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1Department of Psychology, University of Illinois, Urbana-Champaign, 2Department of Computing Science, University of Alberta, Edmonton, 3Department of Psychiatry, University of Alberta, Edmonton, 4Department of Psychology, University of Alberta, Edmonton, 5Centre for Neuroscience, University of Alberta, Edmonton, 6Neuroscience Program, University of Illinois, Urbana-Champaign, 7Beckman Institute, University of Illinois, Urbana-Champaign
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We present a protocol that allows investigation of the neural correlates of deliberate and automatic emotion regulation, using functional magnetic resonance imaging. This protocol can be used in healthy participants, both young and older, as well as in clinical patients.
Dolcos, S., Sung, K., Denkova, E., Dixon, R. A., Dolcos, F. Brain Imaging Investigation of the Neural Correlates of Emotion Regulation. J. Vis. Exp. (54), e2430, doi:10.3791/2430 (2011).
The ability to control/regulate emotions is an important coping mechanism in the face of emotionally stressful situations. Although significant progress has been made in understanding conscious/deliberate emotion regulation (ER), less is known about non-conscious/automatic ER and the associated neural correlates. This is in part due to the problems inherent in the unitary concepts of automatic and conscious processing1. Here, we present a protocol that allows investigation of the neural correlates of both deliberate and automatic ER using functional magnetic resonance imaging (fMRI). This protocol allows new avenues of inquiry into various aspects of ER. For instance, the experimental design allows manipulation of the goal to regulate emotion (conscious vs. non-conscious), as well as the intensity of the emotional challenge (high vs. low). Moreover, it allows investigation of both immediate (emotion perception) and long-term effects (emotional memory) of ER strategies on emotion processing. Therefore, this protocol may contribute to better understanding of the neural mechanisms of emotion regulation in healthy behaviour, and to gaining insight into possible causes of deficits in depression and anxiety disorders in which emotion dysregulation is often among the core debilitating features.
1. Task Design, Stimuli, and Experimental Protocol
The overarching protocol involves assessments of emotional ratings of pictures (immediate impact), and of the memory for
these pictures (long-term impact), as a result of inducing the goal to regulate emotional responses. The goal to regulate is induced explicitly or implicitly, and the immediate and long-term impact is assessed relative to ratings of and memory for pictures presented during baseline blocks/runs that precede the ER manipulations (pre-ER induction baseline); see Figure 1 for a diagram of the overall experimental design. Below we provide details regarding all these aspects.
Figure 1. Diagram of the protocol. The ER goal is induced in each participant both consciously/explicitly and non-consciously/implicitly, but the order of induction is different and counterbalanced across participants - i.e., those assigned to explicit ER in the first part complete the implicit manipulation in the second part, and vice versa; each manipulation is preceded by its own baseline runs. See below for detailed descriptions of the Rating and Memory tasks.
Emotion Regulation Manipulation
Assessments of the Immediate Impact of ER manipulation: The Emotional Rating Task
Assessment of the Long-Term Impact of ER manipulation: The Memory Retrieval Task
2. Preparing the Subject for the Scan
All participants provide written informed consent prior to running the experimental protocol, which is approved by an Ethics Board. They are also warned that many of the pictures depict distressing events, such as acts of violence or trauma, and are provided with printed examples of representative pictures.
In the Scanning Room
3. Data Recording and Processing
We collected MRI data from 24 young healthy participants, using a 1.5 Tesla Siemens Sonata scanner for MRI recordings. Our anatomical images are 3D MPRAGE anatomical series (repetition time (TR) = 1600 ms, echo time (TE) = 3.82 ms; number of slices = 112; voxel size = 1x1x1mm). The functional images consist of series of 28 functional slices (voxel size = 4x4x4 mm), acquired axially using an echoplanar sequence (TR = 2000 ms; TE = 40 ms; field of view FOV = 256x256mm), thus allowing for full-brain coverage.
