| Persisting Learning Deficits in Rats after Exposure to Pfiesteria piscicida Edward D. Levin,
1,2
Donald E. Schmechel,
3,4
JoAnn M. Burkholder,
5
Howard B. Glasgow, Jr.,
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Nora J. Deamer-Melia,
5
Virginia C. Moser,
6
and G. Jean Harry
7
1
Department of Psychiatry;
2
Department of Pharmacology; and
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Department of Neurobiology and Medicine, Duke University Medical Center, Durham, NC 27710 USA;
4
VA Medical Center, Durham, NC 27705 USA
5
Department of Botany, North Carolina State University, Raleigh, NC 27695 USA
6
Neurotoxicology Division, U.S. Environmental Protection Agency, Research Triangle Park, NC 27709 USA
7
National Institute of Environmental Health Sciences, Research Triangle Park, NC 27709 USA Abstract
Pfiesteria piscicida and other toxic Pfiesteria-like dinoflagellates have been implicated as a cause of fish kills in North Carolina estuaries and elsewhere. Accidental laboratory exposure of humans to P. piscicida has been reported to cause a complex syndrome including cognitive impairment. The current project was conducted to experimentally assess the possibility of cognitive effects of P. piscicida exposure in rats. Samples of water from aquaria in which P. piscicida zoospores were killing fish were frozen, a procedure that has been found to induce encystment. Thawed samples were injected into albino Sprague-Dawley rats. A significant learning impairment was documented in rats administered samples of P. piscicida that were recently frozen. Prolonged storage of Pfiesteria samples diminished the effect. No effect was seen in the recall of a previously learned task, but when the rats were called upon to learn a new task, the Pfiesteria-treated animals showed a significant learning deficit. This effect persisted up to at least 10 weeks after a single injection of Pfiesteria. The Pfiesteria-induced learning deficit did not seem to be associated with any obvious debilitation or health impairment of the exposed rats. Deficits in habituation of arousal and rearing behavior were detected using a functional observational battery. No Pfiesteria-induced effects on blood count and white cell differential or in a standard pathological screening of brain, liver, lung, kidney, and spleen tissue were seen at 2 months after exposure. These studies document a persistent learning impairment in rats after exposure to the dinoflagellate P. piscicida in otherwise physically well-appearing rats. This effect may partially model the symptoms of cognitive impairments that humans have shown after Pfiesteria exposure. Key words : dinoflagellates, learning, memory, persisting, Pfiesteria, radial-arm maze, toxic. Environ Health Perspect 105:1320-1325 (1997) .
Address correspondence to Dr. E.D. Levin, Neuro-behavioral Research Laboratory, Department of Psychiatry, 341 Bell Building, Box #3412, Duke University Medical Center, Durham, 27710 USA. This research was supported by grants from the North Carolina Sea Grant College, the National Sea Grant Marine Biotechnology Program, and the National Science Foundation. Support was also provided by the Duke University Department of Psychiatry and Integrated Toxicology Program, the North Carolina State Department of Botany, the North Carolina Agricultural Research Service, the EPA, and the NIEHS. The authors thank C. Christopher, T. Weaver, P. Blackwelder, and P.M. Phillips for their help with testing the rats ; E. Hannon, J. Manning, and J. Springer for assistance with the Pfiesteria cultures ; and H. Tilson for his helpful comments on the manuscript. This manuscript has been reviewed by the National Health and Environmental Effects Research Laboratory, U.S. Environmental Protection Agency, and approved for publication. Approval does not signify that the contents necessarily reflect the views of the agency nor does mention of trade names or commercial products constitute endorsement or recommendation for use. Portions of this work have been presented at the 1996 meeting of the Southeastern Estuarine Research Society, Atlantic Beach, North Carolina, and the 1997 meeting of the Society of Toxicology, Cincinnati, Ohio. Received 15 May 1997 ; accepted 22 August 1997.
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