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. 2017 Mar;38(3):1125-1139.
doi: 10.1002/hbm.23440. Epub 2016 Oct 27.

Default mode network deactivation during odor-visual association

Prasanna R Karunanayaka  1 , Donald A Wilson  2   3 , Michael J Tobia  1 , Brittany E Martinez  1 , Mark D Meadowcroft  1   4 , Paul J Eslinger  1   5 , Qing X Yang  1   4
Affiliations

Default mode network deactivation during odor-visual association

Prasanna R Karunanayaka et al. Hum Brain Mapp. 2017 Mar.

Abstract

Default mode network (DMN) deactivation has been shown to be functionally relevant for goal-directed cognition. In this study, the DMN's role during olfactory processing was investigated using two complementary functional magnetic resonance imaging (fMRI) paradigms with identical timing, visual-cue stimulation, and response monitoring protocols. Twenty-nine healthy, non-smoking, right-handed adults (mean age = 26 ± 4 years, 16 females) completed an odor-visual association fMRI paradigm that had two alternating odor + visual and visual-only trial conditions. During odor + visual trials, a visual cue was presented simultaneously with an odor, while during visual-only trial conditions the same visual cue was presented alone. Eighteen of the twenty-nine participants (mean age = 27.0 ± 6.0 years, 11 females) also took part in a control no-odor fMRI paradigm that consisted of a visual-only trial condition which was identical to the visual-only trials in the odor-visual association paradigm. Independent Component Analysis (ICA), extended unified structural equation modeling (euSEM), and psychophysiological interaction (PPI) were used to investigate the interplay between the DMN and olfactory network. In the odor-visual association paradigm, DMN deactivation was evoked by both the odor + visual and visual-only trial conditions. In contrast, the visual-only trials in the no-odor paradigm did not evoke consistent DMN deactivation. In the odor-visual association paradigm, the euSEM and PPI analyses identified a directed connectivity between the DMN and olfactory network which was significantly different between odor + visual and visual-only trial conditions. The results support a strong interaction between the DMN and olfactory network and highlights the DMN's role in task-evoked brain activity and behavioral responses during olfactory processing. Hum Brain Mapp 38:1125-1139, 2017. © 2016 Wiley Periodicals, Inc.

Keywords: default mode network (DMN); fMRI; olfaction.

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Figures

Figure 1
Figure 1
(a) The odor–visual association or four‐intensity fMRI paradigm with alternating odor + visual and visual‐only trial conditions. During odor + visual trials, the visual cue, “Smell?,” was presented on an LCD screen paired with lavender odor. During visual‐only trials the same visual cue was presented by itself. The word “Rest” was displayed on the LCD screen during the rest period. Four intensities of lavender odorant were presented starting with the weakest intensity and ending with the strong intensity. Each intensity was presented three times before the next odor intensities were presented in a progressive manner from weakest to strong. A constant fresh airflow of 8 L/min was maintained throughout all conditions (including the “Rest”) to avoid tactile or thermal stimulation. Participants had to perform a button press response to indicate the presence/absence of an odor during odor + visual and visual‐only trial conditions. (b) Eighteen of the study participants took part in the control no‐odor paradigm consisting of visual‐only trials during which a constant fresh airflow of 8 L/min was maintained. These visual‐only trials were identical in timing, visual‐cue stimulation and response motoring structure to that of the odor–visual association paradigm. Participants were also asked to respond to the presence or absence of an odor during each visual‐only trial. [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 2
Figure 2
The primary olfactory network (PON1 and PON2) and the Default Mode Network (DMN) behavior during the odor–visual association or four‐intensity paradigm. PON1 (i) and PON2 (ii) showed task‐related behavior for both the odor + visual and visual‐only trial conditions. The DMN (iii) was deactivated or suppressed and opposite in phase during both odor + visual and visual‐only trial conditions. In contrast to the PON1 and PON2 behavior, the DMN was active during rest conditions. Hippocampus/parahippocampal cortex was differentially synchronized with PON1 and the DMN during odor + visual (or visual‐only) trials and interleaved rest conditions. DMN, Default Mode Network. [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 3
Figure 3
Estimated hemodynamic response functions (HRFs) for each network using IC time‐courses shown in Figure 2 (right hand side) where PON1 and PON2 exhibited almost identical temporal behavior during odor + visual and visual‐only conditions. Similarly, the DMN suppression was almost identical during odor + visual and visual‐only conditions. Therefore, a single composite HRF was estimated for both conditions in each network to investigate phase differences between the olfactory networks and the DMN. [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 4
Figure 4
The primary olfactory PON1 (i) and PON2 (ii) networks during the control no‐odor paradigm. In contrast to the odor–visual association paradigm (Fig. 3), PON1 and PON2 showed high intersubject variability in its temporal behavior and also inconsistent task‐related behavior. The data driven method was unable to estimate the HRF and thus single‐trial β estimates for visual‐only trial conditions in this paradigm. The DMN (iii) behavior during the no‐odor paradigm. In contrast to the odor–visual association paradigm, the DMN behavior persisted across both the rest and visual‐only conditions. The temporal behavior of the DMN was uncoupled from the task on‐off reference time course, and mostly unsuppressed in a random fashion. [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 5
Figure 5
Network responses during odor + visual and visual‐only trial conditions in terms of average single trial β estimates. The average was first across odor + visual and visual‐only trial conditions and then across subjects. All three networks showed no significant differences between average β estimates of odor + visual and visual‐only conditions, implying comparable network behavior during both trial conditions. Overall, PON2 had greater network activation (P < 0.001) when compared with PON1 during both the odor + visual and visual‐only conditions. [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 6
Figure 6
The DMN activity in terms of single trial average β estimates during rest conditions before respective odor + visual and visual‐only trial conditions. The mean activity was significantly different between the two types of trial conditions. [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 7
Figure 7
The optimal euSEM represents the interaction between the DMN and PON1 during the odor–visual association paradigm. The subsequent PPI analysis revealed that this connectivity is modulated for odor + visual and visual only trial conditions. [Color figure can be viewed at http://wileyonlinelibrary.com]
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