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: 6.13). 06/2009; 47(3):961-71. DOI: 10.1016/j.neuroimage.2009.05.025
Source: PubMed

ABSTRACT 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.

  • Source
    [Show abstract] [Hide abstract]
    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. The autonomic nervous system has been studied as a correlate of emotion for almost a century (Cannon, 1916). A central technique within this tradition of research is heart rate variability (HRV), which refers to a variety of methods for assessing the beat-to-beat change in the heart over time; these are used to approximate var-ious aspects of autonomic outflow to the heart. Improvements in computing technology and miniaturization have made the electro-cardiographic collection of inter-beat intervals (IBIs) accessible, and the analysis of the resulting beat-to-beat intervals trivial. One consequence of this access is a sustained interest in the application of HRV within the behavioral sciences, and in the psychology of emotion in particular. There are major biobehavioral theories that suggest that HRV can be used to investigate the central relation-ship between autonomic regulation and interpersonal interaction (Porges, 1995; Thayer and Lane, 2000). The neurovisceral inte-gration model suggests that HRV is an index of the capacity for the central autonomic network (Benarroch, 1993) – which includes the brainstem, hypothalamus, and prefrontal cortex – to adjust to environmental demands (Thayer and Lane, 2000). Porges' polyvagal theory takes a phylogenetic approach (i.e., it observes evolutionary and developmental commonalities within the structure and function of the vertebrate autonomic nervous system), arguing that social engagement is centrally facilitated by outflow and functional organization of vagus nerve (Porges, 1995). Consistent with this theory, reduced HRV has been observed in psychiatric disorders characterized by poor social cognition and emotion regulation (Bär et al., 2007; Quintana et al., 2013b). Interestingly, psychiatric patients also demonstrate less HRV reac-tivity during different levels of mental loading in comparison to healthy controls (Valkonen-Korhonen et al., 2003), further highlighting the poor cardiorespiratory regulatory capacity of this population. While it may be the case that HRV can be used as a neuro-biological index of interpersonal interaction, significant caveats exist due to the complicated nature of HRV and consequently uncertainty regarding what information is actually provided by common HRV indices (Berntson et al., 1997; Malpas, 2002; Bill-man, 2011). Additionally, the relationship between HRV and vagal modulation is complex in itself with a large interindividual vari-ation (Picard et al., 2009). The problem is further compounded by the co-modulation of various respiratory and circulatory fac-tors, which occur via numerous mechanisms and over multiple time-scales. Moreover, both breathing and blood pressure regu-lation have their own directly mediated relationships to the tasks employed in social, emotional, and cognitive experiments – if this is the case, we often have a complicated question of inter-locking causalities. For instance, are observed changes in heart period epiphenomena that can be more parsimoniously described by changes in breathing or blood pressure? If the direction of causality between experimental task and the coordinated response within cardiac, circulatory, and respiratory variables is poorly understood, simple relationships between task and output changes may be obscured. Finally, experiments are often poorly designed as uncontrolled variables within typical experimental environments may drastically influence HRV. Few papers ideally control for med-ication, food, and water consumption, bladder filling, time of day, and other extraneous factors (Tak et al., 2009; Heathers, 2014). The overall aim of this review is to highlight the interrelation-ships between the nature and extraneous control of HRV, with a particular emphasis on respiration, and discuss implications for research in emotion science and psychology. Firstly, a number of
    Frontiers in Psychology 07/2014; 5(805). · 2.80 Impact Factor
  • [Show abstract] [Hide abstract]
    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.
    Progress in brain research 01/2014; 209:367-77. · 4.19 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: 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.
    PLoS ONE 08/2014; 9(8):e104729. · 3.53 Impact Factor

Full-text (2 Sources)

Available from
May 28, 2014