Elsevier

NeuroImage

Volume 55, Issue 1, 1 March 2011, Pages 247-252
NeuroImage

The impact of anxiety on the neural processing of respiratory sensations

https://doi.org/10.1016/j.neuroimage.2010.11.050Get rights and content

Abstract

Previous studies demonstrated that anxiety considerably impacts the reported perceptions of respiratory sensations. A novel feature of the current study is exploring the impact of anxiety on the neural processing of respiratory sensations elicited by short inspiratory occlusions during different affective contexts. Using high-density EEG, respiratory-related evoked potentials (RREP) were recorded in 23 low and 23 matched higher anxious individuals when viewing unpleasant or neutral picture series. Low anxious individuals showed the expected pattern of reduced magnitudes of later RREP components P2 and P3 during the unpleasant compared to the neutral affective context (p < 0.05 and p < 0.01). In contrast, higher anxious individuals showed greater magnitudes of P2 and P3 during the unpleasant compared to the neutral affective context (p's < 0.05). Moreover, higher anxiety levels were correlated with greater magnitudes for P2 (r = 0.44, p < 0.01) and P3 (r = 0.54, p < 0.001) during the unpleasant relative to the neutral affective context. Earlier components of the RREP (Nf, P1, N1) were not affected by anxiety. This study demonstrates that anxiety affects the later, higher-order neural processing of respiratory sensations, but not its earlier, first-order sensory processing. These findings might represent a neural mechanism that underlies the increased perception of respiratory sensations in anxious individuals.

Research Highlights

► Low anxious subjects show reduced P2, P3 in unpleasant vs. neutral affective context. ► High anxious subjects show greater P2, P3 in unpleasant vs. neutral affective context. ► Anxiety level correlates with magnitudes for P2 and P3. ► Anxiety affects higher-order neural processing of respiratory sensations.

Introduction

The accurate perception of respiratory sensations is of considerable importance for successful self-management and clinical treatment of respiratory diseases such as asthma or chronic obstructive pulmonary disease (COPD). It motivates patients to initiate appropriate health behavior such as seeking medical (self-) treatment timely and in adequate doses (Banzett et al., 2000). Reduced perception of initial bronchoconstriction and dyspnea in patients with asthma, for example, might lead to increased morbidity due to delayed or inadequate medication use, delayed visits to the physician or emergency department and might even result in near-fatal attacks (Barnes, 1994, Feldman et al., 2007, Kifle et al., 1997, Kikuchi et al., 1994, Magadle et al., 2002). However, over-perception of respiratory sensations can also have negative health effects by leading to excessive use of medication or activity avoidance and resulting deconditioning (Main et al., 2003, Global Initiative for Chronic Obstructive Lung Disease (GOLD), 2008).

A growing body of literature suggests that psychological symptoms such as anxiety are not only frequent comorbidities in patients with respiratory disease (Maurer et al., 2008, Scott et al., 2007), but also affect the perception of respiratory symptoms (Chetta et al., 2005, Janssens et al., 2009, Rietveld, 1998, von Leupoldt and Dahme, 2007). Recent studies in healthy volunteers and patients with asthma or COPD have demonstrated that individuals characterized by high levels of anxiety report more respiratory sensations than low anxious individuals, regardless of their baseline pulmonary status or experimentally induced ventilatory changes (De Peuter et al., 2008, Giardino et al., 2010, Li et al., 2006, Livermore et al., 2008, Spinhoven et al., 1997, Vögele and von Leupoldt, 2008). This increased or inaccurate perception of respiratory symptoms in high anxious individuals has been reported to be particularly prominent in unpleasant compared to neutral or pleasant affective contexts (Janssens et al., 2009, Bogaerts et al., 2005, Van den Bergh et al., 2004).

However, whether anxiety is associated with measurable differences in the neural processing of respiratory signals remains unknown. Because inaccurate perception of respiratory sensations has critical implications for both self-management and clinical treatment, the present study firstly examined the effects of anxiety on neural correlates of respiratory perception by using the respiratory-related evoked potential (RREP) extracted from the electroencephalogram (EEG). The RREP is a measure of cerebral cortical activity elicited by short inspiratory occlusions (Chan and Davenport, 2010, Davenport et al., 1986, Huang et al., 2008, Logie et al., 1998, Redolfi et al., 2005). The early RREP components Nf, P1 and N1 (< 130 ms post stimulus) reflect the initial arrival and first-order sensory processing of afferent respiratory signals in sensorimotor regions. The later components P2 and P3 (> 150 ms post stimulus) characterize subsequent higher-order cognitive processing in other associative cortical areas (Chan and Davenport, 2010, von Leupoldt et al., 2010a) and are vulnerable to cognitive processes not related to respiration per se such as attentional distraction or emotion processing (Davenport et al., 2007, Harver et al., 1995, Webster and Colrain, 2000, von Leupoldt et al., 2010b).

We compared RREPs between low and higher anxious, healthy individuals, which were recorded during neutral and unpleasant affective contexts induced by viewing of respective picture series. Based on previous results demonstrating reduced later RREP components during an unpleasant compared to a neutral affective picture viewing context in low anxious individuals (von Leupoldt et al., 2010b), we expected a similar pattern for low anxious subjects in the present study. In contrast, we hypothesized the opposite pattern for higher anxious individuals with greater amplitudes for later RREP components during an unpleasant compared to a neutral affective context. This pattern would converge with previous studies demonstrating increased perception of respiratory symptoms in anxious individuals to be particularly evident in unpleasant compared to neutral or pleasant affective contexts (Janssens et al., 2009, Bogaerts et al., 2005, Van den Bergh et al., 2004).

Section snippets

Participants

After providing informed written consent, fifty healthy, non-smoking volunteers without history of significant psychological or medical conditions participated in this study that was approved by the Institutional Review Board of the University of Florida (Table 1). Normal baseline lung function was confirmed by spirometry (SpiroPro, Cardinal Health, Hoechberg, Germany) according to international guidelines (Miller et al., 2005).

Anxiety ratings

The transient (state) level of anxiety was measured with the state

Participants

The median state anxiety score across the 50 participants was 34, which led to the exclusion of 4 participants with this score from further analyses. The remaining 46 individuals were assigned to a low anxious and higher anxious group (each N = 23). No differences in baseline characteristics were found between low and higher anxious individuals, except greater state anxiety in the higher anxious group (Table 1).

Evaluative ratings

Evaluative ratings confirmed successful modulation of affective context during RREP

Discussion

The present results show an effective manipulation of affective context without differences between groups. Both low and high anxious individuals rated the unpleasant picture context higher in arousal and lower in hedonic valence, compared to the neutral context, indicating successful affective engagement (Bradley et al., 1996, Bradley and Lang, 2007). The most important and novel finding is that higher anxious individuals showed increased later RREP components P2 and P3 when inspiratory

Conflict of interest statement

The funding sources had no impact on the study design, collection/analysis/interpretation of the data, and preparation of/decision to submit the present manuscript.

No author has a conflict of interest with the present manuscript.

Acknowledgment

This work was supported by the German Research Society (Deutsche Forschungsgemeinschaft, DFG) by a stipend to Andreas von Leupoldt (Heisenberg-Stipendium, LE 1843/9-1) and a grant from the National Institute of Mental Health (P50 MH 72850) to Peter J. Lang. The authors wish to thank Andreas Keil for his valuable support of the present study.

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