Behavioral alterations induced by repeated saxitoxin exposure in drinking water

Blooms of the saxitoxin-producing cyanobacterium Cylindrospermopsis raciborskii have been contaminating drinking water reservoirs in Brazil for many years. Although acute effects of saxitoxin intoxication are well known, chronic deleterious outcomes caused by repeated saxitoxin exposure still require further investigation. The aim of the present work is to investigate the effects of consumption of drinking water contaminated with C. raciborskii for 30 days on learning and memory processes in rats.

Methods

The effects of saxitoxin (3 or 9 μg/L STX equivalents) or cyanobacteria on behavior was determined using the open field habituation task, elevated plus maze anxiety model task, inhibitory avoidance task, and referential Morris water maze task.

Results

No effects of saxitoxin consumption was observed on anxiety and motor exploratory parameters in the elevated plus maze and open field habituation tasks, respectively. However, groups treated with 9 μg/L STX equivalents displayed a decreased memory performance in the inhibitory avoidance and Morris water maze tasks.

Conclusions

These results suggest an amnesic effect of saxitoxin on aversive and spatial memories.

Saxitoxin; Drinking water; Behavior; Aversive memory; Spatial memory; Rats

Authorship

Felipe Diehl ^** Correspondence: felipedhl@gmail.com

Postgraduate Program in Physical, Chemical and Geological Oceanography, Institute of Oceanography, Federal University of Rio Grande (FURG), Rio Grande, RS, Brazil.Federal University of Rio GrandeBrazilRio Grande, RS, BrazilPostgraduate Program in Physical, Chemical and Geological Oceanography, Institute of Oceanography, Federal University of Rio Grande (FURG), Rio Grande, RS, Brazil.

Institute of Oceanography, Federal University of Rio Grande (FURG), Caixa Postal 474, Rio Grande, RS CEP 96203-900, Brazil.Federal University of Rio GrandeBrazilRio Grande, RS, BrazilInstitute of Oceanography, Federal University of Rio Grande (FURG), Caixa Postal 474, Rio Grande, RS CEP 96203-900, Brazil.

Patricia Baptista Ramos

Juliane Marques dos Santos

Daniela Martí Barros

Postgraduate Program in Compared Animal Physiology, Institute of Biological Sciences, Federal University of Rio Grande (FURG), Rio Grande, RS, Brazil.Federal University of Rio GrandeBrazilRio Grande, RS, BrazilPostgraduate Program in Compared Animal Physiology, Institute of Biological Sciences, Federal University of Rio Grande (FURG), Rio Grande, RS, Brazil.

João Sarkis Yunes

* Correspondence: felipedhl@gmail.com

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

FD wrote the first draft of the manuscript and revised it; he also performed all behavioral experiments. PBR contributed to experimental design and animal maintenance. JMS performed all chromatographic analysis. DMB and JSY helped in designing all the experiments and corrected the final version of article. All authors read and approved the final manuscript.

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Figures

Figures (7)

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Fig. 1
Chromatogram showing PST from C. raciborskii used in the experiments. The toxin peak levels separated at 21.8, 32.2 and 37.7 min correspond to neosaxitoxin, dc-saxitoxin, and saxitoxin, respectively

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Fig. 2. a and b Absence of effect of all treatments in the OFH task. Data expressed as mean ± SEM; n= 10 per group. a Number of crossings and rearings in the test probe are significantly different from the corresponding training values for all groups (ANOVA test, p< 0.05)

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Fig. 3
Absence of effect of PST-producing C. raciborskii (9 μg/L STX equivalents) in the EPM task. Data expressed as mean ± SEM; n= 10 per group; TSCA: time spent at closed arms; TSOA: time spent at open arms; TSCA: time spent at central area

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Fig. 4
Effect of consumption of cyanobacteria-contaminated drinking water in the step-down IA task. Data expressed as median and interquartile intervals (training session in white; test session in gray); n= 10 rats per group. Kruskal-Wallis test shows no significant difference among training session latencies (p> 0.05). a Each of the five experimental groups has shown a significant difference between training and test session latencies (p< 0.05, Wilcoxon test). b Only the PST-producing C. raciborskii (9 μg/L STX equivalents) group showed a significant difference in the test session latency compared to the control group (p< 0.05, Dunn test)

