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Original Research: Signs and Symptoms of Chest Disease |

Attentional Modulation of Reflex CoughAttentional Modulation of Reflex Cough FREE TO VIEW

Thomas Janssens, PhD; Mitchell Silva, PhD; Paul W. Davenport, PhD; Ilse Van Diest, PhD; Lieven J. Dupont, MD, PhD; Omer Van den Bergh, PhD
Author and Funding Information

From the Health Psychology Research Unit (Drs Janssens, Van Diest, and Van den Bergh), KU Leuven, and Department of Respiratory Medicine (Dr Dupont), University Hospitals Leuven, University of Leuven, Leuven, Belgium; miMedication (Dr Silva), Brussels, Belgium; and Department of Physiological Sciences (Dr Davenport), University of Florida, Gainesville, FL.

CORRESPONDENCE TO: Thomas Janssens, PhD, Health Psychology Research Unit, University of Leuven, Tiensestraat 102 - Bus 3726, 3000 Leuven, Belgium; e-mail: thomas.janssens@psy.kuleuven.be


FUNDING/SUPPORT: Dr Janssens is a postdoctoral fellow of the Research Foundation, Flanders.

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.


Chest. 2014;146(1):135-141. doi:10.1378/chest.13-2536
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OBJECTIVE:  Reflex cough is a defensive response generated in the brainstem in response to chemical and mechanical stimulation of the airways. However, converging evidence shows that reflex cough is also influenced by central neural control processes. In this study, we investigate whether reflex cough can be modulated by attentional focus on either external stimuli or internal cough-related stimuli.

METHODS:  Healthy volunteers (N = 24; seven men; age range, 18-25 years) completed four blocks of citric acid-induced cough challenges while, simultaneously, auditory stimuli were presented. Within each block, four concentrations were administered (30, 100, 300 and 1,000 mM, randomized). During two subsequent blocks, participants focused their attention externally (counting tones). During the other two blocks, participants focused their attention internally (counting coughs). The order of attentional focus was counterbalanced across participants. Ratings of the urge to cough were collected after each challenge. Cough frequency was determined by audio recording.

RESULTS:  Cough frequency was higher when participants focused their attention internally vs externally (P < .05). Also urge to cough was greater during internal vs external focus (P < .05), but the effect was smaller in later blocks of trials.

CONCLUSIONS:  Reflex cough can be modulated by attentional focus. Internally focused attention may be a mechanism involved in excessive (idiopathic) cough, while an external focus may be introduced as part of treatments targeting excessive cough.

Figures in this Article

Cough is the most common symptom for which individuals consult their general practitioner.1 It is a key symptom of a variety of medical conditions: Acute cough is often the consequence of an upper respiratory tract infection,1 whereas chronic cough may be indicative of postnasal drip syndrome, asthma, or gastroesophageal reflux disease.2 However, in 20% to 42% of patients presenting with chronic cough, cough can persist even after extensive investigation or treatment trials.3 These patients with refractory cough invariably have an enhanced cough reflex, and it has been suggested to label this condition as cough hypersensitivity syndrome.3,4

Cough is, typically, conceived as reflexive behavior wherein afferent activity from mechanical or chemical stimulation of the airways results in changes in the respiratory motor neural pattern generated by the brainstem.5 Evidence from decerebrated and anesthetized animals shows that cough reflexes can occur without the involvement of cortical processes.6,7 However, recent models of cough also emphasize the role of higher brain center neural control processes. Evidence is amassing that higher-order brain mechanisms are involved in the sensory processing of cough stimuli. The afferents that elicit cough relay information from peripheral stimulation to centers of the brain that are involved in the perception of stimulus intensity8 and produce a respiratory sensation, an urge to cough, which, typically, precedes cough motor activity.9 Furthermore, urge-to-cough activation is not limited to brain centers involved in stimulus intensity, but consists of additional brain centers, organized in a “cough network,” suggesting higher brain (cortical) control of urge to cough.5,8 In a similar fashion, descending pathways allow for behavioral modulation of cough behavior by cortical processes.5,8,10,11

One of the behavioral candidates for this higher brain control of cough behavior is attentional focus. Because information processing is resource limited, attentional focus serves as a mechanism determining the processing priority allocated to any given stimulus. Both bottom-up and top-down mechanisms influence attentional focus. For example, stimulus attributes such as intensity, novelty, salience, and suddenness of stimuli (bottom-up) may alter the processing priorities, but also concurrent emotions, expectancy, deliberate strategic orienting, and meaning attributed to stimuli (top-down) may reorganize priorities.12,13 It has been shown that attentional focus on respiratory sensations modulates the perception and magnitude of respiratory-related evoked potentials.14 These findings suggest that any variable altering the processing priority of cough-related stimuli of equal intensity may actually increase or decrease the urge to cough and cough behavior.

