DISTURBANCE OF THE GUT MICROBIOTA IN EARLY-LIFE SELECTIVELY AFFECTS VISCERAL PAIN IN ADULTHOOD WITHOUT IMPACTING COGNITIVE OR ANXIETY-RELATED BEHAVIORS IN MALE RATS

Typeset version

 

TY  - JOUR
  - O'Mahony, SM,Felice, VD,Nally, K,Savignac, HM,Claesson, MJ,Scully, P,Woznicki, J,Hyland, NP,Shanahan, F,Quigley, EM,Marchesi, JR,O'Toole, PW,Dinan, TG,Cryan, JF
  - 2014
  - September
  - Neuroscience
  - DISTURBANCE OF THE GUT MICROBIOTA IN EARLY-LIFE SELECTIVELY AFFECTS VISCERAL PAIN IN ADULTHOOD WITHOUT IMPACTING COGNITIVE OR ANXIETY-RELATED BEHAVIORS IN MALE RATS
  - Validated
  - Altmetric: 15 ()
  - visceral pain brain-gut axis microbiota antibiotic neonatal behavior IRRITABLE-BOWEL-SYNDROME PROBIOTIC BIFIDOBACTERIUM-INFANTIS LACTOBACILLUS-REUTERI INGESTION INTESTINAL MICROBIOTA COLONIC HYPERSENSITIVITY MATERNAL SEPARATION ABDOMINAL-PAIN NERVOUS-SYSTEM ESTROUS-CYCLE RODENT MODEL
  - 277
  - 885
  - 901
  - Disruption of bacterial colonization during the early postnatal period is increasingly being linked to adverse health outcomes. Indeed, there is a growing appreciation that the gut microbiota plays a role in neurodevelopment. However, there is a paucity of information on the consequences of early-life manipulations of the gut microbiota on behavior. To this end we administered an antibiotic (vancomycin) from postnatal days 4-13 to male rat pups and assessed behavioral and physiological measures across all aspects of the brain-gut axis. In addition, we sought to confirm and expand the effects of early-life antibiotic treatment using a different antibiotic strategy (a cocktail of pimaricin, bacitracin, neomycin; orally) during the same time period in both female and male rat pups. Vancomycin significantly altered the microbiota, which was restored to control levels by 8 weeks of age. Notably, vancomycin-treated animals displayed visceral hypersensitivity in adulthood without any significant effect on anxiety responses as assessed in the elevated plus maze or open field tests. Moreover, cognitive performance in the Morris water maze was not affected by early-life dysbiosis. Immune and stress-related physiological responses were equally unaffected. The early-life antibiotic-induced visceral hypersensitivity was also observed in male rats given the antibiotic cocktail. Both treatments did not alter visceral pain perception in female rats. Changes in visceral pain perception in males were paralleled by distinct decreases in the transient receptor potential cation channel subfamily V member 1, the alpha-2A adrenergic receptor and cholecystokinin B receptor. In conclusion, a temporary disruption of the gut microbiota in early-life results in very specific and long-lasting changes in visceral sensitivity in male rats, a hallmark of stress-related functional disorders of the brain-gut axis such as irritable bowel disorder. (C) 2014 IBRO. Published by Elsevier Ltd. All rights reserved.
  - 10.1016/j.neuroscience.2014.07.054
DA  - 2014/09
ER  - 
@article{V279269132,
   = {O'Mahony,  SM and Felice,  VD and Nally,  K and Savignac,  HM and Claesson,  MJ and Scully,  P and Woznicki,  J and Hyland,  NP and Shanahan,  F and Quigley,  EM and Marchesi,  JR and O'Toole,  PW and Dinan,  TG and Cryan,  JF },
   = {2014},
   = {September},
   = {Neuroscience},
   = {DISTURBANCE OF THE GUT MICROBIOTA IN EARLY-LIFE SELECTIVELY AFFECTS VISCERAL PAIN IN ADULTHOOD WITHOUT IMPACTING COGNITIVE OR ANXIETY-RELATED BEHAVIORS IN MALE RATS},
   = {Validated},
   = {Altmetric: 15 ()},
   = {visceral pain brain-gut axis microbiota antibiotic neonatal behavior IRRITABLE-BOWEL-SYNDROME PROBIOTIC BIFIDOBACTERIUM-INFANTIS LACTOBACILLUS-REUTERI INGESTION INTESTINAL MICROBIOTA COLONIC HYPERSENSITIVITY MATERNAL SEPARATION ABDOMINAL-PAIN NERVOUS-SYSTEM ESTROUS-CYCLE RODENT MODEL},
   = {277},
  pages = {885--901},
