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Increased anterior insula activity in anxious individuals is linked to diminished perceived control.

Alvarez RP, Kirlic N, Misaki M, Bodurka J, Rhudy JL, Paulus MP, Drevets WC - Transl Psychiatry (2015)

Bottom Line: Anticipation of unpredictable threat resulted in increased skin conductance responses, anxiety ratings and enhanced activation in bilateral insula, anterior midcingulate cortex (aMCC) and bed nucleus of the stria terminalis.Individuals with greater anxiety proneness and less perceived control showed greater activity in dorsal anterior insula (dAI).Increased dAI activity was associated with increased activity in aMCC, which correlated with increased exploratory behavior.

View Article: PubMed Central - PubMed

Affiliation: 1] Laureate Institute for Brain Research, Tulsa, OK, USA [2] Faculty of Community Medicine, The University of Tulsa, Tulsa, OK, USA.

ABSTRACT
Individuals with high-trait anxiety frequently report decreased perceived control. However, it is unclear how these processes are instantiated at a neural level. Prior research suggests that individuals prone to anxiety may have exaggerated activity in the anterior insula and altered activity in the cingulate cortex during anticipation of aversive events. Thus, we hypothesized that anxiety proneness influences anterior insula activation during anticipation of unpredictable threat through decreased perceived control. Forty physically healthy adults underwent neuroimaging while they explored computer-simulated contexts associated either with or without the threat of an unpredictable shock. Skin conductance, anxiety ratings and blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging were used to assess responses to threat versus no threat. Perceived control was measured using the Anxiety Control Questionnaire-Revised. Mediation analysis examined how anxiety proneness influenced BOLD activity. Anticipation of unpredictable threat resulted in increased skin conductance responses, anxiety ratings and enhanced activation in bilateral insula, anterior midcingulate cortex (aMCC) and bed nucleus of the stria terminalis. Individuals with greater anxiety proneness and less perceived control showed greater activity in dorsal anterior insula (dAI). Perceived control mediated the relationship between anxiety proneness and dAI activity. Increased dAI activity was associated with increased activity in aMCC, which correlated with increased exploratory behavior. Results provide evidence that exaggerated insula activation during the threat of unpredictable shock is directly related to low perceived control in anxiety-prone individuals. Perceived control thus may constitute an important treatment target to modulate insula activity during anxious anticipation in anxiety-disordered individuals.

No MeSH data available.


Related in: MedlinePlus

(a and b) Dorsal anterior insula (dAI) activation is positively correlated with anxiety proneness and negatively correlated with perceived control. (c) Anxiety proneness, as measured by trait anxiety scores, is inversely correlated with perceived control over aversive events. The numeral two indicates two overlapping data points. (d) Increased activity in anterior midcingulate cortex (aMCC) was associated with greater exploratory behavior in the threat context. Activation values on the y axis are beta coefficients representing mean percent signal change during anticipation of unpredictable threat (threat > safe). (e) Schematic representation of the mediation model. The pathway from STAI-T to ACQ-R (path a) and then from ACQ-R to dorsal anterior insula (path b) represents the indirect effect of anxiety proneness on dAI activity through perceived control (quantified as the product of paths a and b). The pathway from STAI-T to dAI (path c') represents the direct effect of anxiety proneness on dAI activity. Model coefficients are reported in unstandardized form, thus they map directly onto the measurement scales used. A 95% confidence interval (CI) for the indirect effect (ab) does not contain and is entirely above zero, thus providing evidence that perceived control serves as a mediator of the effect of anxiety proneness on dAI activity. ACQ-R, Anxiety Control Questionnaire-Revised; STAI-T, Spielberger State-Trait Anxiety Inventory.
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fig3: (a and b) Dorsal anterior insula (dAI) activation is positively correlated with anxiety proneness and negatively correlated with perceived control. (c) Anxiety proneness, as measured by trait anxiety scores, is inversely correlated with perceived control over aversive events. The numeral two indicates two overlapping data points. (d) Increased activity in anterior midcingulate cortex (aMCC) was associated with greater exploratory behavior in the threat context. Activation values on the y axis are beta coefficients representing mean percent signal change during anticipation of unpredictable threat (threat > safe). (e) Schematic representation of the mediation model. The pathway from STAI-T to ACQ-R (path a) and then from ACQ-R to dorsal anterior insula (path b) represents the indirect effect of anxiety proneness on dAI activity through perceived control (quantified as the product of paths a and b). The pathway from STAI-T to dAI (path c') represents the direct effect of anxiety proneness on dAI activity. Model coefficients are reported in unstandardized form, thus they map directly onto the measurement scales used. A 95% confidence interval (CI) for the indirect effect (ab) does not contain and is entirely above zero, thus providing evidence that perceived control serves as a mediator of the effect of anxiety proneness on dAI activity. ACQ-R, Anxiety Control Questionnaire-Revised; STAI-T, Spielberger State-Trait Anxiety Inventory.