To our knowledge, only a few studies have investigated the effects of attentional focus on cough. A series of observational studies in naturalistic settings15 showed that cough frequency was lower when the external environment (eg, a portion of a film clip, a lecture) was rated as more interesting. Another study16 showed that participants with asthma coughed more frequently and rated the urge to cough higher when a citric acid inhalation test was framed as an asthma test vs a taste test. The findings were interpreted as the effects of beliefs on selective attention to respiratory vs taste sensations. However, neither of these studies experimentally manipulated attentional focus. In the current study, we manipulated attentional focus inward (focus on cough sensations) or outward (focus on auditory stimuli) and hypothesized that cough frequency and urge to cough would be greater during internal vs external attentional focus.

Participants

Undergraduate students (N = 28, eight men) were invited to participate in an investigation of cough reflex sensitivity in response to different, harmless, airborne substances. Participants were reached through e-mail and flyers. Based on self-report, individuals diagnosed with a medical condition associated with cough (eg, asthma, allergy, rhinitis) were excluded, as were participants reporting a respiratory infection in the 3 weeks preceding the experiment. The experiment was approved by the medical ethical committee of University Hospitals Leuven (S52118). All participants gave written informed consent. Four participants were excluded because of a self-reported cold, bringing the total number of participants to 24 (seven men; age range, 18-25 years). At the end of the experiment, participants were debriefed, thanked, and given a compensation of €7.

Self-Report Measures

Perceived urge to cough was measured by a 0 to 10 Borg-type scale labeled from “not at all” to “extremely strong.”9 The degree of attentional focus on the tone or cough-counting task was also measured immediately after the single breath inhalation of citric acid with a 0 to 10 Likert-type scale labeled from “not at all” to “extremely focused.”

Apparatus

Cough provocation was carried out using a single-breath, dosimeter-controlled inhalation (Jaeger Aerosol Provocation System dosimeter; Carefusion Corp) of citric acid (2 s). Citric acid was dissolved in a physiologic saline solution by the hospital pharmacy. Different concentrations of citric acid were used: 30 mM or 5.8 mg/mL, 100 mM or 19.2 mg/mL, 300 mM or 58 mg/mL, and 1,000 mM or 192 mg/mL. Participants wore a nose clip when breathing through the dosimeter.

Cough sounds were recorded with a microphone that was pinned to the participant’s clothes. This microphone was connected to a computer equipped with Adobe Audition (Adobe System Corp), sampling the sound at 44.1 kHz.

Stimulus Materials

Eighteen audio clips containing high- (750 Hz) and low-pitched (250 Hz) tones were created with Audacity.17 Each audio clip lasted 25 s and included 12 1-s tones (one to seven high-pitched tones). After every second tone, there was a silence of 1.25 s. The clips were presented through headphones. The same two clips were always used during the training trials; the remaining 16 clips were presented in randomized order during the inhalation trials of the experiment.

Procedure

Participants sat in a comfortable chair. After informed consent (which stated that the inhalations could elicit cough or an urge to cough, but that these effects were short lived and harmless), exclusion criteria were checked by a survey. Next, participants received information about the audio task and instructions on how to take a single deep breath through the dosimeter. Participants performed two training trials with saline inhalation and an audio clip. After each training trial, they rated their urge to cough and attentional focus. If necessary, they received additional instructions.

Next, participants received four blocks of citric acid cough challenges. In each block, participants were confronted with four cough trials, each of them consisting of different concentrations of citric acid (30, 100, 300, and 1,000 mM, presented in random order), which resulted in a total of 16 cough trials across the experiment. Each citric acid inhalation was followed by a 90-s break, during which participants could take a sip of water, blow their nose, or do both. During each trial, an audio clip was presented. Attentional focus was manipulated by instructions that were given prior to each block: In the exteroceptive condition, participants were asked to count the high-pitched tones, whereas in the interoceptive condition, they were asked to count their coughs and to disregard the tones. Order of allocation of blocks to a specific attentional focus condition was counterbalanced, with one-half of the participants first receiving two blocks with an interoceptive attentional focus followed by two blocks with an exteroceptive focus, whereas this order was reversed for the other one-half of participants. After each trial, participants rated the urge to cough and attentional focus. In the exteroceptive condition, they furthermore reported the number of high-pitched tones they had counted, whereas in the interoceptive condition, they reported the number of coughs they had counted.

