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Trait anxiety and the neural efficiency of manipulation in working memory.

Basten U, Stelzel C, Fiebach CJ - Cogn Affect Behav Neurosci (2012)

Bottom Line: Higher levels of anxiety were associated with stronger activation in two regions implicated in the goal-directed control of attention--that is, right dorsolateral prefrontal cortex (DLPFC) and left inferior frontal sulcus--and with stronger deactivation in a region assigned to the brain's default-mode network--that is, rostral-ventral anterior cingulate cortex.Furthermore, anxiety was associated with a stronger functional coupling of right DLPFC with ventrolateral prefrontal cortex.We interpret our findings as reflecting reduced processing efficiency in high-anxious individuals and point out the need to consider measures of functional integration in addition to measures of regional activation strength when investigating individual differences in neural efficiency.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, Goethe University, Postfach 11 19 32, Fach 128, 60054 Frankfurt am Main, Germany. basten@psych.uni-frankfurt.de

ABSTRACT
The present study investigates the effects of trait anxiety on the neural efficiency of working memory component functions (manipulation vs. maintenance) in the absence of threat-related stimuli. For the manipulation of affectively neutral verbal information held in working memory, high- and low-anxious individuals (N = 46) did not differ in their behavioral performance, yet trait anxiety was positively related to the neural effort expended on task processing, as measured by BOLD signal changes in fMRI. Higher levels of anxiety were associated with stronger activation in two regions implicated in the goal-directed control of attention--that is, right dorsolateral prefrontal cortex (DLPFC) and left inferior frontal sulcus--and with stronger deactivation in a region assigned to the brain's default-mode network--that is, rostral-ventral anterior cingulate cortex. Furthermore, anxiety was associated with a stronger functional coupling of right DLPFC with ventrolateral prefrontal cortex. We interpret our findings as reflecting reduced processing efficiency in high-anxious individuals and point out the need to consider measures of functional integration in addition to measures of regional activation strength when investigating individual differences in neural efficiency. With respect to the functions of working memory, we conclude that anxiety specifically impairs the processing efficiency of (control-demanding) manipulation processes (as opposed to mere maintenance). Notably, this study contributes to an accumulating body of evidence showing that anxiety also affects cognitive processing in the absence of threat-related stimuli.

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Effects of trait anxiety on brain activation during working memory manipulation in the whole-brain analysis, controlling for (nonsignificant) variation in performance. Trait anxiety predicts BOLD signal strength in the left inferior frontal sulcus (IFS; upper row) and in the rostral–ventral anterior cingulate cortex (rACC; lower row). (a) Statistical parametric maps are shown at a voxel-level threshold of p < .005. The x-coordinates refer to the Montreal Neurological Institute template brain included in the SPM5 software package. (b, c) Percent signal change extracted from the two regions illustrated in panel A. (b) Percent signal change for manipulation > maintenance, plotted against anxiety.performance—that is, the residual of trait anxiety from the regression on behavioral performance. (c) Comparison of mean percent signal change for the task (MP: manipulation > zero, dark gray) and the reference condition (MT: maintenance > zero, light gray) by the trait-anxiety group (median split). Error bars show the standard errors of the means
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Fig3: Effects of trait anxiety on brain activation during working memory manipulation in the whole-brain analysis, controlling for (nonsignificant) variation in performance. Trait anxiety predicts BOLD signal strength in the left inferior frontal sulcus (IFS; upper row) and in the rostral–ventral anterior cingulate cortex (rACC; lower row). (a) Statistical parametric maps are shown at a voxel-level threshold of p < .005. The x-coordinates refer to the Montreal Neurological Institute template brain included in the SPM5 software package. (b, c) Percent signal change extracted from the two regions illustrated in panel A. (b) Percent signal change for manipulation > maintenance, plotted against anxiety.performance—that is, the residual of trait anxiety from the regression on behavioral performance. (c) Comparison of mean percent signal change for the task (MP: manipulation > zero, dark gray) and the reference condition (MT: maintenance > zero, light gray) by the trait-anxiety group (median split). Error bars show the standard errors of the means