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Fig. 5
Effect of consumption of cyanobacteria-contaminated drinking water in the training trial of MWM task. Data expressed as mean ± SEM; n= 15 rats per group. Both groups showed significant reduction in latency to find the platform during the four training days (p< 0.05, repeated measure ANOVA). The PST-producing C. raciborskii (9 μg/L STX equivalents) group showed a significant difference compared to the control group (p< 0.05, repeated measure ANOVA)

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Fig. 6
Effect of consumption of cyanobacteria-contaminated drinking water in the test session of MWM task. Data expressed as mean ± SEM; n= 15 rats per group. a Only the ASM-1 control group showed significant difference between time spent at TPQ and time spent at OPQ, p< 0.05 (one-way ANOVA test). b Rats treated with PST-producing C. raciborskii (9 μg/L STX equivalents) showed significant difference in the time spent at TPQ (p= 0.001, one-way ANOVA test and Tukey post-hoc test)

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Fig. 7
Absence of effect of PST-producing C. raciborskii (9 μg/L STX equivalents) on the swimming path length during the test session of the MWM task (p= 0.431, one-way ANOVA test). Data expressed as mean ± SEM; n= 15 per group

Fig. 1 Chromatogram showing PST from C. raciborskii used in the experiments. The toxin peak levels separated at 21.8, 32.2 and 37.7 min correspond to neosaxitoxin, dc-saxitoxin, and saxitoxin, respectively

Fig. 2. a and b Absence of effect of all treatments in the OFH task. Data expressed as mean ± SEM; n= 10 per group. a Number of crossings and rearings in the test probe are significantly different from the corresponding training values for all groups (ANOVA test, p< 0.05)

Fig. 3 Absence of effect of PST-producing C. raciborskii (9 μg/L STX equivalents) in the EPM task. Data expressed as mean ± SEM; n= 10 per group; TSCA: time spent at closed arms; TSOA: time spent at open arms; TSCA: time spent at central area

Fig. 4 Effect of consumption of cyanobacteria-contaminated drinking water in the step-down IA task. Data expressed as median and interquartile intervals (training session in white; test session in gray); n= 10 rats per group. Kruskal-Wallis test shows no significant difference among training session latencies (p> 0.05). a Each of the five experimental groups has shown a significant difference between training and test session latencies (p< 0.05, Wilcoxon test). b Only the PST-producing C. raciborskii (9 μg/L STX equivalents) group showed a significant difference in the test session latency compared to the control group (p< 0.05, Dunn test)

Fig. 5 Effect of consumption of cyanobacteria-contaminated drinking water in the training trial of MWM task. Data expressed as mean ± SEM; n= 15 rats per group. Both groups showed significant reduction in latency to find the platform during the four training days (p< 0.05, repeated measure ANOVA). The PST-producing C. raciborskii (9 μg/L STX equivalents) group showed a significant difference compared to the control group (p< 0.05, repeated measure ANOVA)

Fig. 6 Effect of consumption of cyanobacteria-contaminated drinking water in the test session of MWM task. Data expressed as mean ± SEM; n= 15 rats per group. a Only the ASM-1 control group showed significant difference between time spent at TPQ and time spent at OPQ, p< 0.05 (one-way ANOVA test). b Rats treated with PST-producing C. raciborskii (9 μg/L STX equivalents) showed significant difference in the time spent at TPQ (p= 0.001, one-way ANOVA test and Tukey post-hoc test)

Fig. 7 Absence of effect of PST-producing C. raciborskii (9 μg/L STX equivalents) on the swimming path length during the test session of the MWM task (p= 0.431, one-way ANOVA test). Data expressed as mean ± SEM; n= 15 per group

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[1] * Correspondence: felipedhl@gmail.com