We use Statistical Parametric Mapping (SPM: http://www.fil.ion.ucl.ac.uk/spm/) in combination with in-house MATLAB-based tools. Pre-processing involves typical steps: quality assurance, TR alignment, motion correction, co-registration, normalization, and smoothing (8 mm3 kernel)9. Individual and group-level statistical analyses may involve comparisons of brain activity according to ER manipulation (ER vs. baseline runs; see Figure 2), emotional valence (negative vs. neutral), arousal (low vs. high), and memory performance (remembered vs. forgotten). Correlations of brain imaging data with behavioural data (e.g., picture ratings) and/or scores indexing personality measures (e.g., personality traits indexing habitual engagement of ER strategies) can also be performed, to investigate how brain activity co-varies with individual differences in behaviour and personality.
4. Representative Results:
Figure 2. Decreased amygdala activity and increased prefrontal cortex activity following ER manipulation. Inducement of the ER goal was associated with reduced activity in brain areas associated with emotion processing, including the amygdala (a), and increased activity in brain regions associated with cognitive control and emotion regulation10, including ventrolateral prefrontal cortex (PFC) (b), dorsolateral PFC (d), and medial PFC (c)11,12. As shown in the bar graph illustrating the vlPFC activity, explicit and implicit ER were associated with similar patterns of response, suggesting that these changes reflect joint contribution of explicit and implicit ER. The "activation maps" are superimposed on high resolution brain images displayed in coronal views; the color bars indicate the gradient of t values of the activation maps, based on group statistics (N = 24), reflecting brain activity in voxels that show decreased (left panel) or increased (right panel) activity as a result of ER manipulation. It should be noted that activation blobs in the PFC may cover more areas, as follows: vlPFC/Insula (b) and dorsal Anterior Cingulate Cortex/Premotor Cortex (c). The bar graphs illustrate percent signal changes in response to emotional (Emo) and neutral (Neu) pictures before (i.e., BaseRuns) and after the induction of the ER goals (i.e., Combined ER = Explicit and Implicit ER averaged together, Explicit ER, and Implicit ER), as extracted from voxels showing pre- to post-ER differences. L = Left; R = Right.
Table 1. Decreased emotional ratings following ER manipulation. Similar to the fMRI results, there was a reduction of emotional ratings following ER induction, and this effect resulted from decreases following both explicit and implicit ER. Importantly, emotional ratings did not change significantly in a control group that performed the same task following similar delays but in the absence of ER goal induction. Supporting these ideas, a 2 (Manipulation: Baseline vs. ER Induction) x 2 (Valence: Emotional vs. Neutral) repeated-measures ANOVA on data from the experimental group* yielded a significant main effect of Manipulation (F[1, 19] = 11.21, p < 0.002) and a significant Manipulation x Valence Interaction (F[1, 19] = 3.02, p < 0.05), and a similar 2-way ANOVA on data from the control group (N = 9) did not yield a significant main effect of Delay (Baseline vs. Delayed Runs) or a significant Delay x Valence interaction. These findings suggest that the decrease in ratings in the experimental group was due to the induction of the goal to control emotions rather than due to habituation following repeated exposure to emotional stimulation. *because of data attrition due to common causes (e.g., technical failure), behavioral analyses in the experimental group were based on data from 20 participants.
Taken together, these behavioral and brain imaging findings validate the present experimental design, which can be used to compare explicit and implicit inductions of the goal to regulate emotions. It should be noted that the present report emphasizes aspects that result from the joint contribution of the Explicit and Implicit ER manipulations, but this does not exclude the possibility that their effects may be dissociable at behavioral and/or brain level.
We described a protocol that involves explicit and implicit manipulation of the goal to regulate emotion, and allows investigation of the associated neural correlates. This design has the potential to advance our knowledge of how the brain regulates emotions, being well suited for comparisons of explicit ER to implicit ER, which is unintentional and can happen without participant's insight and awareness13,14. Hence, the protocol can be particularly useful for investigations of habitual opposite affective biases, such as those observed in healthy aging (positivity bias15) and depression (negativity bias16), which are associated with enhanced automatic engagement of ER mechanisms (older adults17,18) and impaired ability to regulate emotions (depressed patients19,20).
No conflicts of interest declared.
This research was supported by a Young Investigator Award from the National Alliance for Research on Schizophrenia and Depression and a CPRF Award from the Canadian Psychiatric Research Foundation (to FD). The authors wish to thank Trisha Chakrabarty and Peter Seres for assistance with fMRI data collection and Kristina Suen for assistance with data analysis.
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