Elsevier

Neuroscience Research

Volume 57, Issue 3, March 2007, Pages 434-445
Neuroscience Research

Neurons in the macaque orbitofrontal cortex code relative preference of both rewarding and aversive outcomes

https://doi.org/10.1016/j.neures.2006.12.003Get rights and content

Abstract

Many studies have shown that the orbitofrontal cortex (OFC) is involved in the processing of emotional information. However, although some lines of study showed that the OFC is also involved in negative emotions, few electrophysiological studies have focused on the characteristics of OFC neuronal responses to aversive information at the individual neuron level. On the other hand, a previous study has shown that many OFC neurons code relative preference of available rewards. In this study, we aimed to elucidate how reward information and aversive information are coded in the OFC at the individual neuron level. To achieve this aim, we introduced the electrical stimulus (ES) as an aversive stimulus, and compared the neuronal responses to the ES-predicting stimulus with those to reward-predicting stimuli. We found that many OFC neurons showed responses to both the ES-predicting stimulus and the reward-predicting stimulus, and they code relative preference of not only the reward outcome but also the aversive outcome. This result suggests that the same group of OFC neurons code both reward and aversive information in the form of relative preference.

Introduction

A previous study has shown that a group of orbitofrontal cortex (OFC) neurons code relative preference of available rewards (Tremblay and Schultz, 1999). It suggests that the OFC compares the values of available rewards. This is a very important function to perform in making an adaptive decision. However, it remains unclear that the coding style of relative preference in the OFC could be extended to aversive outcomes. In our daily life we compare various types of outcomes, not only rewards, to make a decision. We sometimes compare rewarding outcomes with aversive outcomes at the same time. For example, if we are on a diet we may think over whether or not to eat a sweet cake. Eating the cake is rewarding but at the same time putting on fat is aversive. The brain must compare the various types of outcomes, rewarding and/or aversive, to make an adaptive decision.

Heretofore, many studies have shown that the OFC is involved in the processing of reward information (Tremblay and Schultz, 1999, Tremblay and Schultz, 2000a, Tremblay and Schultz, 2000b, Schultz et al., 2000, Roesch and Olson, 2004, Roesch and Olson, 2005, Padoa-Schioppa and Assad, 2006). Although many electrophysiological studies have examined the response properties of OFC neurons to rewards, only a few studies have focused on the response properties of OFC neurons to aversive stimuli (Thorpe et al., 1983, Roesch and Olson, 2004). This is in spite of the importance of negative emotions, which are accompanied by aversive events. Negative emotions are as important as positive emotions to the formation of adaptive behavior in the natural environment, especially personal safety and security behaviors. In order to survive in the natural environment, animals must predict the possibility that a danger occurs and select adaptive behavior to avoid it.

Some lines of evidence have indicated that the OFC is also concerned with aversive information. Firstly, some neuroimaging studies have showed that the OFC is activated by aversive stimuli (Elliott et al., 2000, Frey et al., 2000, O’Doherty et al., 2001, Ursu and Carter, 2005). Secondly, patients with damage to the OFC are unable to use aversive information to modify their behavior (Stuss et al., 1983, Freedman et al., 1998). Finally, monkeys with damage to the OFC respond abnormally to aversive objects (Butter and McDonald, 1969b, Ursin et al., 1969, Butter et al., 1970, Butter and Snyder, 1972, Izquierdo and Murray, 2004). These observations suggest that the OFC is processing not only reward information but also aversive information.

In this study, we focused on how the OFC codes aversive information as well as reward information at the individual neuron level. One hypothesis is that reward information and aversive information are coded separately in different groups of neurons in the OFC. Another hypothesis is that they are integrated in the same group of neurons in the way that relative preference is represented. To compare the neuronal response to aversive stimuli with those to rewarding stimuli, we set two stimulus-outcome conditions; one included rewarding and aversive outcomes, and the other included only rewarding outcomes. We examined the response of OFC neurons under these stimulus-outcome conditions in separate experimental blocks, and compared the response properties to aversive-predicting cue stimulus with those to reward-predicting cue stimulus.

Section snippets

Subjects

Two macaque monkeys (Macaca mulatta, monkey P: 5.8 kg, monkey D: 8.9 kg) were used in this study. The experiment was performed in a dark and sound-attenuated room, with the monkey seated in a primate chair facing a 17 in. CRT monitor (PC-KM173: NEC, Tokyo, Japan). During the training and recording sessions, the animals were deprived of water to elevate their motivation for liquid reward. All experiments were carried out in accordance with the “Guide for the Care and Use of the Laboratory Primates”

Behavioral reaction time and task performance

We summarized the behavioral reaction time (from target onset to the hold lever release) of each condition in Table 1. The monkeys showed the differential behavioral reaction time depending on the outcomes. Under the Juice–Water condition, the monkeys responded significantly faster in the trials with juice reward than those with water reward in both the standard and the reversal blocks (p < 0.01; Mann–Whitney U-test). Similarly, under the Water–ESA condition, they responded significantly faster

Discussion

This study showed that a group of OFC neurons code the relative preference of both rewarding and aversive outcomes. We examined activities of OFC neurons under two conditions, one of which included only reward trials (Juice–Water condition) and the other included reward and aversive trials (Water–ESA condition). Many OFC neurons showed differential cue responses depending on whether the outcome was preferable or not under both conditions. This observation indicates that the same group of OFC

Acknowledgement

This study was partially supported by a Grant in Aid for Scientifically Promoted Research (No. 10CE2005).

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