Mentions: The present study was conducted with 46 healthy volunteers who had previously participated in our study on the effects of anxiety on inhibitory control in the Stroop task (Basten et al., 2011). All were students of the University of Heidelberg, were right-handed, and had normal or corrected-to-normal vision, no structural brain abnormalities, and no history of psychiatric or neurological diseases, according to self-report in a telephone interview. Informed consent was obtained in conformity with the protocol approved by the local ethics committee, and the participants were paid for participation in the study. Of the 46 participants, 22 were female and 24 were male, and their ages ranged from 19 to 27 years (M = 22.3, SD = 2.0). Trait anxiety was assessed with the State–Trait Anxiety Inventory (STAI: Spielberger, Gorsuch, & Lushene, 1970; German: Laux, Glanzmann, Schaffner, & Spielberger, 1981) approximately 6 weeks prior to the study. The raw scores on this measure ranged from 24 to 46 (M = 33.3, SD = 5.7), which is comparable to the values of a normative German sample of similar age and education (M = 34.7, SD = 8.4; Laux et al., 1981). For the analysis of variance of the behavioral data and for the illustration of the imaging results in bar plots (see Figs. 2d and 3c below), the sample was median-split into a low-anxious and a high-anxious group, who differed significantly in trait anxiety scores (low-anxious M = 28.6, high-anxious M = 38.1), t(44) = 10.3, p < .001, but not in intelligence, as assessed using the Advanced Progressive Matrices (APM: Raven, Raven, & Court, 1998), t(44) = 0.70, p = .50. Furthermore, trait anxiety did not significantly differ between men (M = 33.0, SD = 6.2) and women (M = 33.7, SD = 5.2), t(44) = 0.389, p = .70. Accordingly, there was no significant difference in the frequency of males versus females in the groups of high-anxious (11 vs. 12) and low-anxious (13 vs. 10) individuals [χ2(1) = 0.348, p = .56].


Trait anxiety and the neural efficiency of manipulation in working memory.

Basten U, Stelzel C, Fiebach CJ - Cogn Affect Behav Neurosci (2012)

Effects of trait anxiety on brain activation during working memory manipulation in the whole-brain analysis, controlling for (nonsignificant) variation in performance. Trait anxiety predicts BOLD signal strength in the left inferior frontal sulcus (IFS; upper row) and in the rostral–ventral anterior cingulate cortex (rACC; lower row). (a) Statistical parametric maps are shown at a voxel-level threshold of p < .005. The x-coordinates refer to the Montreal Neurological Institute template brain included in the SPM5 software package. (b, c) Percent signal change extracted from the two regions illustrated in panel A. (b) Percent signal change for manipulation > maintenance, plotted against anxiety.performance—that is, the residual of trait anxiety from the regression on behavioral performance. (c) Comparison of mean percent signal change for the task (MP: manipulation > zero, dark gray) and the reference condition (MT: maintenance > zero, light gray) by the trait-anxiety group (median split). Error bars show the standard errors of the means
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Related In: Results  -  Collection

