This study tested the hypothesis that deficits in EF, which are believed to underlie goal directed behavior and regulation, would be associated with deficits in emotion regulation. Using a sample of patients (FTLD and AD) and neurologically healthy controls with a wide range of EF and an aversive acoustic startle stimulus known to produce sizeable emotional responding, we found support for this hypothesis both when the demand for regulation was implicit and participant used spontaneously recruited emotion regulatory strategies (our warned only condition) and when it was explicit and participants were instructed to suppress their responses (our warned with instructions to suppress condition). Importantly, there was considerable specificity to this finding in that: (a) EF only predicted emotional responding on the regulation trials, and not when the startle stimulus occurred unexpectedly without a warning; and (b) of four commonly used measures of EF -working-memory, Stroop, trail making, and verbal fluency - only deficits in verbal fluency (a measure of cognitive flexibility) predicted deficits in emotion regulation.
We had predicted that EF deficits would not be related to emotional responding to the unwarned
startle. This prediction was based on the view that emotional reactivity to simple stimuli such as the acoustic startle are largely subserved by brain stem and limbic circuits (Davis, Gendelman, Tischler, & Gendelman, 1982
), which are not assessed by EF measures. Additionally, we had predicted that EF deficits would be related to emotional regulation in the two regulation conditions, both when participants were free to use a regulatory strategy of their choice spontaneously, and in the suppression condition where participants are given explicit instructions to use suppression as emotion regulatory strategy. This prediction was based on the view that emotion regulation is subserved by frontal-subcortical circuits (Roberts, et al., 2004
; Rolls, 2000
; Stuss & Levine, 2002
), which are assessed by EF measures. Together these findings are also supportive of a differentiated view of emotional circuitry in the brain, namely that different circuits are involved for having emotional responses than for regulating these responses.
The finding that among EF measures, only verbal fluency predicted emotion regulation may seem surprising, but it underscores the fact that putative measures of EF are not interchangeable. Rather, they capture clinically, functionally and anatomically different aspects of EF (Miyake et al., 2000
; Royall et al., 2002
). For example the Stroop test, which assesses inhibition of a dominant response, might have been viewed as the most likely candidate for predicting emotion regulation. The result that Stroop performance did not correlate with emotion regulation underscores that the ability to mount a successful emotion regulatory response to an aversive auditory stimulus, both spontaneously and to suppress when instructed, involves more than just response inhibition. In our view, successful emotion regulation draws on a complex set of skills, including strategy formulation, behavioral monitoring, evaluation, and adjustment. Viewed from this perspective, there are similarities between the process of EF as indexed by generating words of a certain kind on the verbal fluency task, and down-regulating an emotion, insofar as both tests require the individual to be able to devise an advantageous strategy, to monitor ongoing performance, and to inhibit erroneous responses (Lezak et al., 2004
; Shimamura, 2000
; Troyer, Moscovitch, & Winokur, 1997
Although emotion down-regulation to acute aversive stimulus is arguably highly prototypical, there clearly are other kinds of emotion regulation and kinds of stimuli that occasion regulation. Additional research will be necessary to determine whether EF as measured by tests of verbal fluency is associated with the ability to engage in other kinds of emotion regulation (e.g., amplification, cognitive reappraisal and attentional control) and other kinds of stimuli (e.g., those that are more chronic, those that evoke different kinds of emotion).
In summary, were able to present evidence that the relationship between verbal fluency and EF was consistent across the three groups and across two different emotion regulatory conditions. Thus, we have confidence that these findings establish a true link between measures of verbal fluency and these two forms of emotion regulation. Furthermore, we demonstrated that the findings do not merely result from the measures associated with diagnosis, and we found that findings hold robust across two different emotion regulatory conditions.
Strengths and limitations
This study bridges the domains of cognitive and emotional functioning using a novel methodology that links neuropsychological tests of EF with emotional regulation in both neurological patients and normal controls. Because EF was measured using performance-based neuropsychological tests and emotion regulation was assessed using laboratory measures of emotional facial behavior and somatic muscle activity, concerns about shared method variance were minimized.
The study has several limitations that may have affected our findings. We tested only a subset of the available tests of EF and only a single emotion elicitor. Thus, our findings might have differed with other tests (e.g., N-back, Wisconsin Card Sort) and other elicitors (e.g., films, pictures). To provide a wide range of EF, we included patients with two kinds of dementia and neurologically-normal participants. Thus, our findings may not generalize to other neurological populations. Additionally, because the three startle conditions occurred in a fixed order, we cannot rule out order or habituation effects. Furthermore, individual patterns of neurodegeneration have not been characterized for the patients in this sample, thus, we cannot directly determine relationships between regional neural loss and deficits in our EF and emotion regulation measures. The fact that no diagnostic group differences emerged in our analyses could be due to small sample size, especially in the AD group. Finally, as noted above, our results establish a link between verbal fluency and the ability to down-regulate the emotional response to an acute aversive stimulus spontaneously and when instructed to suppress expressive responses. Thus, we cannot know the extent to which these findings generalize to other kinds of emotion regulation and to other emotional stimuli.