Elsevier

NeuroImage

Volume 54, Issue 3, 1 February 2011, Pages 2481-2491
NeuroImage

Impact of transient emotions on functional connectivity during subsequent resting state: A wavelet correlation approach

https://doi.org/10.1016/j.neuroimage.2010.10.021Get rights and content

Abstract

The functional properties of resting brain activity are poorly understood, but have generally been related to self-monitoring and introspective processes. Here we investigated how emotionally positive and negative information differentially influenced subsequent brain activity at rest. We acquired fMRI data in 15 participants during rest periods following fearful, joyful, and neutral movies. Several brain regions were more active during resting than during movie-watching, including posterior/anterior cingulate cortices (PCC, ACC), bilateral insula and inferior parietal lobules (IPL). Functional connectivity at different frequency bands was also assessed using a wavelet correlation approach and small-world network analysis. Resting activity in ACC and insula as well as their coupling were strongly enhanced by preceding emotions, while coupling between ventral-medial prefrontal cortex and amygdala was selectively reduced. These effects were more pronounced after fearful than joyful movies for higher frequency bands. Moreover, the initial suppression of resting activity in ACC and insula after emotional stimuli was followed by a gradual restoration over time. Emotions did not affect IPL average activity but increased its connectivity with other regions. These findings reveal specific neural circuits recruited during the recovery from emotional arousal and highlight the complex functional dynamics of default mode networks in emotionally salient contexts.

Research highlights

►Transient emotions can modulate the brain activity in subsequent resting state. ►Activity in default network shows progressive recovery after emotional conditions. ►ACC-insula coupling during resting state is enhanced after fearful situations. ►Connectivity of IPL with several regions increases at rest after joyful situations. ►Emotion effect on interregional connectivity is specific for higher frequency band.

Introduction

Some brain regions are spontaneously more active during the awake-resting state than during cognitive tasks. These regions constitute the so-called ‘default mode network’ (DMN) and are thought to relate at least partly to introspective processes and homeostasis regulation (Raichle et al., 2001, Greicius et al., 2003, Buckner and Vincent, 2007, Fox and Raichle, 2007). This network includes the posterior and anterior cingulate cortices (PCC, ACC), medial and inferior parietal lobules (IPL), ventro-medial prefrontal cortex (vMPFC), and lateral temporal areas, all being consistently deactivated during demanding cognitive tasks such as working memory, language, or attention (Greicius et al., 2003, Greicius and Menon, 2004, Fox et al., 2005), relative to rest. Although the amount of decreases in DMN may depend on the task difficulty (Esposito et al., 2006) or the nature of preceding cognitive activity (Waites et al., 2005, Buckner et al., 2008), it is unknown how resting conditions are modified by particular states of mind or moods that are likely to have an impact on interoceptive processes and homeostasis. This issue is crucial to better understand the functional significance of the default mode (Raichle, 2009), as well as the pathological changes observed in neuropsychiatry conditions (Zhang and Raichle, 2010).

Here we investigated how prior emotions (positive or negative) alter spontaneous brain activity and large-scale network connectivity during subsequent rest. Emotions are pervasive in daily life and exert long-lasting effects on cognition, attention, and motivation (Dolan, 2002). Thus, emotional experiences and moods are likely to influence the way we process information through attentional, perceptual, or mnesic biases (Vuilleumier, 2005). However, unlike moods, emotions are defined as transient physiological events (Scherer, 2005), and their impact on subsequent mental activity is poorly known. Most neuroimaging studies on emotion processing have typically focused on phasic responses to brief emotional stimuli (pictures, faces), but it is intuitively evident that even transient emotions can have lingering effects on mental and physiological states. Recent findings suggest that sad mood may decrease connectivity between areas belonging to the DMN (Harrison et al., 2008), whereas prior exposure to emotionally arousing pictures may reduce the magnitude of activation in parietal areas during rest (Pitroda et al., 2008). However, the pattern and dynamics of changes induced by transient emotions on activity and connectivity of the extended DMN still remain unclear. Measures of functional connectivity (based on temporal correlations between distant regions) are particularly useful to evaluate spontaneous fluctuations throughout the brain (Greicius et al., 2003, van de Ven et al., 2004, Achard et al., 2006), and have commonly been used to study the DMN in healthy controls and neurological disorders (Greicius et al., 2004, Greicius et al., 2007).

The main goal of our study was to determine the effects of positive (joy) and negative (fear) emotions induced by short movie excerpts on subsequent brain activity and interregional connectivity within the DMN. Specifically, we used fMRI with wavelet correlation analysis and small-world connectivity methods to investigate how the ‘resting state’ is altered and then returns to a spontaneous ‘default mode’ after emotional movies, and to determine whether such changes differ depending on the preceding emotion type.

Section snippets

Participants

We recruited 15 volunteers (4 male) without any history of neurological or psychiatric disorders, age between 18 and 36 years (mean = 23.8), and right-handed. All participants signed a consent form approved by the local ethics committee.

Emotional stimuli

The experimental protocol consisted of short video clips alternating with resting periods (see below for details of the procedure). In order to induce different emotions before each resting period, we created a series of video clips by editing popular movies or TV

Behavioral results

After each resting period, the participants classified their predominant mental activity during the preceding 90 s of rest by choosing among four possible options: a) movie content, b) personal issues, c) experiment environment such as MRI noise and settings, and d) sleepiness or struggle against sleep. There were 6 resting blocks for each emotion type, after which this question was asked. Fig. 2 shows the mean number of each possible response for each resting condition averaged across our 15

Discussion

We examined brain activity and functional connectivity during different rest conditions, following exposure to situations with varying emotional content. Because complex mental states like emotions may have lingering effects and can influence the processing of subsequent information through perceptual or memory biases (Dolan, 2002), our study aimed at determining the impact of transient (positive and negative) emotions on the following resting states. Our findings show that emotions induced by

Conclusion

In summary, by demonstrating that short emotional events may have prolonged effects on spontaneous brain states at rest, our study highlights the dynamic structure of DMN and reveals specific networks associated with emotion regulation mechanisms. These findings have important implications for understanding the functional role of the DMN and investigating the impact of emotional stressors in psychopathological conditions, but also call for careful control of emotional context in imaging studies

Acknowledgments

This work was supported by grants from the Swiss National Science Foundation (#310000-114008 to S.S.; #PP00P2-123438 to D.V.D.V.; and National Center of Competence in Research for Affective Sciences: #51NF40-104897), and by the Academic Society of Geneva (Foremane Fund).

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