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Acute tryptophan depletion alters the effective connectivity of emotional arousal circuitry during visceral stimuli in healthy women.

ABSTRACT: Alterations in serotonin signalling within the brain-gut axis have been implicated in the pathophysiology of irritable bowel syndrome (IBS) and is a treatment target. Acute tryptophan depletion (ATD) decreases brain serotonin (5-hydroxytryptamine; 5-HT) levels, and increases visceral perception and negative emotional bias in patients with IBS. The aim of the present study was to determine the effect of ATD on brain activity and connectivity during visceral stimuli in healthy women, and to compare the ATD-induced brain connectivity of an arousal circuit in female patients with IBS without ATD.12 healthy females (19-25 years) were studied under placebo (PLA) conditions and ATD. Functional MRI measurements were performed during a rectal barostat protocol, consisting of random non-painful and maximal tolerable distensions. Partial least squares analyses and structural equation modelling were used to evaluate the effect of ATD on functional and effective brain connectivity during distension. Results in healthy controls under ATD were compared with the effective connectivity of brain responses to 45 mm?Hg rectal distension in 14 female patients with constipation-predominant IBS (IBS-C) (24-50 years).In healthy controls, ATD resulted in increased response of an extensive brain network to balloon distension, including the amygdala and nodes of emotional arousal and homeostatic afferent networks. The effect was greater during high inflation, suggesting greater engagement of the central serotonion system with more aversive visceral stimuli. Effective connectivity analysis revealed a profound effect of ATD on coupling between emotional arousal network nodes, resulting in loss of negative feedback inhibition of the amygdala. A near-identical pattern was identified in the patients with IBS-C.The findings are consistent with an ATD-induced disinhibition of and increased connectivity within an emotional arousal network during aversive stimulation. Together with the previous demonstration of ATD-induced visceral hyperalgesia in healthy controls, and the near-identical effective connectivity pattern observed in patients with IBS-C, these findings suggest that dysregulation of this brain network may play a role in central pain amplification and IBS pathophysiology.

SUBMITTER: Labus JS

PROVIDER: S-EPMC3871999 | biostudies-literature | 2011 Sep

REPOSITORIES: biostudies-literature

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Acute tryptophan depletion alters the effective connectivity of emotional arousal circuitry during visceral stimuli in healthy women.

Labus J S JS Mayer E A EA Jarcho J J Kilpatrick L A LA Kilkens T O C TO Evers E A T EA Backes W H WH Brummer R-J M RJ van Nieuwenhoven M A MA

Gut 20110314 9

<h4>Objective</h4>Alterations in serotonin signalling within the brain-gut axis have been implicated in the pathophysiology of irritable bowel syndrome (IBS) and is a treatment target. Acute tryptophan depletion (ATD) decreases brain serotonin (5-hydroxytryptamine; 5-HT) levels, and increases visceral perception and negative emotional bias in patients with IBS. The aim of the present study was to determine the effect of ATD on brain activity and connectivity during visceral stimuli in healthy wo ...[more]

PMID: 21402618

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Project description:The role of emotional factors in maintaining cognitive control is one of the most intriguing issues in understanding emotion-cognition interactions. In the current experiment, we assessed the role of emotional factors (valence, arousal, and subjective significance) in perceptual and conceptual inhibition processes. We operationalised both processes with the classical cognitive paradigms, i.e., the flanker task and the emotional Stroop task merged into a single experimental procedure. The procedure was based on the presentation of emotional words displayed in four different font colours flanked by the same emotional word printed with the same or different font colour. We expected to find distinct effects of both types of interference: earlier for perceptual and later for emotional interference. We also predicted an increased arousal level to disturb inhibitory control effectiveness, while increasing the subjective significance level should improve this process. As we used orthogonal manipulations of emotional factors, our study allowed us for the first time to assess interactions within emotional factors and between types of interference. We found on the behavioural level the main effects of flanker congruency as well as effects of emotionality. On the electrophysiological level, we found effects for EPN, P2, and N450 components of ERPs. The exploratory analysis revealed that effects due to perceptual interference appeared earlier than the effects of emotional interference, but they lasted for an extended period of processing, causing perceptual and emotional interference to partially overlap. Finally, in terms of emotional interference, we showed the effect of subjective significance: the reduction of interference cost in N450 for highly subjective significant stimuli. This study is the first one allowing for the investigation of two different types of interference in a single experiment, and provides insight into the role of emotion in cognitive control.

Dataset Information

Acute tryptophan depletion alters the effective connectivity of emotional arousal circuitry during visceral stimuli in healthy women.

Publications

Acute tryptophan depletion alters the effective connectivity of emotional arousal circuitry during visceral stimuli in healthy women.

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