Data Reduction and Analysis

Coughs were counted from the recorded sounds that occurred within 15 s of the citric acid challenge.18 Every cough that occurred during a series of sound bursts was identified as a single cough. Because of the low cough frequencies that were observed during the experiment (participants only coughed in 35.6% of trials), we summed cough frequencies over the four citric acid concentrations within the same trial block. This resulted in a 2 × 2 (attentional focus: internal vs external; block: first vs second trial block within the attentional focus condition) within-subject design for cough frequency and a 2 × 2 × 4 (attentional focus, block, and trial, respectively) within-subject design for the other variables of interest. We carried out repeated-measures analysis of variance with Greenhouse-Geisser corrections where appropriate. Post hoc comparisons were adjusted for multiple tests using Bonferroni correction. Partial η squared (η2p) was used as a measure of effect size. When variables were not normally distributed, nonparametric tests were used instead. All analyses were carried out in Statistica version 11 (Statsoft Inc).

Manipulation Check

Participants reported, overall, a similar degree of focus during the interoceptive and exteroceptive counting tasks [F(1,23) = 0.70; not statistically significant]. However, the degree of focus differed according to citric acid concentration [focus × trial interaction: F(3,69) = 7.69; P = .0002; η2p = 0.25]: The difference between the degree of focus in the interoceptive vs exteroceptive condition was larger during inhalation of 30 mM and 100 mM citric acid compared with inhalation of 300 mM and 1,000 mM citric acid [F(1,23) = 13.73; P = .001], and a plot exploring this effect showed that this was likely due to a reduction in the degree of focus for the exteroceptive condition and an increase in the degree of focus during the interoceptive condition with increasing citric acid levels (Fig 1). A similar number of counting errors was made during both tasks (Wilcoxon signed rank test, P = .075), and there was no correlation between self-reported degree of focus and counting errors (ρ = −0.08; P = .10).

Figure Jump LinkFigure 1  Mean levels (± SE) of self-reported attentional focus for cough challenge tests with different concentrations of citric acid during interoceptive and exteroceptive attention tasks.Grahic Jump Location
Cough and Urge to Cough

Participants coughed more when counting coughs compared with counting tones [F(1,23) = 13.31; P = .001; η2p = 0.37]. However, the elevated cough frequency during interoceptive attentional focus was limited to the first trial block [block × focus interaction effect: F(1,23) = 5.04; P = .035; η2p = 0.18] (Fig 2). The main effect of block (reductions in cough frequency from block 1 to block 2) did not reach significance [F(1,23) = 2.13; P = .158; η2p = 0.08] (Fig 2). An alternative analysis strategy that did not pool cough frequencies over citric acid concentrations but excluded 30 mM trials showed similar results (e-Appendix 1, e-Tables 1-3, e-Fig 1).

Figure Jump LinkFigure 2  Mean levels (± SE) of cough frequency for the first and second block of cough challenges during interoceptive and exteroceptive attention tasks.Grahic Jump Location

Also the self-rated urge to cough increased during interoceptive focus compared with exteroceptive focus during the first but not the second trial block [block × focus interaction effect: F(1,23) = 5.76; P = .025; η2p = 0.20] (Fig 3). Contrary to cough frequency, we did not find a main effect of attentional focus on urge to cough [F(1,23) = 0.94; P = .34], but overall, the urge to cough became more intense as the citric acid concentration increased [F(3,69) = 126.61; P < .0001; ε = 0.64; η2p = 0.85] (Fig 3). The effects of attentional focus did not differ significantly for the different citric acid concentrations [trial × focus interaction effect: F(3,69) = 0.873; P = .443; trial × block × focus interaction effect: F(3,69) = 1.953; P = .129]. Urge to cough did not show a reduction across trial blocks [F(1,23) = 0.06; P = .815]. Cough frequency and urge-to-cough ratings correlated highly (ρ = 0.72; P < .0001).

Figure Jump LinkFigure 3  Mean levels (± SE) of self-reported urge to cough for the block 1 and block 2 cough challenges during interoceptive and exteroceptive attention tasks.Grahic Jump Location

In this study, we found that cough frequency was higher and perceived urge to cough was more intense when participants focused their attention on internal cough-related sensations compared with focusing on external stimuli. However, the effects were short lived and limited to the first trial block.

