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Dissociable Behavioral, Physiological and Neural Effects of Acute Glucose and Fructose Ingestion: A Pilot Study.

Wölnerhanssen BK, Meyer-Gerspach AC, Schmidt A, Zimak N, Peterli R, Beglinger C, Borgwardt S - PLoS ONE (2015)

Bottom Line: Glucose ingestion induced significantly greater elevations in plasma glucose, insulin, GLP-1 and GIP, while feelings of fullness increased and prospective food consumption decreased relative to fructose.Our findings suggest that glucose and fructose induce dissociable effects on rsFC within the basal ganglia/limbic network, which are probably mediated by different insulin levels.A larger study would be recommended in order to confirm these findings.

View Article: PubMed Central - PubMed

Affiliation: Department of Gastroenterology, University Hospital of Basel, Basel, Switzerland.

ABSTRACT
Previous research has revealed that glucose and fructose ingestion differentially modulate release of satiation hormones. Recent studies have begun to elucidate brain-gut interactions with neuroimaging approaches such as magnetic resonance imaging (MRI), but the neural mechanism underlying different behavioral and physiological effects of glucose and fructose are unclear. In this paper, we have used resting state functional MRI to explore whether acute glucose and fructose ingestion also induced dissociable effects in the neural system. Using a cross-over, double-blind, placebo-controlled design, we compared resting state functional connectivity (rsFC) strengths within the basal ganglia/limbic network in 12 healthy lean males. Each subject was administered fructose, glucose and placebo on three separate occasions. Subsequent correlation analysis was used to examine relations between rsFC findings and plasma concentrations of satiation hormones and subjective feelings of appetite. Glucose ingestion induced significantly greater elevations in plasma glucose, insulin, GLP-1 and GIP, while feelings of fullness increased and prospective food consumption decreased relative to fructose. Furthermore, glucose increased rsFC of the left caudatus and putamen, precuneus and lingual gyrus more than fructose, whereas within the basal ganglia/limbic network, fructose increased rsFC of the left amygdala, left hippocampus, right parahippocampus, orbitofrontal cortex and precentral gyrus more than glucose. Moreover, compared to fructose, the increased rsFC after glucose positively correlated with the glucose-induced increase in insulin. Our findings suggest that glucose and fructose induce dissociable effects on rsFC within the basal ganglia/limbic network, which are probably mediated by different insulin levels. A larger study would be recommended in order to confirm these findings.

No MeSH data available.


Related in: MedlinePlus

(A) Correlations between resting state functional connectivity, insulin release and subjective appetite perception. In relation to placebo, the glucose-induced increase in functional connectivity strength (parameter estimates; PE) within the basal ganglia/limbic network correlated positively with the glucose-induced insulin release (μU/mL) (r = 0.62, p = 0.03). (B) Relative to fructose, the glucose-induced increase in functional connectivity strength within basal ganglia/limbic network correlated positively with and the glucose-induced insulin release (r = 0.65, p = 0.02). (C) In relation to placebo, the fructose-induced increase in functional connectivity strength within the basal ganglia/limbic network correlated positively at trend level with the fructose-induced feeling of hunger (r = 0.57, p = 0.069).
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pone.0130280.g006: (A) Correlations between resting state functional connectivity, insulin release and subjective appetite perception. In relation to placebo, the glucose-induced increase in functional connectivity strength (parameter estimates; PE) within the basal ganglia/limbic network correlated positively with the glucose-induced insulin release (μU/mL) (r = 0.62, p = 0.03). (B) Relative to fructose, the glucose-induced increase in functional connectivity strength within basal ganglia/limbic network correlated positively with and the glucose-induced insulin release (r = 0.65, p = 0.02). (C) In relation to placebo, the fructose-induced increase in functional connectivity strength within the basal ganglia/limbic network correlated positively at trend level with the fructose-induced feeling of hunger (r = 0.57, p = 0.069).

Mentions: Exploratory correlation analysis showed that the increased rsFC within the basal ganglia/limbic network induced by glucose relative to placebo correlated positively with the insulin level after glucose ingestion (r = 0.62, p = 0.03), as the glucose-induced effect on rsFC relative to fructose (r = 0.65, p = 0.02; Fig 6A and 6B, uncorrected for multiple testing). Moreover, there was a trend between the fructose-induced effect within the basal ganglia network relative to placebo and the fructose-induced feelings of hunger (r = 0.57, p = 0.069; Fig 6C, uncorrected for multiple testing). No other significant correlations between resting state data, behavioral and physiological parameters were found.


