Breathing above the brainstem: Volitional control and attentional modulation in humans.

While the neurophysiology of respiration has traditionally focused on automatic brainstem processes, higher brain mechanisms underlying the cognitive aspects of breathing are gaining increasing interest. Therapeutic techniques have used conscious control and awareness of breathing for millennia with little understanding of the mechanisms underlying their efficacy. Using direct intracranial recordings in humans, we correlated cortical and limbic neuronal activity as measured by the intracranial electroencephalogram (iEEG) with the breathing cycle. We show this to be the direct result of neuronal activity, as demonstrated both by the specificity of the finding to the cortical grey matter and the tracking of breath by the gamma band (40-150 Hz) envelope in these structures. We extend prior observations by showing the iEEG signal to track the breathing cycle across a widespread network of cortical and limbic structures. We further demonstrate a sensitivity of this tracking to cognitive factors using tasks adapted from cognitive behavioral therapy and meditative practice. Specifically, volitional control and awareness of breathing engage distinct but overlapping brain circuits. During volitionally-paced breathing, iEEG-breath coherence increases in a fronto-temporal-insular network, and during attention to breathing, we demonstrate increased coherence in the anterior cingulate, premotor, insular and hippocampal cortices. 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.

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