Review
The functional neuroanatomy of reappraisal: Time matters

https://doi.org/10.1016/j.neubiorev.2009.06.003Get rights and content

Abstract

Humans can regulate their emotional states through a number of effortful cognitive strategies, a type of adaptive behavior not found in animals. The best studied strategy is reappraisal which consists in deliberately changing the emotional interpretation of a stimulus. Reappraisal modulates both subjective and physiological emotional response components and has long-term effects on well-being and mental health. Over the past few years, a rapidly growing neuroimaging literature has attempted to characterize the neural mechanisms that mediate reappraisal, but results have so far been relatively inconsistent. This article provides an overview of the current state of the field and presents a first formal quantitative meta-analysis of neuroimaging findings. It introduces a new model of the cognitive processes underlying reappraisal which builds on a conceptualization of reappraisal as a temporally extended, dynamic process and partitions reappraisal episodes into an early implementation and a later maintenance stage. In agreement with the model, preliminary evidence from parametric meta-analysis suggests the two stages are supported by distinct frontal networks. Hypotheses for further research are presented.

Introduction

Emotion regulation has been defined as a “heterogeneous set of processes” through which “individuals influence which emotions they have, when they have them, and how they experience and express these emotions” (Gross, 1999). The capacity to volitionally influence one's emotional reactions conveys enormous behavioral flexibility and adaptive advantage. From a quality-of-life perspective, emotion regulation enhances a sense of self-determination and well-being. From a clinical perspective, emotion regulation may protect against affective disorder and be a useful tool in cognitive psychotherapy.

Volitional emotion regulation strategies are manifold and can broadly be subdivided into action-oriented strategies that attempt to change the emotion-eliciting character of the environment, cognitive strategies that attempt to modify the way emotional stimuli are processed, and response-focused strategies that attempt to change the overt behavioral output of the emotional processing stream (Gross, 2002). One of the best studied strategies is the cognitive technique of reappraisal. Reappraisal is a conscious change in the way an emotional stimulus is interpreted, initiated in order to change its emotion-eliciting character (Gross, 2002). For example, being fired is usually spontaneously appraised as negative and would induce worry, anger or sadness. To reduce these negative reactions, one could try to see the situation as an opportunity for an overdue change or as effectively less dramatic as might appear at first sight. Reappraisal thus involves bringing to mind alternative appraisals in the form of thoughts or mental images that contradict the first, spontaneous interpretation of the situation. Such a change in working memory contents can be remarkably powerful in modulating emotional reactions, both at the subjective and at the physiological level (Dillon and Labar, 2005, Gross, 2002, Gross and John, 2003, Houston and Holmes, 1974, Jackson et al., 2000, Kalisch et al., 2005, Schaefer et al., 2003), and may also have long-term adaptive consequences (Kross and Ayduk, 2008). Further, habitual reappraisers have an advantage over individuals who prefer a response-focused type of emotion regulation, namely suppression of emotional expression, in terms of mental health and social functioning (Gross, 2002, Gross and John, 2003).

There is now a substantive body of neuroimaging studies on reappraisal that have tried to delineate the brain areas engaged by reappraisal. Most of these have focussed on reappraisal in the service of reducing negative emotion (rather than enhancing emotion or modulating positive emotion). Existing reviews (Ochsner and Gross, 2005, Phillips et al., 2008, Quirk and Beer, 2006) have pointed out the importance of the lateral and medial frontal cortices (LFC, MFC), but frontal activations are typically widespread and can vary considerably between studies, and no clear picture has emerged so far as to what the exact contributions of each area are.

The picture gets even more complicated when trying to integrate findings from other types of emotion regulation such as self-distraction (e.g., Delgado et al., 2008a, Delgado et al., 2008b, Depue et al., 2007, Frankenstein et al., 2001, Kalisch et al., 2006, Wyland et al., 2003) or expressive suppression (e.g., Goldin et al., 2008, Gross, 2002, Ohira et al., 2006). For instance, it appears that the dorsolateral prefrontal cortex (DLPFC) and the anterior cingulate cortex (ACC) are involved in distraction, reappraisal, and suppression (Phillips et al., 2008), but again the localization of DLPFC and ACC activations can vary substantially and sometimes even more between two given studies that examine the same strategy than between two studies that look at two different strategies. These divergences may stem from variability in paradigms, samples, or analysis methods. But they also highlight a fundamental lack of knowledge about the cognitive operations that support the different strategies and about how these interact in a causal and dynamic fashion. One possible solution is to try to understand one particular “model” strategy in as much detail as possible and then to expand the analysis to other types of strategies, in a comparative fashion. In this article, I will use reappraisal in the service of down-regulating negative emotion as a model or prototypical case and attempt to sketch what might be the nucleus for a mechanistic theory of reappraisal which, I hope, will eventually become a good basis for hypothesis-driven investigation of other types of reappraisal or regulation strategies as well.

