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Hyperbaric oxygen and chemical oxidants stimulate CO₂/H⁺-sensitive neurons in rat brain stem slices

¹Department of Physiology and Biophysics, Environmental and Hyperbaric Cell Biology Facility, and ²Department of Community Health, Wright State University School of Medicine, Dayton, Ohio 45435

Submitted 20 September 2002 ; accepted in final form 4 April 2003

Hyperoxia, a model of oxidative stress, can disrupt brain stem function, presumably by an increase in O₂ free radicals. Breathing hyperbaric oxygen (HBO₂) initially causes hyperoxic hyperventilation, whereas extended exposure to HBO₂ disrupts cardiorespiratory control. Presently, it is unknown how hyperoxia affects brain stem neurons. We have tested the hypothesis that hyperoxia increases excitability of neurons of the solitary complex neurons, which is an important region for cardiorespiratory control and central CO₂/H⁺ chemoreception. Intracellular recordings were made in rat medullary slices during exposure to 2-3 atm of HBO₂, HBO₂ plus antioxidant (Trolox C), and chemical oxidants (N-chlorosuccinimide, chloramine-T). HBO₂ increased input resistance and stimulated firing rate in 38% of neurons; both effects of HBO₂ were blocked by antioxidant and mimicked by chemical oxidants. Hypercapnia stimulated 32 of 60 (53%) neurons. Remarkably, these CO₂/H⁺-chemosensitive neurons were preferentially sensitive to HBO₂; 90% of neurons sensitive to HBO₂ and/or chemical oxidants were also CO₂/H⁺ chemosensitive. Conversely, only 19% of HBO₂-insensitive neurons were CO₂/H⁺ chemosensitive. We conclude that hyperoxia decreases membrane conductance and stimulates firing of putative central CO₂/H⁺-chemoreceptor neurons by an O₂ free radical mechanism. These findings may explain why hyperoxia, paradoxically, stimulates ventilation.

central chemoreception; reactive oxygen species; cardiorespiratory control; intracellular recording; hyperoxia

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