.GräffN.LinderA.MichalonI.M.. Mansuy (2010). Epigenetic transmission of the impact of early stress across generations. Biological Psychiatry, 68, 408–415.
21. S.B.FreedmanS.Williamson-UrquhartS.SchuhP.M.ShermanK.J.FarionS.GouinM.H.. Gorelick (2014). Impact of emergency department probiotic treatment of pediatric gastroenteritis: Study protocol for the PROGUT (Probiotic Regimen for Outpatient Gastroenteritis Utility of Treatment) randomized controlled trial. Trials, 15, Article 170. doi:10.1186/1745-6215-15-170
22. K.GappA.JawaidP.SarkiesJ.BohacekP.PelczarJ.PradosI.M.. Mansuy (2014). Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nature Neuroscience, 17, 667–669.
23. M.G.GareauJ.JuryG.MacQueenP.M.ShermanM.H.Perdue (2007). Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut, 56, 1522–1528.
24. J.K.GoodrichJ.L.WatersA.C.PooleJ.L.SutterO.KorenR.BlekhmanR.E.. Ley (2014). Human genetics shape the gut microbiota. Cell, 159, 789–799.
25. M.S.GoyalS.VenkateshJ.MilbrandtJ.I.GordonM.E.Raichle (2015). Feeding the brain and nurturing the mind: Linking nutrition and the gut microbiota to brain development. Proceedings of the National Academy of Sciences, USA, 112, 14105–14112.
26. M.B.HennessyN.P.StaffordB.Yusko-OsborneP.A.SchimlE.D.XanthosT.Deak (2015). Naproxen attenuates sensitization of depressive-like behavior and fever during maternal separation. Physiology & Behavior, 139, 34–40.
27. R.L.HuotK.ThrivikramanM.J.MeaneyP.M.Plotsky (2001). Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology, 158, 366–373.
28. E.JašarevicćC.L.HowertonC.D.HowardT.L.Bale (2015). Alterations in the vaginal microbiota by maternal stress are associated with metabolic reprogramming of the offspring gut and brain. Endocrinology, 156, 3265–3276.
29. M.KalinichevK.W.EasterlingP.M.PlotskyS.G.Holtzman (2002). Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long–Evans rats. Pharmacology Biochemistry & Behavior, 73, 131–140.
30. H.K.KimD.M.CapaldiK.C.PearsD.C.R.KerrL.D.Owen (2009). Intergenerational transmission of internalising and externalising behaviours across three generations: Gender-specific pathways. Criminal Behaviour and Mental Health, 19, 125–141.
31. J.H.KimR.Richardson (2010). New findings on extinction of conditioned fear early in development: Theoretical and clinical implications. Biological Psychiatry, 67, 297–303.
32. S.J.LupienB.S.McEwenM.R.GunnarC.Heim (2009). Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience, 10, 434–445.
33. A.ParasharM.Udayabanu (2016). Gut microbiota regulates key modulators of social behavior. European Neuropsychopharmacology, 26, 78–91.
34. R.L.RepettiS.E.TaylorT.E.Seeman (2002). Risky families: Family social environments and the mental and physical health of offspring. Psychological Bulletin, 128, 330–366.
35. R.M.StillingF.J.RyanA.E.HobanF.ShanahanG.ClarkeM.J.ClaessonJ.F.. Cryan (2015). Microbes & neurodevelopment—absence of microbiota during early life increases activity-related transcriptional pathways in the amygdala. Brain, Behavior, and Immunity, 50, 209–220.
36. K.TillischJ.LabusL.KilpatrickZ.JiangJ.StainsB.EbratE.A.. Mayer (2013). Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology, 144, 1394–1401.
37. C.S.WidomS.J.CzajaT.BentleyM.S.Johnson (2012). A prospective investigation of physical health outcomes in abused and neglected children: New findings from a 30-year follow-up. American Journal of Public Health, 102, 1135–1144.
38. J.M.YanoK.YuG.P.DonaldsonG.G.ShastriP.AnnL.MaE.Y.. Hsiao (2015). Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell, 161, 264–276.
39. R.YehudaA.BellL.M.BiererJ.Schmeidler (2008). Maternal, not paternal, PTSD is related to increased risk for PTSD in offspring of Holocaust survivors. Journal of Psychiatric Research, 42, 1104–1111.
40. M.A.ZijlmansK.KorpelaJ.M.Riksen-WalravenW.M.de VosC.de Weerth (2015). Maternal prenatal stress is associated with the infant intestinal microbiota. Psychoneuroendocrinology, 53, 233–245.