Olfactory sensitivity to changes in environmental [Ca(2+)] in the freshwater teleost Carassius auratus: an olfactory role for the Ca(2+)-sensing receptor?

Abstract

Olfactory sensitivity to changes in environmental Ca(2+) has been demonstrated in two teleost species; a salmonid (Oncorhynchus nerka) and a marine/estuarine perciform (Sparus aurata). To assess whether this phenomenon is restricted to species that normally experience large fluctuations in external ion concentrations (e.g. moving from sea water to fresh water) or is present in a much wider range of species, we investigated olfactory Ca(2+) sensitivity in the goldfish (Carassius auratus), which is a stenohaline, non-migratory freshwater cyprinid. Extracellular recording from the olfactory bulb in vivo by electroencephalogram (EEG) demonstrated that the olfactory system is acutely sensitive to changes in external Ca(2+) within the range that this species is likely to encounter in the wild (0.05-3 mmol l(-1)). The olfactory system responded to increases in external calcium with increasing bulbar activity in a manner that fitted a conventional Hill plot with an apparent EC(50) of 0.9+/-0.3 mmol l(-1) (close to both ambient and plasma free [Ca(2+)]) and an apparent Hill coefficient of 1.1+/-0.3 (means +/- S.E.M., N=6). Thresholds of detection were below 50 micro mol l(-1). Some olfactory sensitivity to changes in external [Na(+)] was also recorded, but with a much higher threshold of detection (3.7 mmol l(-1)). The olfactory system of goldfish was much less sensitive to changes in [Mg(2+)] and [K(+)]. Preliminary data suggest that Ca(2+) and Mg(2+) are detected by the same mechanism, although with a much higher affinity for Ca(2+). Olfactory sensitivity to Na(+) may warn freshwater fish that they are reaching the limit of their osmotic tolerance when in an estuarine environment. Olfaction of serine, a potent odorant in fish, was not dependent on the presence of external Ca(2+) or Na(+). Finally, the teleost Ca(2+)-sensing receptor (Ca-SR) was shown to be highly expressed in a subpopulation of olfactory receptor neurones by both immunocytochemistry and in situ hybridisation. The olfactory sensitivity to Ca(2+) (and Mg(2+)) is therefore likely to be mediated by the Ca-SR. We suggest that olfactory Ca(2+) sensitivity is a widespread phenomenon in teleosts and may have an input into the physiological mechanisms regulating internal calcium homeostasis.