Abstract

In an uncertain world, the ability to predict and update the relationships between environmental cues and outcomes is a fundamental element of adaptive behaviour. This type of learning is typically thought to depend on prediction error, the difference between expected and experienced events and in the reward domain that has been closely linked to mesolimbic dopamine. There is also increasing behavioural and neuroimaging evidence that disruption to this process may be a cross-diagnostic feature of several neuropsychiatric and neurological disorders in which dopamine is dysregulated. However, the precise relationship between haemodynamic measures, dopamine and reward-guided learning remains unclear. To help address this issue, we used a translational technique, oxygen amperometry, to record haemodynamic signals in the nucleus accumbens (NAc) and orbitofrontal cortex (OFC), while freely moving rats performed a probabilistic Pavlovian learning task. Using a model-based analysis approach to account for individual variations in learning, we found that the oxygen signal in the NAc correlated with a reward prediction error, whereas in the OFC it correlated with an unsigned prediction error or salience signal. Furthermore, an acute dose of amphetamine, creating a hyperdopaminergic state, disrupted rats’ ability to discriminate between cues associated with either a high or a low probability of reward and concomitantly corrupted prediction error signalling. These results demonstrate parallel but distinct prediction error signals in NAc and OFC during learning, both of which are affected by psychostimulant administration. Furthermore, they establish the viability of tracking and manipulating haemodynamic signatures of reward-guided learning observed in human fMRI studies by using a proxy signal for BOLD in a freely behaving rodent.

Highlights

  • The world is an uncertain place, where behaviour of animals must continuously change to promote optimal survival

  • Amperometry: We performed two sets of complementary analyses: (i) model-free analyses, where we investigated the average signals in nucleus accumbens (NAc) and orbitofrontal cortex (OFC) during cue presentation or in the 30 s after outcome delivery over the course of learning and after amphetamine administration, and (ii) model-based analyses where we regressed the same signals against estimates from our computational model using the model with the lowest Bayesian information criterion (BIC) score (Fig. 1d)

  • The results presented here show that haemodynamic signals in NAc and OFC dynamically track expectation of reward as rats form associations between cues with high or low probability of reward outcome

Read more

Summary

Introduction

The world is an uncertain place, where behaviour of animals must continuously change to promote optimal survival. Learning to predict the relationship between environmental cues and significant events is a critical element of adaptive behaviour. It is hypothesised that adaptive behaviour depends upon comparisons of neural representations of cue-evoked expectations of events with events that occurred. Mismatch between these two representations is defined as a prediction error, and is likely a vital substrate by which accuracy of ensuing predictions about cue-event relationships can be improved. Prediction errors related to receipt of reward have been strongly associated with dopaminergic neurons and their projections to frontostriatal circuits [1,2,3,4]. Experimental disruption of dopaminergic transmission can impair formation of appropriate cue–reward associations [13,14,15]

Objectives
Methods
Results
Conclusion
Full Text
Published version (Free)

Talk to us

Join us for a 30 min session where you can share your feedback and ask us any queries you have

Schedule a call