   = {{Disruption of bacterial colonization during the early postnatal period is increasingly being linked to adverse health outcomes. Indeed, there is a growing appreciation that the gut microbiota plays a role in neurodevelopment. However, there is a paucity of information on the consequences of early-life manipulations of the gut microbiota on behavior. To this end we administered an antibiotic (vancomycin) from postnatal days 4-13 to male rat pups and assessed behavioral and physiological measures across all aspects of the brain-gut axis. In addition, we sought to confirm and expand the effects of early-life antibiotic treatment using a different antibiotic strategy (a cocktail of pimaricin, bacitracin, neomycin; orally) during the same time period in both female and male rat pups. Vancomycin significantly altered the microbiota, which was restored to control levels by 8 weeks of age. Notably, vancomycin-treated animals displayed visceral hypersensitivity in adulthood without any significant effect on anxiety responses as assessed in the elevated plus maze or open field tests. Moreover, cognitive performance in the Morris water maze was not affected by early-life dysbiosis. Immune and stress-related physiological responses were equally unaffected. The early-life antibiotic-induced visceral hypersensitivity was also observed in male rats given the antibiotic cocktail. Both treatments did not alter visceral pain perception in female rats. Changes in visceral pain perception in males were paralleled by distinct decreases in the transient receptor potential cation channel subfamily V member 1, the alpha-2A adrenergic receptor and cholecystokinin B receptor. In conclusion, a temporary disruption of the gut microbiota in early-life results in very specific and long-lasting changes in visceral sensitivity in male rats, a hallmark of stress-related functional disorders of the brain-gut axis such as irritable bowel disorder. (C) 2014 IBRO. Published by Elsevier Ltd. All rights reserved.}},
   = {10.1016/j.neuroscience.2014.07.054},
  source = {IRIS}
}
AUTHORSO'Mahony, SM,Felice, VD,Nally, K,Savignac, HM,Claesson, MJ,Scully, P,Woznicki, J,Hyland, NP,Shanahan, F,Quigley, EM,Marchesi, JR,O'Toole, PW,Dinan, TG,Cryan, JF
YEAR2014
MONTHSeptember
JOURNAL_CODENeuroscience
TITLEDISTURBANCE OF THE GUT MICROBIOTA IN EARLY-LIFE SELECTIVELY AFFECTS VISCERAL PAIN IN ADULTHOOD WITHOUT IMPACTING COGNITIVE OR ANXIETY-RELATED BEHAVIORS IN MALE RATS
STATUSValidated
TIMES_CITEDAltmetric: 15 ()
SEARCH_KEYWORDvisceral pain brain-gut axis microbiota antibiotic neonatal behavior IRRITABLE-BOWEL-SYNDROME PROBIOTIC BIFIDOBACTERIUM-INFANTIS LACTOBACILLUS-REUTERI INGESTION INTESTINAL MICROBIOTA COLONIC HYPERSENSITIVITY MATERNAL SEPARATION ABDOMINAL-PAIN NERVOUS-SYSTEM ESTROUS-CYCLE RODENT MODEL
VOLUME277
ISSUE
START_PAGE885
END_PAGE901
ABSTRACTDisruption of bacterial colonization during the early postnatal period is increasingly being linked to adverse health outcomes. Indeed, there is a growing appreciation that the gut microbiota plays a role in neurodevelopment. However, there is a paucity of information on the consequences of early-life manipulations of the gut microbiota on behavior. To this end we administered an antibiotic (vancomycin) from postnatal days 4-13 to male rat pups and assessed behavioral and physiological measures across all aspects of the brain-gut axis. In addition, we sought to confirm and expand the effects of early-life antibiotic treatment using a different antibiotic strategy (a cocktail of pimaricin, bacitracin, neomycin; orally) during the same time period in both female and male rat pups. Vancomycin significantly altered the microbiota, which was restored to control levels by 8 weeks of age. Notably, vancomycin-treated animals displayed visceral hypersensitivity in adulthood without any significant effect on anxiety responses as assessed in the elevated plus maze or open field tests. Moreover, cognitive performance in the Morris water maze was not affected by early-life dysbiosis. Immune and stress-related physiological responses were equally unaffected. The early-life antibiotic-induced visceral hypersensitivity was also observed in male rats given the antibiotic cocktail. Both treatments did not alter visceral pain perception in female rats. Changes in visceral pain perception in males were paralleled by distinct decreases in the transient receptor potential cation channel subfamily V member 1, the alpha-2A adrenergic receptor and cholecystokinin B receptor. In conclusion, a temporary disruption of the gut microbiota in early-life results in very specific and long-lasting changes in visceral sensitivity in male rats, a hallmark of stress-related functional disorders of the brain-gut axis such as irritable bowel disorder. (C) 2014 IBRO. Published by Elsevier Ltd. All rights reserved.
PUBLISHER_LOCATION
ISBN_ISSN
EDITION
URL
DOI_LINK10.1016/j.neuroscience.2014.07.054
FUNDING_BODY
GRANT_DETAILS