Mentions: The magnitude of the BOLD signal elevation in dAI correlated positively with the extent of anxiety proneness (STAI-T: r=0.32, P<0.05, Figure 3a) and negatively with perceived control (ACQ-R: r=−0.40, P<0.05, Figure 3b). In contrast, the corresponding correlations with BOLD activity in the vAI were not significant (STAI-T: r=−0.15, P=0.36; ACQ-R: r=0.20, P=0.21). Moreover, the levels of anxiety proneness correlated inversely with perceived control (r=−0.73, P<0.001, Figure 3c). The magnitude of the BOLD activity change in the dAI correlated positively with that of the aMCC (r=0.32, P<0.05), but was not significantly correlated with that of the pMCC (r=0.29, P=0.07). In addition, greater aMCC activation was associated with increased time spent exploring the threat context during AUT (r=0.43, P<0.01, Figure 3d). By contrast the corresponding correlation with pMCC activation was not significant (r=0.24, P=0.14). Note that no significant difference was observed between threat and safe contexts in time spent exploring overall (t(39)=0.14, P=0.89, Supplementary Figure S2).


Increased anterior insula activity in anxious individuals is linked to diminished perceived control.

Alvarez RP, Kirlic N, Misaki M, Bodurka J, Rhudy JL, Paulus MP, Drevets WC - Transl Psychiatry (2015)

(a and b) Dorsal anterior insula (dAI) activation is positively correlated with anxiety proneness and negatively correlated with perceived control. (c) Anxiety proneness, as measured by trait anxiety scores, is inversely correlated with perceived control over aversive events. The numeral two indicates two overlapping data points. (d) Increased activity in anterior midcingulate cortex (aMCC) was associated with greater exploratory behavior in the threat context. Activation values on the y axis are beta coefficients representing mean percent signal change during anticipation of unpredictable threat (threat > safe). (e) Schematic representation of the mediation model. The pathway from STAI-T to ACQ-R (path a) and then from ACQ-R to dorsal anterior insula (path b) represents the indirect effect of anxiety proneness on dAI activity through perceived control (quantified as the product of paths a and b). The pathway from STAI-T to dAI (path c') represents the direct effect of anxiety proneness on dAI activity. Model coefficients are reported in unstandardized form, thus they map directly onto the measurement scales used. A 95% confidence interval (CI) for the indirect effect (ab) does not contain and is entirely above zero, thus providing evidence that perceived control serves as a mediator of the effect of anxiety proneness on dAI activity. ACQ-R, Anxiety Control Questionnaire-Revised; STAI-T, Spielberger State-Trait Anxiety Inventory.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4490294&req=5