Our findings are in-line with the role of attention in the perception of pain and other physical symptoms such as dyspnea and fatigue.19,20 However, a major difference between cough and these other interoceptive symptoms is that the registration of cough presence, intensity, and frequency is not dependent on self-report but can be objectively recorded. The present effect on cough frequencies is, therefore, free from self-report biases, unlike many other findings on symptom perception.20

Importantly, using a well-controlled behavioral experiment, our findings add evidence to the finding that the characterization of cough solely as a reflexive motor behavior generated by the brainstem is incomplete. The present data suggest that attentional modulation is an important mechanism in the higher brain (cortical) control of urge to cough and that changes in attentional processing can change the descending neural drive for motor action in a way that is similar to volitional changes in cough reflex sensitivity.10 This is in-line with evidence for the effects of placebo medication on cough and the depression of cough in individuals under anesthesia or in individuals suffering from disorders of the CNS21 and may partially explain the wide intrapatient variability of cough frequency during the day in patients with chronic cough.22 The suprapontine brain areas involved in neural control of capsaicin-induced urge to cough and placebo-induced suppression of urge to cough have been described.8,23,24 One of the brain regions that is involved in the processing of cough stimulus intensity23 and placebo-induced reduction of urge to cough24 is the anterior insula. Interestingly, the anterior insula has also been reported to be a critical structure of a salience network involved in high-level cognitive control and attentional processes, with the anterior insula and anterior cingulate cortex acting as an integrator of stimulus-driven attention switching and cortically driven control and sensory bias.13,25 The changes in insula activity that have been found in response to citric acid inhalation and placebo-induced suppression of urge to cough would fit with the role of the insula as a saliency detector. Taken together, these findings provide us with a credible locus for the impact of attentional manipulation on perceived urge to cough and cough responses, which could be tested in future studies.

We replicated the strong correlation between cough and urge to cough reported earlier,9 and consistent with this, we found similar effects of attentional focus on both motor cough and perceived urge to cough. The urge to cough may be conceived as the result of an integrated signal of peripheral and cortical processing entering awareness to help protect the integrity of the body by behavioral actions, such as increasing cough frequency, the strength of the cough reflex, or both.5,26,27 This urge to cough may enter awareness in a more compelling way (ie, demand more attention) as the intensity of the cough trigger increases. This is shown in our study by the fact that the self-reported degree of attentional focus changed with increasing concentrations of citric acid: During higher concentrations, participants found it harder to focus their attention on the tones and easier to focus attention on the coughs. In that respect, the urge to cough acts like a pain stimulus: With increasing intensity, it is more likely to interrupt ongoing activities, to reset processing priorities, and to direct the attentional focus on the pain, which may cause a nonpainful stimulus to become painful.28,29

Considering cough as a defensive reflex, it is interesting to note that modulating effects of attention have also been found in the study of the eye-blink startle, a defensive blinking reflex of the eyelid in response to a startling noise.30 Furthermore, results on fear conditioning have shown that eye-blink startle is also modulated by acquired unpleasantness of a conditioned stimulus,31 showing that apart from attention, the startle reflex is also modulated by the emotional meaning of a stimulus. In cough, a similar effect of meaning on cough responses has been documented16: Cough frequency induced by citric acid inhalation increased in an asthma-related context compared with a context in which participants had to focus on the taste of the citric acid.

Our findings have several clinical implications. First, our findings show that a sustained attention on cough sensations or cough-related stimuli may cause individuals to react with an increased urge to cough or increased motor cough activity to stimuli that would not otherwise elicit these responses. It is likely that patients who are concerned about their cough and become hypervigilant toward cough-related sensations in an attempt to avoid and/or control cough are actually prone to become trapped in a cycle characterized by increased attention and increased cough responses that may contribute to pathogenesis of chronic cough hypersensitivity. Second, the impact of attentional focus on cough frequency and urge to cough may also create treatment opportunities. Helping patients to focus attention on external stimuli instead of on cough may contribute to a decrease in cough frequency and urge to cough. There are several potential ways to shift attention away from internal sensations. For example, the administration of placebo medication may cause participants to have the belief that their cough will get better, which may reduce its threat value and shift attention away from respiratory sensations.5 Furthermore, an increase in external information, such as participation in a difficult, varied, or interesting task may also reduce cough.15,19,20

However, studies on the role of attention in pain suggest weak effects for usefulness of attentional strategies as a treatment tool.3234 In such threatening conditions, it may be difficult to disengage attention from internal respiratory sensations and a reduction of the threat value of cough may be needed to reduce attention to internal cough-related sensations.

