Breathing as a Fundamental Rhythm of Brain Function

Abstract

Ongoing fluctuations of neuronal activity have long been considered intrinsic noise that introduces unavoidable and unwanted variability into neuronal processing, which the brain eliminates by averaging across population activity (Georgopoulos et al., 1986; Lee et al., 1988; Shadlen and Newsome, 1994; Maynard et al., 1999). It is now understood, that the seemingly random fluctuations of cortical activity form highly structured patterns, including oscillations at various frequencies, that modulate evoked neuronal responses (Arieli et al., 1996; Poulet and Petersen, 2008; He, 2013) and affect sensory perception (Linkenkaer-Hansen et al., 2004; Boly et al., 2007; Sadaghiani et al., 2009; Vinnik et al., 2012; Palva et al., 2013). Ongoing cortical activity is driven by proprioceptive and interoceptive inputs. In addition, it is partially intrinsically generated in which case it may be related to mental processes (Fox and Raichle, 2007; Deco et al., 2011). Here we argue that respiration, via multiple sensory pathways, contributes a rhythmic component to the ongoing cortical activity. We suggest that this rhythmic activity modulates the temporal organization of cortical neurodynamics, thereby linking higher cortical functions to the process of breathing.

Amygdala‐stimulation‐induced apnea is attention and nasal‐breathing dependent

“…In humans, the continuous, involuntary rhythm of breathing is generated within the brainstem 49 , however, very little is known about the conscious control of breathing 24 . This study demonstrates a role for the amygdala in voluntary respiratory control and allows for further study of this pathway in dysfunctional breathing states - not only in those with epilepsy but also infants with developmental abnormalities and in neurodegenerative disorders.…”

Respiration modulates oscillatory neural network activity at rest

“…Notably, the authors suggest crossfrequency coupling to involve neural interactions between premotor areas and both insular and cingulate cortex as well as the medulla, which is precisely the pathway we propose to connect deep and cortical nodes within the RMBO network. A simple graph model of excitatory and inhibitory cells has been shown as proof of principle for cortical gamma modulation through respiration (modelled as sinusoidal input) 45 . The authors later concluded that respiration-locked brain activity has two driving sources 46 : On the one hand, respiration entrains OB activity via mechanoreceptors (i.e., phase-phase coupling), as seen in LFP 23 .…”

Dissociation of fear initiation and maintenance by breathing-driven prefrontal oscillations

“…Although most research has focused on the cardiovascular system, the respiratory rhythm is a strong candidate to bridge the gap between brain and body during emotion. Breathing is strongly modulated during fear and other emotions (14,15) and numerous studies have shown that the respiratory rhythm can influence neuronal dynamics, mainly via feedback from the olfactory system (16), in many brain areas such as the hippocampus, amygdala and prefrontal cortex in both rodents (17)(18)(19)(20) and humans (21). We hypothesized that breathing is therefore a marker of emotional state poised to directly impact neuronal functioning in the cortical and limbic system to regulate fear expression (FigS1).…”