Abstract
Fluoride occurs naturally in the terrestrial and aquatic environment and is a major component in tea. Prolonged fluoride exposure alters metabolic activity in several aquatic invertebrates. For the first time, we investigated the effects of fluoride on cognition in the pond snail Lymnaea stagnalis as it is capable of a higher form of associative learning called configural learning. We first showed suppressive effects of black tea and fluoride on feeding (i.e., rasping) behavior. We then investigated how fluoride may alter cognition by introducing fluoride (1.86 mg/L) before, during, after, a day before and a week before the snails underwent the configural learning training procedure. Our results show that any 45-min exposure to fluoride (before, during or after a configural learning training procedure) blocks configural learning memory formation in Lymnaea and these effects are long-lasting. One week after a fluoride exposure, snails are still unable to form a configural learning memory and this result is upheld when the snails are exposed to a lower concentration of fluoride, one which is naturally occurring in ponds that a wild strain of Lymnaea can be found (0.3 mg/L). Thus, fluoride obstructs configural learning memory formation in a fluoride-naïve, inbred strain of Lymnaea.
Keywords: Associative learning; Configural learning; Fluoridation; Long-term memory; Pond snail.
*Original abstract online at https://link.springer.com/article/10.1007%2Fs00359-021-01528-9
Author Affiliations
Bevin Wiley, Anuradha Batabyal & Ken Lukowi: Hotchkiss Brain Institute, Cumming School of Medicine, University of Calgary, 3330 Hospital Drive NW, Calgary, AB, T2N 4N1, Canada
Funding
The current study was supported by Natural Sciences and Engineering Research Council of Canada [grant number: 227993-2019].
References
-
Aguirre-Sierra A, Alonso Á, Camargo JA (2011) Contrasting sensitivities to fluoride toxicity between juveniles and adults of the aquatic snail Potamopyrgus antipodarum (Hydrobiidae, Mollusca). Bull Environ Contam Toxicol 86:476–479. https://doi.org/10.1007/s00128-011-0241-z
-
Alexander JE, Covich AP (1991) Predation risk and avoidance behavior in two freshwater snails. Biol Bull 180:387–393. https://doi.org/10.2307/1542339
-
Batabyal A, Lukowiak K (2021) Configural learning memory can be transformed from intermediate-term to long-term in pond snail Lymnaea stagnalis. Physiol Behav 239:113509. https://doi.org/10.1016/J.PHYSBEH.2021.113509
-
Camargo JA (2003) Fluoride toxicity to aquatic organisms: a review. Chemosphere 50(3):251–264
-
Camargo JA, Alonso Á (2017) Ecotoxicological assessment of the impact of fluoride (F?) and turbidity on the freshwater snail Physella acuta in a polluted river receiving an industrial effluent. Environ Sci Pollut Res 24:15667–15677. https://doi.org/10.1007/s11356-017-9208-x
-
CEPA (1994) Canadian Environmental Protection Act, 1994. Priority substances list supporting document for inorganic fluorides. Prepared by Eco-Health Branch and Environment Canada, Ottawa
-
Dalesman S, Lukowiak K (2010) Effect of acute exposure to low environmental calcium on respiration and locomotion in Lymnaea stagnalis (L.). J Exp Biol 213:1471–1476. https://doi.org/10.1242/jeb.040493
-
Dobbs GG (1974) Fluoride and the environment. Fluoride 7(1974):123–135
-
Dong YT, Wang Y, Wei N, Zhang QF, Guan ZZ (2015) Deficit in learning and memory of rats with chronic fluorosis correlates with the decreased expressions of M1 and M3 muscarinic acetylcholine receptors. Arch Toxicol 89:1981–1991. https://doi.org/10.1007/s00204-014-1408-2
-
Dyer AG (2012) The mysterious cognitive abilities of bees: why models of visual processing need to consider experience and individual differences in animal performance. J Exp Biol 215:387–395. https://doi.org/10.1242/JEB.038190
-
Fluoride in Calgary’s water [WWW Document]. 2021. URL https://www.calgary.ca/uep/water/drinking-water/fluoride.html. Accessed 4 Dec 2021
-
Fung KF, Zhang ZQ, Wong JW, Wong MH (1999) Fluoride contents in tea and soil from tea plantations and the release of fluoride into tea liquor during infusion. Environ Poll 104(2):197–205
-
Garcia J, Kimeldorf DJ, Koelling RA (1955) Conditioned aversion to saccharin resulting from exposure to gamma radiation. Science 122:157–158. https://doi.org/10.1126/SCIENCE.122.3160.157
-
Hagen HA (1870) Monograph of the North American astacidae. In illustrated catalogue of the museum of comparative zoology at Harvard College 3: viii
-
Ito E, Kojima S, Lukowiak K, Sakakibara M (2013) From likes to dislikes: conditioned taste aversion in the great pond snail (Lymnaea stagnalis). Can J Zool 91:405–412. https://doi.org/10.1139/cjz-2012-0292
