Modulation of spontaneous breathing via limbic/paralimbic–bulbar circuitry: An event-related fMRI study

Department of Psychiatry, Division of Neurotherapeutics, Massachusetts General Hospital-East, 13th Street, Building 149, Suite 2625, Charlestown, MA 02129, USA.
NeuroImage (Impact Factor: 6.36). 06/2009; 47(3):961-71. DOI: 10.1016/j.neuroimage.2009.05.025
Source: PubMed


It is well established that pacemaker neurons in the brainstem provide automatic control of breathing for metabolic homeostasis and survival. During waking spontaneous breathing, cognitive and emotional demands can modulate the intrinsic brainstem respiratory rhythm. However the neural circuitry mediating this modulation is unknown. Studies of supra-pontine influences on the control of breathing have implicated limbic/paralimbic-bulbar circuitry, but these studies have been limited to either invasive surgical electrophysiological methods or neuroimaging during substantial respiratory provocation. Here we probed the limbic/paralimbic-bulbar circuitry for respiratory-related neural activity during unlabored spontaneous breathing at rest as well as during a challenging cognitive task (sustained random number generation). Functional magnetic resonance imaging (fMRI) with simultaneous physiological monitoring (heart rate, respiratory rate, tidal volume, end-tidal CO(2)) was acquired in 14 healthy subjects during each condition. The cognitive task produced expected increases in breathing rate, while end-tidal CO(2) and heart rate did not significantly differ between conditions. The respiratory cycle served as the input function for breath-by-breath, event-related, voxel-wise, random-effects image analyses in SPM5. Main effects analyses (cognitive task+rest) demonstrated the first evidence of coordinated neural activity associated with spontaneous breathing within the medulla, pons, midbrain, amygdala, anterior cingulate and anterior insular cortices. Between-condition paired t-tests (cognitive task>rest) demonstrated modulation within this network localized to the dorsal anterior cingulate and pontine raphe magnus nucleus. We propose that the identified limbic/paralimbic-bulbar circuitry plays a significant role in cognitive and emotional modulation of spontaneous breathing.

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Available from: Darin D Dougherty
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    • "Distinctly different from autonomic breathing, voluntary breathing requires extensive cortical and subcortical activation and suppression of brainstem respiratory center for autonomic breathing [33], [34]. According to brain imaging studies, these respiratory-related areas include the primary motor cortex, the premotor cortex, the supplementary motor area, the primary and secondary somatosensory cortices, the insula, the ACC and amygdala, and the dorsolateral prefrontal cortex [35]–[46]. "
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    ABSTRACT: Objective Painful peripheral electrical stimulation to acupuncture points was found to cause sensitization if delivered randomly (EStim), but induced habituation if triggered by voluntary breathing (BreEStim). The objective was to systematically compare the effectiveness of BreEStim and EStim and to investigate the possible mechanisms mediating the habituation effect of BreEStim. Methods Eleven pain-free, healthy subjects (6 males, 5 females) participated in the study. Each subject received the BreEStim and EStim treatments in a random order at least three days apart. Both treatments consisted of 120 painful but tolerable stimuli to the ulnar nerve at the elbow on the dominant arm. BreEStim was triggered by voluntary breathing while EStim was delivered randomly. Electrical sensation threshold (EST) and electrical pain threshold (EPT) were measured from the thenar and hypothenar eminences on both hands at pre-intervention and 10-minutes post-intervention. Results There was no difference in the pre-intervention baseline measurement of EST and EPT between BreEStim and EStim. BreEStim increased EPT in all tested sites on both hands, while EStim increased EPT in the dominant hypothenar eminence distal to the stimulating site and had no effect on EPT in other sites. There was no difference in the intensity of electrical stimulation between EStim and BreEStim. Conclusion Our findings support the important role human voluntary breathing plays in the systemic habituation effect of BreEStim to peripheral painful electrical stimulation.
    Full-text · Article · Aug 2014 · PLoS ONE
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    • "However, there is no relationship between cardiorespiratory coupling and baroreflex sensitivity or blood pressure variability (Tzeng et al., 2003). Further, shared neural networks for respiratory and HR oscillations (Evans et al., 2009) suggest that the manipulation on breathing may also lead to unintended effects on HRV by removing some of the variance in HRV that may relevantly covary with experimental task. Intriguingly, the degree of coupling may be higher when HRV is increased and at lower breathing frequencies (Galletly and Larsen, 2001; Tzeng et al., 2003), suggesting that unhealthy populations or experiments that are designed to reduce HRV may be more prone to decoupling of cardiorespiratory oscillations . "
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    ABSTRACT: Heart rate variability (HRV) refers to various methods of assessing the beat-to-beat variation in the heart over time, in order to draw inference on the outflow of the autonomic nervous system. Easy access to measuring HRV has led to a plethora of studies within emotion science and psychology assessing autonomic regulation, but significant caveats exist due to the complicated nature of HRV. Firstly, both breathing and blood pressure regulation have their own relationship to social, emotional, and cognitive experiments – if this is the case are we observing heart rate (HR) changes as a consequence of breathing changes? Secondly, experiments often have poor internal and external controls. In this review we highlight the interrelationships between HR and respiration, as well as presenting recommendations for researchers to use when collecting data for HRV assessment. Namely, we highlight the superior utility of within-subjects designs along with the importance of establishing an appropriate baseline and monitoring respiration.
    Full-text · Article · Jul 2014 · Frontiers in Psychology
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    • "In addition, amygdala activity was synchronized with each breath. Thus, it appears that several limbic and paralimbic areas, in addition to the amygdala, are involved in breathing changes associated with cognition and emotional processing (Evans et al., 2009; Masaoka et al., 2005 Masaoka et al., , 2012). "
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    ABSTRACT: As a result of recent progress in brain imaging techniques, a number of studies have been able to identify anatomical correlates of various emotions (Pujol et al., 2013; Tettamanti et al., 2012; van der Zwaag et al., 2012). However, emotions are not solely a phenomenon within the brain-they are also composed of body responses. These include autonomic and behavioral responses, such as changes in heart rate, blood pressure, skin conductance, and respiration. Among these physiological responses, respiration has a unique relationship to emotion. While the primary role of respiration concerns metabolism and homeostasis, emotions such as disgust, anger, and happiness also influence respiratory activities (Boiten et al., 1994). While respiratory change that accompanies emotions can occur unconsciously, respiration can also be voluntarily altered associating with an activation of the motor cortex. There may be no physiological expression for the association between the three areas of the brain that regulate respiration: the brainstem, the limbic system, and the cerebral cortex. The brainstem works to maintain homeostasis, the limbic system is responsible for emotional processing, and the cerebral cortex controls intention. Investigating the interaction between these brain regions may lead to an explanation about why they are so widely dispersed in the brain, despite their common role in the regulation of respiration. In this chapter, we review our findings on breathing behavior and discuss the mechanisms underlying the relationship between emotion and respiration.
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