Brain and gills as internal and external ammonia sensing organs for ventilatory control in rainbow trout, Oncorhynchus mykiss.

Ammonia is both a respiratory gas and a toxicant in teleost fish. Hyperventilation is a well-known response to elevations of both external and internal ammonia levels. Branchial neuroepithelial cells (NECs) are thought to serve as internal sensors of plasma ammonia (peripheral chemoreceptors), but little is known about other possible ammonia-sensors. Here, we investigated whether trout possess external sensors and/or internal central chemoreceptors for ammonia. For external sensors, we analyzed the time course of ventilatory changes at the start of exposure to high environmental ammonia (HEA, 1 mM). Hyperventilation developed gradually over 20 min, suggesting that it was a response to internal ammonia elevation. We also directly perfused ammonia solutions (0.01-1 mM) to the external surfaces of the first gill arches. Immediate hypoventilation occurred. For central chemoreceptors, we injected ammonia solutions (0.5-1.0 mM) directly onto the surface of the hindbrain of anesthetized trout. Immediate hyperventilation occurred. This is the first evidence of central chemoreception in teleost fish. We conclude that trout possess both external ammonia sensors, and dual internal ammonia sensors (perhaps for redundancy), but their roles differ. External sensors cause short term hypoventilation, which would help limit toxic waterborne ammonia uptake. When fish cannot avoid HEA, the diffusion of waterborne ammonia into the blood will stimulate both peripheral (NECs) and central (brain) chemoreceptors, resulting in hyperventilation. This hyperventilation will be beneficial in increasing ammonia excretion via the Rh metabolon system in the gills not only after HEA exposure, but also after endogenous ammonia loading from feeding or exercise.