-
Kagan D, Lukowiak K (2019) Configural learning in freshly collected, smart, wild Lymnaea. J Exp Biol 222:jeb212886. https://doi.org/10.1242/jeb.212886
-
Korneev SA, Vavoulis DV, Naskar S, Dyakonova VE, Kemenes I, Kemenes G (2018) A CREB2-targeting microRNA is required for long-term memory after single-trial learning. Sci Rep 81(8):1–12. https://doi.org/10.1038/s41598-018-22278-w
-
Laundré JW, Hernández L, Altendorf KB (2001) Wolves, elk, and bison: reestablishing the “landscape of fear” in Yellowstone National Park, USA. https://doi.org/10.1139/cjz-79-8-1401
-
Linnaeus CV (1758) Systema naturae, 1
-
Liu YJ, Gao Q, Wu CX, Guan ZZ (2010) Alterations of nAChRs and ERK1/2 in the brains of rats with chronic fluorosis and their connections with the decreased capacity of learning and memory. Toxicol Lett 192:324–329. https://doi.org/10.1016/j.toxlet.2009.11.002
-
Lu YI, Guo WF, Yang XQ (2004) Fluoride content in tea and its relationship with tea quality. J Agric Food Chem 52(14):4472–4476
-
Lukowiak K, Sunada H, Teskey M, Lukowiak K, Dalesman S (2014) Environmentally relevant stressors alter memory formation in the pond snail Lymnaea. J Exp Biol 217(1):76–83
-
Orr MV, Lukowiak K (2008) Electrophysiological and behavioral evidence demonstrating that predator detection alters adaptive behaviors in the snail Lymnaea. J Neurosci 28:2726–2734. https://doi.org/10.1523/JNEUROSCI.5132-07.2008
-
Orr MV, El-Bekai M, Lui M, Watson K, Lukowiak K (2007) Predator detection in Lymnaea stagnalis. J Exp Biol 210:4150–4158. https://doi.org/10.1242/jeb.010173
-
Ribeiro MJ, Schofield MG, Kemenes I, O’Shea M, Kemenes G, Benjamin PR (2005) Activation of MAPK is necessary for long-term memory consolidation following food-reward conditioning. Learn Mem 12:538–545. https://doi.org/10.1101/LM.8305
-
Rigby MC, Jokela J (2000) Predator avoidance and immune defence: costs and trade–offs in snails. Proc R Soc Lond Ser B Biol Sci 267:171–176. https://doi.org/10.1098/rspb.2000.0983
-
Rivi V, Benatti C, Colliva C, Radighieri G, Brunello N, Tascedda F, Blom JMC (2020) Lymnaea stagnalis as model for translational neuroscience research: from pond to bench. Neurosci Biobehav Rev 108:602–616. https://doi.org/10.1016/J.NEUBIOREV.2019.11.020
-
Rivi V, Batabyal A, Juego K, Kakadiya M, Benatti C, Blom JMC, Lukowiak K (2021) To eat or not to eat: a Garcia effect in pond snails (Lymnaea stagnalis). J Comp Physiol A 207:479–495. https://doi.org/10.1007/S00359-021-01491-5
-
Rosenegger D, Lukowiak K (2010) The participation of NMDA receptors, PKC, and MAPK in the formation of memory following operant conditioning in Lymnaea. Mol Brain 3:24. https://doi.org/10.1186/1756-6606-3-24
-
Sadamoto H, Sato H, Kobayashi S, Murakami J, Aonuma H, Ando H, Fujito Y, Hamano K, Awaji M, Lukowiak K, Urano A, Ito E (2004) CREB in the pond snail Lymnaea stagnalis: cloning, gene expression and function in identifiable neurons of the central nervous system. J Neurobiol 58:455–466. https://doi.org/10.1002/NEU.10296
-
Schafe GE, Atkins CM, Swank MW, Bauer EP, Sweatt JD, LeDoux JE (2000) Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of pavlovian fear conditioning. J Neurosci 20:8177–8187. https://doi.org/10.1523/JNEUROSCI.20-21-08177.2000
-
Seligman ME (1970) On the generality of the laws of learning. Psychol Rev 77:406–418. https://doi.org/10.1037/h0029790
-
Sigler WF, Neuhold JM (1972) Fluoride intoxication in fish: a review. J Wildl Dis 8(3):252–254
-
Skjelkvåle BL (1994) Water chemistry in areas with high deposition of fluoride. Sci Tot Environ 152(2):105–112
-
Šket T, Kukec A, Kosem R, Artnik B (2017) The history of public health use of fluorides in caries prevention. Slov J Public Heal 56:140–146. https://doi.org/10.1515/sjph-2017-0018
-
Spyra A, Strzelec M (2014) Identifying factors linked to the occurrence of alien gastropods in isolated woodland water bodies. Naturwissenschaften 101:229–239. https://doi.org/10.1007/s00114-014-1153-7
-
Swinton C, Swinton E, Shymansky T, Hughes E, Zhang J, Rothwell C, Kakadiya M, Lukowiak K (2019) Configural learning: a higher form of learning in Lymnaea. J Exp Biol 222:jeb190405. https://doi.org/10.1242/jeb.190405
-
Taylor L, Watkins SL, Marshall H, Dascombe BJ, Foster J (2016) The impact of different environmental conditions on cognitive function: a focused review. Front Physiol 6(6):372
-
USDA Nutrient Data Laboratory Beltsville Human Nutrition Research Center Agricultural Research Service (2005) USDA national fluoride database of selected beverages and foods, vol 26. USDA National Fluoride Database of Selected Beverages and Foods, USA