In particular, I will argue that our understanding of the neural bases of reappraisal might be considerably enhanced by clarifying the role of time in the process of reappraisal. As I will discuss in detail below, most neuroscientists still conceptualize reappraisal as a process that is either very brief and restricted to the beginning of an emotional episode or that occurs in an invariant fashion across the duration of an emotional episode. I will point out why these, often implicit, assumptions are implausible and why a more realistic model of the dynamic nature of reappraisal might be useful in understanding associated neural activation patterns. I will start off, however, by summarizing the current state of the field using a formal meta-analytic approach. I consider a meta-analytic approach as advantageous over a mere qualitative review of activation foci, because formal meta-analysis provides a quantitative measure of the consistency of activations across studies that can be tested for statistical significance (Wager et al., 2007) and thus provide a safe ground for theorizing.

Section snippets

Meta-analysis of neuroimaging studies

In a typical reappraisal study, subjects are shown aversive pictures from the International Affective Picture System (IAPS; Lang et al., 1997) to generate negative emotion. In a “decrease” condition, subjects are instructed to reappraise the picture in a more positive fashion while in a comparison “view” condition subjects are supposed to look at the pictures without trying to modulate their emotions. The cue telling subjects whether to reappraise or to simply view a given picture may occur at

The dynamic nature of reappraisal

Any cognitive model of reappraisal should describe the psychological processes involved in reappraisal and also the temporal relationship among these and with regards to other relevant processes during an emotional episode, that is, to stimulus detection and evaluation, and behavioral response generation. An influential view holds that reappraisal is an “antecedent-focused” process (Gross, 1998). That is, reappraisal plays on the evaluation of a stimulus in terms of its emotional–motivational

The model

As a first step towards capturing the temporal complexity of reappraisal and generating predictions for neuroimaging studies, I would like to propose a simple model that follows the idea of early and late reappraisal components. In this model, ‘early’ refers to those operations needed to choose and implement an initial reappraisal strategy; ‘late’ refers to the operations needed to maintain that strategy in working memory and to monitor its success during the course of an emotional situation.

A speculation on cognitive sub-operations and their neural substrates

Given IMMO survives testing, it would be highly desirable to determine in more detail the cognitive processes that allow for choosing, implementing, maintaining and monitoring a reappraisal strategy. I would speculate that early implementation processes strongly rely on retrieval from long-term memory of the thoughts and mental images that constitute the reappraisal strategy. This controlled retrieval process may also include an element of selecting from potential alternative retrieval products

Conclusion

The psychological and neurobiological analysis of reappraisal will improve our understanding of adaptive human behavior and help bridge the artificial gap between what is sometimes called “cold” cognitive and “hot” emotional functions of the brain. Reappraisal research may also yield insights into the nature of affective disease and the working mechanisms of therapy. The faster the field moves from exploratory to theory-driven inquiry, the faster we will be able to fulfil these goals. These

Acknowledgements

I thank C. Büchel, T. Sommer, F. Eippert, A. Etkin, T. Egner, and B. Strange for useful comments on an earlier version of this manuscript. This work was funded by the Deutsche Forschungsgemeinschaft (DFG Emmy Noether program KA 1623/3-1).

Raffael Kalisch has obtained a Diploma in Human Biology from Phillips-Universität, Marburg, Germany, and a PhD in Biology from Ludwig-Maximilans-Universität (LMU), Munich, Germany. He worked as a PhD student at the animal high-field imaging laboratory of the Max Planck Institute of Psychiatry, Munich, and was a postdoctoral student at the Functional Imaging Laboratory (FIL) of the Wellcome Department of Imaging Neuroscience at University College London, UK (with R. Dolan) and at the Institute

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    Raffael Kalisch has obtained a Diploma in Human Biology from Phillips-Universität, Marburg, Germany, and a PhD in Biology from Ludwig-Maximilans-Universität (LMU), Munich, Germany. He worked as a PhD student at the animal high-field imaging laboratory of the Max Planck Institute of Psychiatry, Munich, and was a postdoctoral student at the Functional Imaging Laboratory (FIL) of the Wellcome Department of Imaging Neuroscience at University College London, UK (with R. Dolan) and at the Institute for Systems Neuroscience at University Medical Center Hamburg-Eppendorf, Germany (with C. Büchel). He currently leads an Emmy Noether research group.

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