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This link between LFP oscillations and the breathing cycle can be tracked with high temporal resolution by measuring their coherence. 2017) to closely track the inhalation-exhalation cycle. 2014) and prefrontal cortices ( Biskamp et al. More direct electrophysiological measures in rodents show local field potential (LFP) oscillations in hippocampus ( Nguyen Chi et al. 2002), albeit with limited spatial and temporal resolution, have implicated premotor, motor, and supplementary motor cortices in the voluntary control of breathing. 2006), and neuroimaging studies ( Evans et al. 2009), transcranial magnetic stimulation (TMS Locher et al.
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1998 Kaada and Jasper 1952) suggests a more complex breathing circuitry above the brain stem level. 2000 Bruce and Ackerson 1986 Foerster 1936 Gandevia and Rothwell 1987), the fact that the rate of breathing can be influenced by stimulation of the hippocampus, amygdala, and insula ( Frysinger and Harper 1989, 1990 Harper et al. While motor cortex stimulation elicits diaphragmatic contraction at expected somatotopic loci (Başar et al. Our findings imply a fundamental role of breathing-related oscillations in driving neuronal activity and provide insight into the neuronal mechanisms of interoceptive attention.Ī wealth of historical literature has focused on automatic breathing driven by brain stem structures ( Butler 2007 Tenney and Ou 1977) with more recent interest in cortical involvement ( Feldman et al. Volitional pacing of the breath engages frontotemporal-insular cortices, whereas attention to automatic breathing modulates the cingulate cortex. Using intracranial recordings in humans, we show neuronal activity to track the breathing cycle throughout widespread cortical/limbic sites. NEW & NOTEWORTHY Whereas the link between breathing and brain activity has a long history of application to therapy, its neurophysiology remains unexplored. Our findings suggest that breathing can act as an organizing hierarchical principle for neuronal oscillations throughout the brain and detail mechanisms of how cognitive factors impact otherwise automatic neuronal processes during interoceptive attention. During volitionally paced breathing, iEEG-breath coherence increases in a frontotemporal-insular network, and during attention to breathing, we demonstrate increased coherence in the anterior cingulate, premotor, insular, and hippocampal cortices.
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Specifically, volitional control and awareness of breathing engage distinct but overlapping brain circuits. We further demonstrate a sensitivity of this tracking to cognitive factors by using tasks adapted from cognitive behavioral therapy and meditative practice. We extend prior observations by showing the iEEG signal to track the breathing cycle across a widespread network of cortical and limbic structures. We show this to be the direct result of neuronal activity, as demonstrated by both the specificity of the finding to the cortical gray matter and the tracking of breath by the gamma-band (40–150 Hz) envelope in these structures. Using direct intracranial recordings in humans, we correlated cortical and limbic neuronal activity as measured by the intracranial electroencephalogram (iEEG) with the breathing cycle. Therapeutic techniques have used conscious control and awareness of breathing for millennia with little understanding of the mechanisms underlying their efficacy. Whereas the neurophysiology of respiration has traditionally focused on automatic brain stem processes, higher brain mechanisms underlying the cognitive aspects of breathing are gaining increasing interest.