Dissociable Behavioral, Physiological and Neural Effects of Acute Glucose and Fructose Ingestion: A Pilot Study.

Wölnerhanssen BK, Meyer-Gerspach AC, Schmidt A, Zimak N, Peterli R, Beglinger C, Borgwardt S - PLoS ONE (2015)

(A) Correlations between resting state functional connectivity, insulin release and subjective appetite perception. In relation to placebo, the glucose-induced increase in functional connectivity strength (parameter estimates; PE) within the basal ganglia/limbic network correlated positively with the glucose-induced insulin release (μU/mL) (r = 0.62, p = 0.03). (B) Relative to fructose, the glucose-induced increase in functional connectivity strength within basal ganglia/limbic network correlated positively with and the glucose-induced insulin release (r = 0.65, p = 0.02). (C) In relation to placebo, the fructose-induced increase in functional connectivity strength within the basal ganglia/limbic network correlated positively at trend level with the fructose-induced feeling of hunger (r = 0.57, p = 0.069).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4481317&req=5

pone.0130280.g006: (A) Correlations between resting state functional connectivity, insulin release and subjective appetite perception. In relation to placebo, the glucose-induced increase in functional connectivity strength (parameter estimates; PE) within the basal ganglia/limbic network correlated positively with the glucose-induced insulin release (μU/mL) (r = 0.62, p = 0.03). (B) Relative to fructose, the glucose-induced increase in functional connectivity strength within basal ganglia/limbic network correlated positively with and the glucose-induced insulin release (r = 0.65, p = 0.02). (C) In relation to placebo, the fructose-induced increase in functional connectivity strength within the basal ganglia/limbic network correlated positively at trend level with the fructose-induced feeling of hunger (r = 0.57, p = 0.069).
Mentions: Exploratory correlation analysis showed that the increased rsFC within the basal ganglia/limbic network induced by glucose relative to placebo correlated positively with the insulin level after glucose ingestion (r = 0.62, p = 0.03), as the glucose-induced effect on rsFC relative to fructose (r = 0.65, p = 0.02; Fig 6A and 6B, uncorrected for multiple testing). Moreover, there was a trend between the fructose-induced effect within the basal ganglia network relative to placebo and the fructose-induced feelings of hunger (r = 0.57, p = 0.069; Fig 6C, uncorrected for multiple testing). No other significant correlations between resting state data, behavioral and physiological parameters were found.

Bottom Line: Glucose ingestion induced significantly greater elevations in plasma glucose, insulin, GLP-1 and GIP, while feelings of fullness increased and prospective food consumption decreased relative to fructose.Our findings suggest that glucose and fructose induce dissociable effects on rsFC within the basal ganglia/limbic network, which are probably mediated by different insulin levels.A larger study would be recommended in order to confirm these findings.

View Article: PubMed Central - PubMed

Affiliation: Department of Gastroenterology, University Hospital of Basel, Basel, Switzerland.

ABSTRACT
Previous research has revealed that glucose and fructose ingestion differentially modulate release of satiation hormones. Recent studies have begun to elucidate brain-gut interactions with neuroimaging approaches such as magnetic resonance imaging (MRI), but the neural mechanism underlying different behavioral and physiological effects of glucose and fructose are unclear. In this paper, we have used resting state functional MRI to explore whether acute glucose and fructose ingestion also induced dissociable effects in the neural system. Using a cross-over, double-blind, placebo-controlled design, we compared resting state functional connectivity (rsFC) strengths within the basal ganglia/limbic network in 12 healthy lean males. Each subject was administered fructose, glucose and placebo on three separate occasions. Subsequent correlation analysis was used to examine relations between rsFC findings and plasma concentrations of satiation hormones and subjective feelings of appetite. Glucose ingestion induced significantly greater elevations in plasma glucose, insulin, GLP-1 and GIP, while feelings of fullness increased and prospective food consumption decreased relative to fructose. Furthermore, glucose increased rsFC of the left caudatus and putamen, precuneus and lingual gyrus more than fructose, whereas within the basal ganglia/limbic network, fructose increased rsFC of the left amygdala, left hippocampus, right parahippocampus, orbitofrontal cortex and precentral gyrus more than glucose. Moreover, compared to fructose, the increased rsFC after glucose positively correlated with the glucose-induced increase in insulin. Our findings suggest that glucose and fructose induce dissociable effects on rsFC within the basal ganglia/limbic network, which are probably mediated by different insulin levels. A larger study would be recommended in order to confirm these findings.

No MeSH data available.


Related in: MedlinePlus