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Articles, Behavioral/Cognitive

When the Sense of Smell Meets Emotion: Anxiety-State-Dependent Olfactory Processing and Neural Circuitry Adaptation

Elizabeth A. Krusemark, Lucas R. Novak, Darren R. Gitelman and Wen Li
Journal of Neuroscience 25 September 2013, 33 (39) 15324-15332; DOI: https://doi.org/10.1523/JNEUROSCI.1835-13.2013
Elizabeth A. Krusemark
1Department of Psychology and
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Lucas R. Novak
1Department of Psychology and
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Darren R. Gitelman
3Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, Illinois 60611
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Wen Li
1Department of Psychology and
2the Waisman Center, University of Wisconsin-Madison, Madison, Wisconsin 53706, and
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    Figure 1.

    Study design. A, Olfactory stimuli consisted of neutral odors (pure and mixture odorants) and negative odors (filler items). B, Each participant underwent a series of seven events through the study. Odor ratings (Steps I and VII) were performed outside the scanner and the others inside the scanner. C, Paradigm of the odor detection task. The task was conducted in both fMRI runs immediately before and after a 6-min-long anxiety induction procedure. Respiration was recorded throughout the task.

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    Figure 2.

    Behavioral results. A, State anxiety ratings increased after induction. B, Odor valence ratings became more negative for neutral odors after induction. C, Valence rating change specific to neutral odors (neutral − negative odors) correlated with magnitude of induced anxiety (post − pre). D, RTs in the odor detection task slowed down for neutral (vs air) trials after induction. Error bar indicates SEM. *p > 0.05.

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    Figure 3.

    Conventional SPM results and PPI results. A, Right olfactory OFC exhibited augmented activity and heightened functional coupling with the right amygdala (Amyg) in response to neutral odors (vs air) from pre-induction to post-induction. B, Right pgACC showed response enhancement to neutral odors (vs air) from pre-induction to post-induction, correlated positively with the magnitude of induced anxiety. Activations superimposed on the group average T1 image (display threshold p < 0.005 uncorrected). *p < 0.05.

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    Figure 4.

    Model specification for DCM analyses. A five-region DCM was specified with bidirectional endogenous connections between all regions and with driving inputs of odors/air into both the APC and amygdala (models 1, 2, 5, and 6) or the APC alone (models 3, 4, 7, and 8). Sources within each model were olfactory regions (APC, PPC, and olfactory OFC) and emotion regions (amygdala/Amyg and pgACC). Models 1–8 contained a pgACC and olfactory OFC connection (illustrated as a gray line), which was absent in models 9–16. Olf. OFC, Olfactory OFC.

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    Figure 5.

    DCM results: Neural circuitry for olfaction and emotion integration in anxiety. A, Model 15 emerged as the winner with maximal expected and exceedance probabilities among the 16 models specified. B, Model 15 at pre-induction baseline. Left column, Emotion areas. Right column, Olfactory areas (arranged according to the hierarchical level). Black solid lines and gray dashed lines represent significant connections (with intrinsic connectivity parameters alongside) and theoretical but nonsignificant connections, respectively. C, Model 15 at post-induction. Bolstered intrinsic connections after anxiety induction are marked as green solid lines (with intrinsic connectivity parameters alongside). The initially nonsignificant PPC → amygdala projection was further weakened by anxiety (blue dashed line). Red intercepting lines represent significant modulatory effects of neutral odor (vs air) in post-induction (vs pre-induction). D, Olfactory neural circuit in anxiety. Yellow lines represent intrinsic connections initially significant, with green lines for those that became significant after anxiety induction, and red intercepting lines for modulation resulting from neutral odors at post-induction. Amyg, Amygdala; Olf. OFC, olfactory OFC. *p < 0.05. **p < 0.01. ***p < 0.005. ****p < 0.001.

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    Table 1.

