The effects of acute tryptophan depletion on costly information sampling: impulsivity or aversive processing?

Abstract

Rationale: The neurotransmitter serotonin (5-HT) has been implicated in both aversive processing and impulsivity. Reconciling these accounts, recent studies have demonstrated that 5-HT is important for punishment-induced behavioural inhibition. These studies focused on situations where actions lead directly to punishments. However, decision-making often involves making tradeoffs between small 'local' costs and larger 'global' losses.

Objective: We aimed to distinguish whether 5-HT promotes avoidance of local losses, global losses, or both, in contrast to an overall effect on reflection impulsivity. We further examined the influence of individual differences in sub-clinical depression, anxiety and impulsivity on global and local loss avoidance.

Methods: Healthy volunteers (N = 21) underwent an acute tryptophan depletion procedure in a double-blind, placebo-controlled crossover design. We measured global and local loss avoidance in a decision-making task where subjects could sample information at a small cost to avoid making incorrect decisions, which resulted in large losses.

Results: Tryptophan depletion removed the suppressive effects of small local costs on information sampling behaviour. Sub-clinical depressive symptoms produced effects on information sampling similar to (but independent from) those of tryptophan depletion. Dispositional anxiety was related to global loss avoidance. However, trait impulsivity was unrelated to information sampling.

Conclusions: The current findings are consistent with recent theoretical work that characterises 5-HT as pruning a tree of potential decisions, eliminating options expected to lead to aversive outcomes. Our results extend this account by proposing that 5-HT promotes reflexive avoidance of relatively immediate aversive outcomes, potentially at the expense of more globally construed future losses.

Fig. 1

Screen display for the Information Sampling Task (Costly condition). Each trial commenced (left) with the presentation of 25 grey boxes arranged in a 5 × 5 matrix, covering a random assortment of two colours of squares; these two colours were displayed on panels at the foot of the screen. When the subject touched a box (middle), it opened to reveal its colour. Subjects were instructed to decide which of the two colours was in the majority on the board. They were told they could open as many boxes as they wished and to touch the corresponding panel at the foot of the screen (bottom right) once they had decided which colour was in the majority. The amount to be won or lost on the current trial was displayed in the upper left corner; in the Costly condition, the “Win” amount decreased by 10 with each box opened. Reprinted from Biological Psychiatry, vol. 60, L. Clark et al., Reflection impulsivity in current and former substance users, p. 516, Copyright (2006), with permission from Elsevier

Fig. 2

a The mean information sampled per trial (defined as P(correct) at decision) as a function of condition (Free, Costly) and treatment [placebo (PLA), ATD]. b The mean change in information sampling from the Free condition to the Costly condition as a function of treatment. Error bars represent the standard error of the difference between treatments

Fig. 3

Correlations between BDI scores and information sampling (P(correct) at decision) in the Costly condition (a) and Free condition (b), averaged across treatment conditions

Fig. 4

Correlations between BIS scores and information sampling (P(correct) at decision) in the Costly condition (a) and Free condition (b), averaged across treatment conditions