There are some limitations to our study. First, on average, we used rather low concentrations of citric acid, which resulted in an overall low incidence of coughs. Our decision to sum cough occurrences across trials precluded us from investigating the interaction of stimulus intensity and attentional focus on cough frequencies. Therefore, future studies may consider manipulations that lead to higher or more sustained cough frequencies, such as increased or individualized levels of citric acid or the use of cough triggers with higher threat value. A second limitation is that our manipulation of attentional focus may not be easy to maintain for all participants. Participant ratings of attentional focus suggested that focusing on external stimuli may be more difficult when confronted with more intense stimulation of the airways, and individual differences in the ability to maintain an external focus could potentially have influenced our findings. Increasing the task demands of the attention task could be a way to mitigate this problem. In that case, care has to be taken to select a task that does not increase stress or negative emotions, which have been shown to increase perception of physical symptoms32 and may, therefore, make it more difficult to detect attention effects of cough and urge to cough. Furthermore, when using a more demanding attention task, the design of an interoceptive attention task that is comparable in task demand may prove to be difficult. Finally, our sample was specific in that the majority of subjects were female and only included young healthy participants. A replication of our findings in other clinical samples may shed a light on the involvement of attention- and threat-related effects in explaining sex-related differences in cough thresholds or differences in cough thresholds between different clinical groups.35 Finally, the inclusion of individual difference variables, related to specific concerns and illness beliefs about cough and/or to broader trait variables such negative affectivity, may be needed to further explain the effects of attention on cough frequency and urge to cough.

In conclusion, we showed that in healthy volunteers, cough reflexes were increased during internal attentional focus compared with external attentional focus. These findings show that reflexive cough can be modulated by higher-order brain functions and may be a potential target to reduce the burden of cough.

Author contributions: T. J. and O. V. d. B. had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. T. J. served as principal author. T. J. and O. V. d. B. contributed to the data analysis; I. V. D., L. J. D., and O. V. d. B. contributed to the study concept and design; M. S. and P. W. D. contributed to the study methodology; T. J. and O. V. d. B. contributed to the drafting of the manuscript; and T. J., M. S., P. W. D., I. V. D., L. J. D., and O. V. d. B. contributed to the revision of the manuscript.

Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Role of sponsors: The funder had no role in the design of the study, the collection and analysis of the data, or the preparation of the manuscript.

Other contributions: The authors would like to thank Jolien Dhooge, MS, and Tine Vrancken, MS for their help with data collection.

Additional information: The e-Appendix, e-Tables, and e-Figure can be found in the Supplemental Materials section of the online article.

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Figures

Figure Jump LinkFigure 1  Mean levels (± SE) of self-reported attentional focus for cough challenge tests with different concentrations of citric acid during interoceptive and exteroceptive attention tasks.Grahic Jump Location
Figure Jump LinkFigure 2  Mean levels (± SE) of cough frequency for the first and second block of cough challenges during interoceptive and exteroceptive attention tasks.Grahic Jump Location
Figure Jump LinkFigure 3  Mean levels (± SE) of self-reported urge to cough for the block 1 and block 2 cough challenges during interoceptive and exteroceptive attention tasks.Grahic Jump Location

Tables

References

Fathi H, Morice AH. Cough. Medicine (Baltimore). 2008;36(3):129-131. [CrossRef]
 
Palombini BC, Villanova CAC, Araújo E, et al. A pathogenic triad in chronic cough: asthma, postnasal drip syndrome, and gastroesophageal reflux disease. Chest. 1999;116(2):279-284. [CrossRef] [PubMed]
 
Chung KF. Chronic ‘cough hypersensitivity syndrome’: a more precise label for chronic cough. Pulm Pharmacol Ther. 2011;24(3):267-271. [CrossRef] [PubMed]
 
Morice AH. Chronic cough hypersensitivity syndrome. Cough. 2013;9(1):14. [CrossRef] [PubMed]
 
Van den Bergh O, Van Diest I, Dupont LJ, Davenport PW. On the psychology of cough. Lung. 2012;190(1):55-61. [CrossRef] [PubMed]
 
Ohi Y, Yamazaki H, Takeda R, Haji A. Phrenic and iliohypogastric nerve discharges during tussigenic stimulation in paralyzed and decerebrate guinea pigs and rats. Brain Res. 2004;1021(1):119-127. [CrossRef] [PubMed]
 
Canning BJ, Mazzone SB, Meeker SN, Mori N, Reynolds SM, Undem BJ. Identification of the tracheal and laryngeal afferent neurones mediating cough in anaesthetized guinea-pigs. J Physiol. 2004;557(pt 2):543-558. [CrossRef] [PubMed]
 
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