-
Zanette LY, Clinchy M (2019) Ecology of fear. Curr Biol 29:R309–R313. https://doi.org/10.1016/J.CUB.2019.02.042
-
Zhang J, de Freitas E, Lukowiak K (2018) Black tea differs from green tea: it suppresses long-term memory formation in Lymnaea. Comm Int Biol 11(3):1–4
-
Zhao Q, Niu Q, Chen J, Xia T, Zhou G, Li P, Dong L, Xu C, Tian Z, Luo C, Liu L, Zhang S, Wang A (2019) Roles of mitochondrial fission inhibition in developmental fluoride neurotoxicity: mechanisms of action in vitro and associations with cognition in rats and children. Arch Toxicol 93:709–726. https://doi.org/10.1007/S00204-019-02390-0
-
-
Study on the correlation between daily total fluoride intake and children’s intelligence quotient.
Objective: To explore the exact relationship between daily total intake of fluoride and children's intelligence quotient (IQ). Methods: Wamiao village (severely endemic fluorosis area, drinking water fluoirde was 0.57-4.50 mgL) and Hinhuai village (non-endemic fluorosis area, drinking water fluoride was 0.18-0.76 mgL-1) in Shong County, Jiangsu Province, were selected for this
-
Developmental Fluoride Neurotoxicity: Choi et al. Respond
Sabour and Ghorbani’s comments about the reported mean difference in IQ (intelligence quotient) scores reported in our article (Choi et al. 2012) suggest a misunderstanding of the scale unit we used and the public health significance of even a small decrease in the average IQ associated with exposure. We appreciate
-
Developmental neurotoxicity of fluoride: a quantitative risk analysis toward establishing a safe daily dose of fluoride for children
Background: A recent 2015 study from New Zealand indicated water fluoridation did not have an effect on children’s IQs. A 2012 meta-analysis showed that children with higher fluoride exposure have lower IQs than similar children with lower exposures. Levels of the fluoride ion (F) in blood and urine in children
-
WITHDRAWN: Co-exposure effects of arsenic and fluoride on intelligence and oxidative stress in school-aged children: a cohort study.
This article has been withdrawn at the request of the editor. The Publisher apologizes for any inconvenience this may cause. as of November 6, 2020 Highlights Pioneer biomonitoring study on rural children to address As and F- co-exposure. High dental Fluorosis found in relation to urinary As and F- levels in
-
Exposure to fluoride aggravates the impairment in learning and memory and neuropathological lesions in mice carrying the APP/PS1 double-transgenic mutation.
BACKGROUND: Alzheimer's disease (AD) is responsible for 60-70% of all cases of dementia. On the other hand, the tap water consumed by hundreds of millions of people has been fluoridated to prevent tooth decay. However, little is known about the influence of fluoride on the expression of APP and subsequent
Related Studies :
-
-
-
Fluoride Affects Learning & Memory in Animals
An association between elevated fluoride exposure and reduced intelligence has now been observed in 65 IQ studies. Although a link between fluoride and intelligence might initially seem surprising or random, it is actually consistent with a large body of animal research. This animal research includes the following 45 studies (out
-
Fluoride's Direct Effects on Brain: Animal Studies
The possibility that fluoride ingestion may impair intelligence and other indices of neurological function is supported by a vast body of animal research, including over 40 studies that have investigated fluoride's effects on brain quality in animals. As discussed by the National Research Council, the studies have consistently demonstrated that fluoride, at widely varying concentrations, is toxic to the brain.
-
NRC (2006): Fluoride's Neurotoxicity and Neurobehavioral Effects
The NRC's analysis on fluoride and the brain.
-
Fluoride & IQ: 76 Studies
• As of July 18, 2022, a total of 85 human studies have investigated the relationship between fluoride and human intelligence. • Of these investigations, 76 studies have reported that elevated fluoride exposure is associated with reduced IQ in humans. • The studies which reported an association of reduced IQ with exposure
-
Fluoride's Effect on Fetal Brain
The human placenta does not prevent the passage of fluoride from a pregnant mother's bloodstream to the fetus. As a result, a fetus can be harmed by fluoride ingested pregnancy. Based on research from China, the fetal brain is one of the organs susceptible to fluoride poisoning. As highlighted by the excerpts
Related FAN Content :
-