The blood-brain barrier is impervious to many toxicants and can protect the brain from accumulation of substances present in the blood stream. In fish,toxicants can enter the blood stream from the diet and across the gills from the external environment. But circumvention of the blood-brain barrier can occur if toxins are taken up via nerves that innervate water-exposed sensory organs. Nerve terminals in the lateral line, olfactory and gustatory systems, have all been highlighted as routes of uptake for waterborne metals.
Interference with sensory systems can have severe effects on fish behavior. Direct accumulation of metals in the olfactory, lateral line and gustatory systems can disrupt processes relying on sensory detection such as predator avoidance, social interaction, migration and feeding. Uptake of metals into the brain via sensory neurons could also interfere with the entire nervous system. It is therefore important that we understand this potential route of uptake from the external environment.
Previously, the transport of contaminants to the brain of fish viasensory pathways has only been considered for trace metals. Whether the extremely toxic organometals, such as tributyltin, a chemical applied to the underside of boats to prevent growth of marine life, can reach the brain via water-exposed sensory nerves is not known. Neither is much known about the effects of tributyltin on fish behavior. Claude Rouleau and colleagues set out to determine whether tributyltin could penetrate the rainbow trout's neural system.
The team looked at the body distribution of tributyltin in rainbow trout that had been exposed to waterborne tributyltin and following an intravenous injection of the compound. In this way, they could distinguish between any differences in uptake patterns of tributyltin due to exposure routes using whole-body autoradiography. The team reasoned that, after injection,tributyltin would accumulate in the brain if it crossed the blood-brain barrier, whereas waterborne tributyltin could either accumulate in the brain by crossing the gills and subsequently the blood-brain barrier or if it was taken up by the sensory nervous system.
The autoradiographs showed that tributyltin crossed the blood-brain barrier and was present in the brains of water-exposed fish and those given tributyltin in an intravenous injection. In the water-exposed trout, it was therefore difficult to separate the amount of tributyltin taken up via the gills and via the nervous system. However, this study is particularly interesting as the authors demonstrate hot spots of tributyltin accumulation in brain regions known to receive nerve fibers innervating water-exposed sensory organs, in particular the eminentia granulares, where nerve fibers from the mechanoreceptors in lateral lines terminate. Tributyltin was also seen in the olfactory system. This evidence strongly supports brain uptake of tributyltin via axonal transport from water-exposed sensory organs.
In this study, Rouleau and colleagues demonstrate that the uptake of contaminants via sensory systems is not limited to trace metals but is also seen in organometals. Investigating mechanisms of uptake and tissue distribution of waterborne contaminants is vital to our understanding of how toxicants manifest their effects. In particular, discovering how toxins interfere with sensory systems could help explain associated changes in fish behavior.