Anxiety-Like Behavioural Inhibition Is Normative under Environmental Threat-Reward Correlations.

Dominik R Bach,Aldo A Faisal

doi:10.1371/journal.pcbi.1004646

Abstract

Behavioural inhibition is a key anxiety-like behaviour in rodents and humans, distinct from avoidance of danger, and reduced by anxiolytic drugs. In some situations, it is not clear how behavioural inhibition minimises harm or maximises benefit for the agent, and can even appear counterproductive. Extant explanations of this phenomenon make use of descriptive models but do not provide a formal assessment of its adaptive value. This hampers a better understanding of the neural computations underlying anxiety behaviour. Here, we analyse a standard rodent anxiety model, the operant conflict test. We harvest Bayesian Decision Theory to show that behavioural inhibition normatively arises as cost-minimising strategy in temporally correlated environments. Importantly, only if behavioural inhibition is aimed at minimising cost, it depends on probability and magnitude of threat. Harnessing a virtual computer game, we test model predictions in four experiments with human participants. Humans exhibit behavioural inhibition with a strong linear dependence on threat probability and magnitude. Strikingly, inhibition occurs before motor execution and depends on the virtual environment, thus likely resulting from a neural optimisation process rather than a pre-programmed mechanism. Individual trait anxiety scores predict behavioural inhibition, underlining the validity of this anxiety model. These findings put anxiety behaviour into the context of cost-minimisation and optimal inference, and may ultimately pave the way towards a mechanistic understanding of the neural computations gone awry in human anxiety disorder.

Highlights

Rodent models of human anxiety commonly involve a conflict between approach and avoidance [1,2,3,4], as exemplified in the Elevated Plus Maze [5,6,7], Open Field test [8], operant conflict tests [9, 10], or novelty-suppressed feeding test [11]
Results may suggest a neural implementation that relies on online cost minimisation
This finding could afford a better understanding of human anxiety disorder and the underlying neural computations

Summary

Introduction

Rodent models of human anxiety commonly involve a conflict between approach and avoidance [1,2,3,4], as exemplified in the Elevated Plus Maze [5,6,7], Open Field test [8], operant conflict tests [9, 10], or novelty-suppressed feeding test [11]. Hippocampus lesions reduce anxiety-like behaviour in rodents [1, 14, 15] and humans [13] alike which suggests a neural implementation that is conserved across species. Extant theories assume that behavioural inhibition arises because of time requirements in the decision-making process: in one model because the animal uses that time to collect information about the situation (risk assessment) [1, 16], and in another suggestion because the decision whether to approach or to avoid is difficult [7]. We demonstrate behavioural inhibition in humans, with a pattern that cannot be explained by previous accounts but is consistent with model predictions and may suggest a neural implementation based on goal-directed cost minimisation. Behavioural inhibition as measured in our task is related to individual anxiety scores, and this independently confirms the validity of the experimental anxiety model

Methods

Results

Discussion

Conclusion