The Good and Bad Differentially Encoded within the Subthalamic Nucleus in Rats(1,2,3).

Christelle Baunez,Emmanuel Breysse,Yann Pelloux

doi:10.1523/eneuro.0014-15.2015

Abstract

The subthalamic nucleus (STN) has only recently been added into the reward circuit. It has been shown to encode information regarding rewards (4% sucrose, 32% cocaine). To investigate the encoding of negative value, STN neurons were recorded in rats performing a task using discriminative stimuli predicting various rewards and especially during the replacement of a positive reinforcer (4% sucrose) by an aversive reinforcer (quinine). The results show that STN neurons encode information relative to both positive and aversive reinforcers via specialized subpopulations. The specialization is reset when the context is modified (change from a favorable context (4% vs 32% sucrose) to an unfavorable context (quinine vs 32% sucrose). An excitatory response to the cue light predicting the reward seems to be associated with the preferred situation, suggesting that STN plays a role in encoding the relative value of rewards. STN also seems to play a critical role in the encoding of execution error. Indeed, various subpopulations of neurons responding exclusively at early (i.e., “oops neurons”) or at correct lever release were identified. The oops neurons respond mostly when the preferred reward (32% sucrose) is missed. Furthermore, STN neurons respond to reward omission, suggesting a role in reward prediction error. These properties of STN neurons strengthen its position in the reward circuit as a key cerebral structure through which reward-related processes are mediated. It is particularly important given the fact that STN is the target of surgical treatment for Parkinson’s disease and obsessive compulsive disorders, and has been suggested for the treatment of addiction as well.

Highlights

Motivation and its neurobiological substrate have been studied largely with a principal focus on the various components of the classic reward system, the dopamine (DA) mesocorticolimbic pathway, the striatum, the nucleus accumbens, ventral pallidum, and prefrontal cortex (PFC)
The quinine induced no tongue protrusions compared with the 4%, 10%, and 32% sucrose, and the sucrose solution induced no gapes whatever the sucrose concentration compared to quinine solution
Positive and negative reinforcers can modulate Subthalamic nucleus (STN) activity via various subpopulations The present study shows that STN neurons can encode the expectation of an aversive reinforcer, as well eNeuro.sfn.org as a positive reinforcer

Summary

Introduction

Motivation and its neurobiological substrate have been studied largely with a principal focus on the various components of the classic reward system, the dopamine (DA) mesocorticolimbic pathway, the striatum, the nucleus accumbens, ventral pallidum, and prefrontal cortex (PFC). It was important to further investigate how reward-related information could be encoded by the STN neurons. Reward-related information is not expected to be encoded in the STN only at the moment of reward delivery, and at the presentation of the cue. It has been shown that STN neuronal activity could be modulated by different positive reinforcers (various concentrations of sucrose or cocaine, and fruit juice) at delivery and by their associated predicting cues whatever the nature of the rewards (Darbaky et al, 2005; Espinosa-Parrilla et al, 2013; Lardeux et al, 2009, 2013). In order to further assess the role of STN in motivational processes, and in encoding aversive stimuli, here the responses of STN neurons have been studied during the replacement of a positive reinforcer (sucrose) by an aversive reinforcer

Methods

Results

Conclusion