    Parameter estimates of intrinsic and modulatory parameters for Model 15

    PathwayIntrinsic connectionsModulatory parameters
    Mean (SD) Pre/PostT, p (Post/Pre)Neutral (Pre/Post)/Mean (SD)Air (Pre/Post)/Mean (SD)Anxiety × Odor (F, p)
    APC → Amyg−0.09 (0.23)/0.20 (0.13)****3.33, 0.007**0.002 (0.061)/0.106 (0.076)0.063 (0.073)/0.080 (0.085)9.52, 0.01**
    APC → PPC0.007 (0.33)/0.34 (0.09)****3.06, 0.01*0.044 (0.059)/0.070 (0.052)0.058 (0.072)/0.045 (0.056)1.56, 0.24
    PPC → Amyg0.05 (0.10)/−0.04 (0.13)−2.28, 0.04*0.004 (0.007)/0.008 (0.009)0.001 (0.010)/0.005 (0.008)0.003, 0.96
    PPC → APC−0.001 (0.07)/0.03 (0.11)0.88, 0.390.002 (0.003)/0.001 (0.002)−0.001 (0.007)/0.001 (0.001)1.33, 0.27
    PPC → Olf. OFC0.17 (0.16)***/0.16 (0.12)****−0.16, 0.880.003 (0.024)/0.018 (0.019)0.005 (0.016)/0.003 (0.005)3.03, 0.11
    Amyg → APC−0.01 (0.09)/0.03 (0.05)†1.12, 0.29−0.002 (0.009)/0.001 (0.001)−0.001 (0.006)/0.001 (0.001)0.79, 0.39
    Amyg → PPC0.14 (0.17)*/0.07 (0.04)****−1.69, 0.12−0.001 (0.009)/0.005 (0.006)0.003 (0.005)/0.003 (0.004)4.78, 0.05*
    Amyg → Olf. OFC0.07 (0.08)*/0.12 (0.06)****1.73, 0.110.002 (0.021)/0.019 (0.020)0.002 (0.017)/0.004 (0.007)1.49, 0.25
    Amyg → pgACC0.24 (0.18)****/0.23 (0.26)**−0.72, 0.940.006 (0.009)/0.018 (0.019)0.010 (0.017)/0.018 (0.024)0.13, 0.72
    Olf. OFC → Amyg0.004 (0.03)/−0.02 (0.03)†−1.79, 0.10†0.002 (0.006)/0.004 (0.001)−0.001 (0.004)/0.001 (0.001)1.42, 0.36
    Olf. OFC → PPC0.03 (0.04)*/0.03 (0.06)†0.21, 0.84−0.001 (0.003)/0.001 (0.001)0.001 (0.002)/0.001 (0.001)0.58, 0.46
    pgACC → Amyg0.02 (0.04)/−0.002 (0.04)−1.29, 0.220.001 (0.002)/0.001 (0.001)0.002 (0.006)/0.001 (0.001)0.35, 0.57
    • ↵*p < 0.05;

    • ↵**p < 0.01;

    • ↵***p < 0.005;

    • ↵****p < 0.001;

    • ↵†p < 0.10; two-tailed. Amyg, Amygdala; APC, anterior piriform; Olf. OFC, olfactory OFC; pgACC, pregenual ACC; PPC, posterior piriform.

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The Journal of Neuroscience: 33 (39)
Journal of Neuroscience
Vol. 33, Issue 39
25 Sep 2013
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When the Sense of Smell Meets Emotion: Anxiety-State-Dependent Olfactory Processing and Neural Circuitry Adaptation
Elizabeth A. Krusemark, Lucas R. Novak, Darren R. Gitelman, Wen Li
Journal of Neuroscience 25 September 2013, 33 (39) 15324-15332; DOI: 10.1523/JNEUROSCI.1835-13.2013

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When the Sense of Smell Meets Emotion: Anxiety-State-Dependent Olfactory Processing and Neural Circuitry Adaptation
Elizabeth A. Krusemark, Lucas R. Novak, Darren R. Gitelman, Wen Li
Journal of Neuroscience 25 September 2013, 33 (39) 15324-15332; DOI: 10.1523/JNEUROSCI.1835-13.2013
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