1Department of Psychiatry, University of Alberta, 2Centre for Neuroscience, University of Alberta, 3Department of Psychology, University of Illinois, 4Brain Imaging and Analysis Center, Duke University, 5Department of Psychiatry and Behavioral Sciences, Duke University, 6Mid-Atlantic Mental Illness Research Education and Clinical Center, VA Medical Center, 7Department of Psychology, Yale University, 8Neuroscience Program, University of Illinois, 9Beckman Institute for Advanced Science & Technology, University of Illinois
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Wong, G., Dolcos, S., Denkova, E., Morey, R., Wang, L., McCarthy, G., et al. Brain Imaging Investigation of the Impairing Effect of Emotion on Cognition. J. Vis. Exp. (60), e2434, doi:10.3791/2434 (2012).
Emotions can impact cognition by exerting both enhancing (e.g., better memory for emotional events) and impairing (e.g., increased emotional distractibility) effects (reviewed in 1). Complementing our recent protocol 2 describing a method that allows investigation of the neural correlates of the memory-enhancing effect of emotion (see also 1, 3-5), here we present a protocol that allows investigation of the neural correlates of the detrimental impact of emotion on cognition. The main feature of this method is that it allows identification of reciprocal modulations between activity in a ventral neural system, involved in 'hot' emotion processing (HotEmo system), and a dorsal system, involved in higher-level 'cold' cognitive/executive processing (ColdEx system), which are linked to cognitive performance and to individual variations in behavior (reviewed in 1). Since its initial introduction 6, this design has proven particularly versatile and influential in the elucidation of various aspects concerning the neural correlates of the detrimental impact of emotional distraction on cognition, with a focus on working memory (WM), and of coping with such distraction 7,11, in both healthy 8-11 and clinical participants 12-14.
I. Task Design, Stimuli, and Experimental Protocol
Figure 1. General Diagram of the Delayed-Response Working Memory Task with Distraction (from 6, with permission). Three faces are used in the memoranda in order to strongly engage the dorsal executive system, and pairs of novel distracters are used in order to increase the impact of emotional distraction on WM performance and brain activity. The impact of emotional distracters can also be increased by presenting the pictures in color (not shown), and by pairing distracters with similar emotional and semantic content. In this context, careful attention should be paid to also match emotional and neutral pictures in basic properties, such as brightness and spatial frequency 15, to avoid introducing possible confounds. Participants are instructed to maintain their focus on the WM task while still processing the distracters, and to make quick and accurate responses to the probes by pressing a response button (1 = Old, 2 = New). For stimulus presentation, we used CIGAL (http://www.nitrc.org/projects/cigal/). The memoranda and probes can be presented in color or black & white.
II. Preparing the Subject for the Scan
All participants should provide written informed consent prior to running the experimental protocol, which should be approved by an Ethics Board.
Prior to Entering the Scanning Room
Entering the Scanning Room
Following the Scanning Session
III. Data Recording and Analysis
In the original study 6, we collected MRI data using a 4 Tesla General Electric scanner for MRI recordings, but for the more recent versions of the task we were also successful in collecting MRI data with a 1.5 T scanner 11. In the 4T scanner, series of 30 functional slices (voxel size = 4 x 4 x 4 mm) were acquired axially using an inverse-spiral pulse sequence (TR = 2000 ms; TE = 31 ms; field of view = 256 x 256mm), thus allowing for full-brain coverage. Similarly, in the 1.5 scanner, series of 28 functional slices (voxel size = 4 x 4 x 4 mm), were acquired axially using an echoplanar sequence (TR = 2000 ms; TE = 40 ms; field of view = 256 x 256 mm). High-resolution structural images were also acquired in axial orientation (in-plane resolution = 1 mm2; anatomical-functional ratio = 4:1).
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 (using a 8 x 8 x 8 mm Kernel); *basic quality assurance involved visual inspection of the data, to detect gross movements of the participants and motion-related artefacts in the data, as well as identification of volumes with unusual spikes in the MR signal. Individual and group-level statistical analyses involve comparisons of brain activity according to distracter type (emotional vs. neutral distraction). Moreover, correlations of brain imaging data with subjective or objective measures of distractibility (e.g., emotional and distractibility ratings and working memory performance)6,8,11 and/or scores indexing personality measures (e.g., trait anxiety)11 can also be performed, to investigate how brain activity co-varies with individual differences in those measures. Analyses in all of our studies using this protocol have typically focused on activity observed during the delay interval, when the distracters are presented, but activity time-locked to other events (e.g., probes) can also be investigated.
IV. Representative Results
Figure 2. Opposite Pattern of Activity in the Ventral vs. Dorsal Brain Systems in the Presence of Emotional Distraction (from 6, with permission). Emotional distracters produced enhanced activity in ventral affective brain regions (red blobs), such as the ventrolateral prefrontal cortex (vlPFC) and amygdala (not shown), while producing decreased activity in dorsal executive brain regions (blue blobs), such as dorsolateral prefrontal cortex (dlPFC) and lateral parietal cortex (LPC). The central image shows activation maps of the direct contrast between the most vs. the least distracting conditions (i.e., emotional vs. scrambled), superimposed on a high-resolution brain image displayed in a lateral view of the right hemisphere. The color horizontal bars at the bottom of the brain image indicate the gradient of t values of the activation maps. The line graphs show the time course of activity in representative dorsal and ventral brain regions (indicated by color-coded arrows). The grey rectangular boxes above the x-axes indicate the onset and duration of the memoranda, distracters, and probes, respectively. FFG = Fusiform Gyrus.
This experimental design provided initial brain imaging evidence that the detrimental effect of emotional distraction on the ongoing cognitive processes entails reciprocal modulations between the HotEmo ventral neural system and the ColdEx dorsal system. This dorso-ventral dissociation was linked to impaired WM performance in the presence of emotional distraction 6, has been systematically replicated in normal 8-11, clinical 12-14, and other altered conditions, such as sleep deprivation 10 and stress 18. Importantly, it was also shown to be specific to emotional, both positive and negative 17, but not to neutral distraction 8, 19. Given its versatility, this protocol and its variants can be used in the investigation of the neural correlates of responding and coping with emotional distraction in both healthy and clinical groups. In the latter cohort, it allows identification of the mechanisms underlying the exacerbated impact of emotional distraction observed in anxiety disorders, which are associated with increased emotional distractibility (e.g., PTSD, social phobia)12,20. The success of this protocol relies on the possibility to simultaneously explore activity in emotion- and cognition-related brain regions and of their interactions, as well as on its adaptability to select the specificity of emotional distraction according to the goals of the investigations.
No conflicts of interest declared.
FD was supported by a Young Investigator Award from the US National Alliance for Research on Schizophrenia and Depression and a CPRF Award from the Canadian Psychiatric Research Foundation.