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Early‐Life Prebiotics Alter Exploratory Behavior, Recognition Memory, and Brain Serotonin in the Neonatal Piglet
Author(s) -
Fleming Stephen A,
Monaikul Supida,
Patsavas Alexander J,
Berg Brian M,
Waworuntu Rosaline V,
Dilger Ryan N
Publication year - 2017
Publication title -
the faseb journal
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.709
H-Index - 277
eISSN - 1530-6860
pISSN - 0892-6638
DOI - 10.1096/fasebj.31.1_supplement.650.22
Subject(s) - prebiotic , propionate , butyrate , medicine , endocrinology , zoology , biology , food science , biochemistry , fermentation
A prebiotic blend of polydextrose and galactooligoasaccaride (PDX‐GOS) represents a mixture of long‐ and short‐chain oligosaccharides. Emerging evidence in rodent models suggests dietary prebiotics are capable of modulating the gut microbiota and animal behavior. The present research set out to describe the effects of feeding PDX‐GOS early in life on cognition, exploratory behaviors and brain neurochemistry using a piglet model. Piglets were provided customized milk replacer containing 2 g/L each of PDX and GOS (TEST) or 0 g/L (CONT) from postnatal day (PND) 2–33. Beginning at PND 25, piglets were tested on the novel object recognition (NOR), novel location recognition, and tonic immobility tasks to measure recognition memory and response to restraint stress. At study conclusion, piglets were euthanized, and intestine and brain tissues were collected. No effects of diet were observed for lengths or weights of intestinal tissues ( P > 0.119). Concentrations of volatile fatty acids (acetate, propionate, butyrate) were decreased in the ascending colon of pigs in the TEST group ( P < 0.012), but unchanged in the cecum ( P > 0.383). Piglets consuming the TEST diet were able to demonstrate NOR after a 48 h delay ( P < 0.001), but piglets consuming the CONT diet could not ( P = 0.184). Additionally, piglets consuming the TEST diet visited both the novel and sample objects more frequently (all P < 0.05), spent less time per visit exploring the sample object ( P = 0.028), and exhibited greater total movement during the sample phase ( P < 0.001) than those on the CONT diet. Neither group was able to complete the novel location recognition task after a delay of 24 h (all P > 0.320), and there were no effects of diet observed for outcomes in the tonic immobility task (all P > 0.537). Concentrations of serotonin were lower ( P = 0.016) in the hippocampus of pigs fed the TEST diet and tended to be lower ( P = 0.055) in the striatum of those same pigs. These findings suggest that early‐life consumption of PDX‐GOS results in prebiotic effects in the ascending colon, subtly alters concentrations of catecholamines in the brain and supports recognition memory. We believe this is the first account of non‐digestible prebiotic fibers displaying simultaneous effects in the gut and brain of neonatal piglets. Such findings are likely the result of interactions within the gut‐microbiome‐brain axis, signifying dietary intervention as a possible mechanism to impact both gut and brain development and function in early life. Support or Funding Information This project was supported by Mead Johnson Nutrition.