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Forebrain Response to Breathing in Humans during Awake and Unconscious States

Although the brainstem has long been studied as the site responsible for automatic breathing, little is known about how the forebrain responds to breathing in humans during awake and unconscious states. Here, we tested the hypotheses (1) that forebrain sites will exhibit responses to phases of breathing and (2) these responses will differ based on type of breathing (nasal, oral, or via an endotracheal tube), level of consciousness, and whether the subject is breathing automatically or being mechanically ventilated. We studied five neurosurgical patients undergoing intracranial electroencephalography (IEEG). We recorded respiration using a oral/nasal thermistor, nasal pressure transducer, and chest/abdominal plethysmography belts. Under general anesthesia, additional respiratory measures were obtained using a standard clinical ventilator. Using spectral and bispectrum IEEG analysis, we found that oscillations entrained to the breath phase (inspiration/exhalation) during both nasal and mouth only breathing in numerous cortical and subcortical sites while awake. Interestingly, this entrainment appeared to increase under general anesthesia when the subjects were unconscious and breathing automatically, an effect which was altered when the subjects were mechanically ventilated. The sites that had the most significant entrainment localized to the sensorimotor cortex, ventral frontal lobe, and limbic system. These findings suggest that forebrain oscillations respond to all types of breathing and forebrain entrainment to the respiratory cycle may increase during unconsciousness. This interesting finding may prove critical for a predictive coding model for breathing, which might serve as a defense mechanism to ensure adequate ventilation.