How do you (estimate you will) like them apples? Integration as a defining trait of orbitofrontal function

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The past 15 years have seen a rapid increase in our understanding of orbitofrontal function. Today this region is the focus of an enormous amount of research, including work on such complex phenomena as regret, ambiguity, and willingness to pay. The orbitofrontal cortex is also credited as a major player in a host of neuropsychiatric diseases. This transformation arguably began with the application of concepts derived from animal learning theory. We will review data from studies emphasizing these approaches to argue that the orbitofrontal cortex forms a crucial part of a network of structures that signals information about expected outcomes. Further we will suggest that, within this network, the orbitofrontal cortex provides the critical ability to integrate information in real-time to make what amounts to actionable predictions or estimates about future outcomes. As we will show, the influence of these estimates can be demonstrated experimentally in appropriate behavioral settings, and their operation can also readily explain the role of orbitofrontal cortex in much more complex phenomena such as those cited above.

Introduction

In the past 15 years, we have seen a rapid and exponential increase in our understanding of orbitofrontal function. Today this region is the focus of an enormous amount of research, including work on such complex phenomena as regret, ambiguity, and willingness to pay [1•, 2•, 3•]. The orbitofrontal cortex is also credited as a major player in a host of neuropsychiatric diseases, including diverse disorders such as addiction, obsessive–compulsive disorder, mania and depression, and even schizophrenia [4•, 5, 6, 7, 8]. Here we will argue that this transformation began with the application of concepts derived from animal learning theory. We will review data from studies emphasizing these approaches to argue that the orbitofrontal cortex forms a crucial part of a network of structures that signals information about expected outcomes. Further we will suggest that, within this network, the orbitofrontal cortex provides the critical ability to integrate information in real-time to make what amounts to actionable predictions or estimates about future outcomes. As we will show, the influence of these estimates can be demonstrated experimentally in appropriate behavioral settings, and their operation can also readily explain the role of orbitofrontal cortex in much more complex phenomena such as those cited above. Additionally we will lay out a number of areas where critical questions remain to be answered.

Section snippets

Orbitofrontal cortex signals information about specific outcomes

An overarching principle of learning theory is that even very simple learning situations involve the acquisition of multiple parallel associative representations [9]. In other words, when an animal is presented with a simple predictive relationship between a cue (e.g. light) and an outcome (e.g. food), the animal does not learn a simple unitary association. Rather the animal actually learns to represent different features of the relationship. While it is unclear how finely the unitary

Orbitofrontal cortex signals estimates about future outcomes

Yet even as associative significance was a poor descriptor of the function of the orbitofrontal cortex 20 years ago, the idea that the orbitofrontal cortex is crucial for signaling information about specific outcomes also seems scarcely sufficient for describing the complex role this area plays in behavior. For one, the orbitofrontal cortex is only one of a number of areas that is crucial to outcome-guided behaviors revealed by devaluation tasks [30, 31•, 32, 33, 34]. Moreover some of the more

Conclusions

Here we have reviewed evidence regarding the role of orbitofrontal cortex in associative learning, focusing on studies that have employed concepts from learning theory to specify more precisely the function mediated by this area. On the basis of this work, we have suggested that the orbitofrontal cortex is crucial for signaling information about the specific outcomes that can be expected in a particular situation. This function seems particularly necessary (i.e. not redundant with that provided

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

This work was supported by grants to Dr Schoenbaum from the NIDA (R01-DA015718), NIMH (R01-MH080865), and NIA (R01-AG027097). In addition, Dr Esber was supported on an NIMH grant to Dr Peter Holland (R01-MH053667). The authors have no competing interests.

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