fig3: (a and b) Dorsal anterior insula (dAI) activation is positively correlated with anxiety proneness and negatively correlated with perceived control. (c) Anxiety proneness, as measured by trait anxiety scores, is inversely correlated with perceived control over aversive events. The numeral two indicates two overlapping data points. (d) Increased activity in anterior midcingulate cortex (aMCC) was associated with greater exploratory behavior in the threat context. Activation values on the y axis are beta coefficients representing mean percent signal change during anticipation of unpredictable threat (threat > safe). (e) Schematic representation of the mediation model. The pathway from STAI-T to ACQ-R (path a) and then from ACQ-R to dorsal anterior insula (path b) represents the indirect effect of anxiety proneness on dAI activity through perceived control (quantified as the product of paths a and b). The pathway from STAI-T to dAI (path c') represents the direct effect of anxiety proneness on dAI activity. Model coefficients are reported in unstandardized form, thus they map directly onto the measurement scales used. A 95% confidence interval (CI) for the indirect effect (ab) does not contain and is entirely above zero, thus providing evidence that perceived control serves as a mediator of the effect of anxiety proneness on dAI activity. ACQ-R, Anxiety Control Questionnaire-Revised; STAI-T, Spielberger State-Trait Anxiety Inventory.
Mentions: The magnitude of the BOLD signal elevation in dAI correlated positively with the extent of anxiety proneness (STAI-T: r=0.32, P<0.05, Figure 3a) and negatively with perceived control (ACQ-R: r=−0.40, P<0.05, Figure 3b). In contrast, the corresponding correlations with BOLD activity in the vAI were not significant (STAI-T: r=−0.15, P=0.36; ACQ-R: r=0.20, P=0.21). Moreover, the levels of anxiety proneness correlated inversely with perceived control (r=−0.73, P<0.001, Figure 3c). The magnitude of the BOLD activity change in the dAI correlated positively with that of the aMCC (r=0.32, P<0.05), but was not significantly correlated with that of the pMCC (r=0.29, P=0.07). In addition, greater aMCC activation was associated with increased time spent exploring the threat context during AUT (r=0.43, P<0.01, Figure 3d). By contrast the corresponding correlation with pMCC activation was not significant (r=0.24, P=0.14). Note that no significant difference was observed between threat and safe contexts in time spent exploring overall (t(39)=0.14, P=0.89, Supplementary Figure S2).

Bottom Line: Anticipation of unpredictable threat resulted in increased skin conductance responses, anxiety ratings and enhanced activation in bilateral insula, anterior midcingulate cortex (aMCC) and bed nucleus of the stria terminalis.Individuals with greater anxiety proneness and less perceived control showed greater activity in dorsal anterior insula (dAI).Increased dAI activity was associated with increased activity in aMCC, which correlated with increased exploratory behavior.

View Article: PubMed Central - PubMed

Affiliation: 1] Laureate Institute for Brain Research, Tulsa, OK, USA [2] Faculty of Community Medicine, The University of Tulsa, Tulsa, OK, USA.

ABSTRACT
Individuals with high-trait anxiety frequently report decreased perceived control. However, it is unclear how these processes are instantiated at a neural level. Prior research suggests that individuals prone to anxiety may have exaggerated activity in the anterior insula and altered activity in the cingulate cortex during anticipation of aversive events. Thus, we hypothesized that anxiety proneness influences anterior insula activation during anticipation of unpredictable threat through decreased perceived control. Forty physically healthy adults underwent neuroimaging while they explored computer-simulated contexts associated either with or without the threat of an unpredictable shock. Skin conductance, anxiety ratings and blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging were used to assess responses to threat versus no threat. Perceived control was measured using the Anxiety Control Questionnaire-Revised. Mediation analysis examined how anxiety proneness influenced BOLD activity. Anticipation of unpredictable threat resulted in increased skin conductance responses, anxiety ratings and enhanced activation in bilateral insula, anterior midcingulate cortex (aMCC) and bed nucleus of the stria terminalis. Individuals with greater anxiety proneness and less perceived control showed greater activity in dorsal anterior insula (dAI). Perceived control mediated the relationship between anxiety proneness and dAI activity. Increased dAI activity was associated with increased activity in aMCC, which correlated with increased exploratory behavior. Results provide evidence that exaggerated insula activation during the threat of unpredictable shock is directly related to low perceived control in anxiety-prone individuals. Perceived control thus may constitute an important treatment target to modulate insula activity during anxious anticipation in anxiety-disordered individuals.

No MeSH data available.


Related in: MedlinePlus