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Fig3: Effects of trait anxiety on brain activation during working memory manipulation in the whole-brain analysis, controlling for (nonsignificant) variation in performance. Trait anxiety predicts BOLD signal strength in the left inferior frontal sulcus (IFS; upper row) and in the rostral–ventral anterior cingulate cortex (rACC; lower row). (a) Statistical parametric maps are shown at a voxel-level threshold of p < .005. The x-coordinates refer to the Montreal Neurological Institute template brain included in the SPM5 software package. (b, c) Percent signal change extracted from the two regions illustrated in panel A. (b) Percent signal change for manipulation > maintenance, plotted against anxiety.performance—that is, the residual of trait anxiety from the regression on behavioral performance. (c) Comparison of mean percent signal change for the task (MP: manipulation > zero, dark gray) and the reference condition (MT: maintenance > zero, light gray) by the trait-anxiety group (median split). Error bars show the standard errors of the means
Mentions: The present study was conducted with 46 healthy volunteers who had previously participated in our study on the effects of anxiety on inhibitory control in the Stroop task (Basten et al., 2011). All were students of the University of Heidelberg, were right-handed, and had normal or corrected-to-normal vision, no structural brain abnormalities, and no history of psychiatric or neurological diseases, according to self-report in a telephone interview. Informed consent was obtained in conformity with the protocol approved by the local ethics committee, and the participants were paid for participation in the study. Of the 46 participants, 22 were female and 24 were male, and their ages ranged from 19 to 27 years (M = 22.3, SD = 2.0). Trait anxiety was assessed with the State–Trait Anxiety Inventory (STAI: Spielberger, Gorsuch, & Lushene, 1970; German: Laux, Glanzmann, Schaffner, & Spielberger, 1981) approximately 6 weeks prior to the study. The raw scores on this measure ranged from 24 to 46 (M = 33.3, SD = 5.7), which is comparable to the values of a normative German sample of similar age and education (M = 34.7, SD = 8.4; Laux et al., 1981). For the analysis of variance of the behavioral data and for the illustration of the imaging results in bar plots (see Figs. 2d and 3c below), the sample was median-split into a low-anxious and a high-anxious group, who differed significantly in trait anxiety scores (low-anxious M = 28.6, high-anxious M = 38.1), t(44) = 10.3, p < .001, but not in intelligence, as assessed using the Advanced Progressive Matrices (APM: Raven, Raven, & Court, 1998), t(44) = 0.70, p = .50. Furthermore, trait anxiety did not significantly differ between men (M = 33.0, SD = 6.2) and women (M = 33.7, SD = 5.2), t(44) = 0.389, p = .70. Accordingly, there was no significant difference in the frequency of males versus females in the groups of high-anxious (11 vs. 12) and low-anxious (13 vs. 10) individuals [χ2(1) = 0.348, p = .56].

Bottom Line: Higher levels of anxiety were associated with stronger activation in two regions implicated in the goal-directed control of attention--that is, right dorsolateral prefrontal cortex (DLPFC) and left inferior frontal sulcus--and with stronger deactivation in a region assigned to the brain's default-mode network--that is, rostral-ventral anterior cingulate cortex.Furthermore, anxiety was associated with a stronger functional coupling of right DLPFC with ventrolateral prefrontal cortex.We interpret our findings as reflecting reduced processing efficiency in high-anxious individuals and point out the need to consider measures of functional integration in addition to measures of regional activation strength when investigating individual differences in neural efficiency.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, Goethe University, Postfach 11 19 32, Fach 128, 60054 Frankfurt am Main, Germany. basten@psych.uni-frankfurt.de

ABSTRACT
The present study investigates the effects of trait anxiety on the neural efficiency of working memory component functions (manipulation vs. maintenance) in the absence of threat-related stimuli. For the manipulation of affectively neutral verbal information held in working memory, high- and low-anxious individuals (N = 46) did not differ in their behavioral performance, yet trait anxiety was positively related to the neural effort expended on task processing, as measured by BOLD signal changes in fMRI. Higher levels of anxiety were associated with stronger activation in two regions implicated in the goal-directed control of attention--that is, right dorsolateral prefrontal cortex (DLPFC) and left inferior frontal sulcus--and with stronger deactivation in a region assigned to the brain's default-mode network--that is, rostral-ventral anterior cingulate cortex. Furthermore, anxiety was associated with a stronger functional coupling of right DLPFC with ventrolateral prefrontal cortex. We interpret our findings as reflecting reduced processing efficiency in high-anxious individuals and point out the need to consider measures of functional integration in addition to measures of regional activation strength when investigating individual differences in neural efficiency. With respect to the functions of working memory, we conclude that anxiety specifically impairs the processing efficiency of (control-demanding) manipulation processes (as opposed to mere maintenance). Notably, this study contributes to an accumulating body of evidence showing that anxiety also affects cognitive processing in the absence of threat-related stimuli.

Show MeSH
Related in: MedlinePlus