Abstract
The present study was conducted to provide evidence of conditioned taste aversion learning (CTA) in the snail Cornu aspersum, using quinidine as the aversive stimulus in a procedure of Pavlovian Conditioning of Tentacle Lowering. Subjects were split into two groups: paired and unpaired. During the devaluation phase, subjects from the “paired group” received the US followed by the quinidine exposure, while subjects from the “unpaired group” received the quinidine and, 30 min later, the US. Subjects which had received the US paired with the quinidine showed a decrease of the conditioned response (CR), in contrast to subjects which had received the quinidine and the US unpaired. These results provide a useful CTA procedure in terrestrial snails. The implication of the results for learning and the physiological correlates is discussed.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10071-023-01760-7/MediaObjects/10071_2023_1760_Fig1_HTML.png)
Data availability
All data are available from the corresponding authors.
References
Bermudez-Rattoni F, McGaugh JL (1991) Insular cortex and amygdala lesions differentially affect acquisition on inhibitory avoidance and conditioned taste aversion. Brain Res 549:165–170. https://doi.org/10.1016/0006-8993(91)90616-4
Brookshire K, Brackbill R (1976) Formation and retention of conditioned taste aversions and UCS habituation. Bull Psychon Sac 7:125–128
Colby JJ, Smith NF (1977) The effect of three procedures for eliminating a conditioned taste aversion in the rat. Learn Motiv 8:404–413. https://doi.org/10.1016/0023-9690(77)90060-1
Darmaillacq AS, Dickel L, Chichery MP, Agin V, Chichery R (2004) Rapid taste aversion learning in adult cuttlefish, Sepia officinalis. Anim Behav 68:1291–1298. https://doi.org/10.1016/j.anbehav.2004.01.015
Escobar M, Dunaway EP, Gennaro KH (2014) Conditioned avoidance responses survive contingency degradation in the garden slug, Lehmannia valentiana. Learn Behav 42:305–312. https://doi.org/10.3758/s13420-014-0147-9
Gallo M, Cándido A (1995) Dorsal hippocampal lesions impair blocking but not latent inhibition of taste aversion learning in rats. Behav Neurosci 109:413. https://doi.org/10.1037/0735-7044.109.3.413
García J, Koelling RA (1966) Relation of cue to consequence in avoidance learning. Psychon Sci 4:123–124
Gaston KE (1978a) Brain mechanisms of conditioned taste aversion learning: a review of the literature. Physiol Psychol 6:340–353. https://doi.org/10.3758/BF03326736
Gaston KE (1978b) Interocular transfer of a visually mediated conditioned food aversion in chicks. Behav Biol 24:272–278. https://doi.org/10.1016/S0091-6773(78)93149-8
Gelperin A (1975) Rapid food-aversion learning by a terrestrial mollusk. Scien 189:567–570. https://doi.org/10.1126/science.1145215
Gustavson CR (1982) An evaluation of taste aversion control of wolf (Canis lupus) predation in Northern Minnesota. Appl Anim Ethol 9:63–71. https://doi.org/10.1016/0304-3762(82)90166-3
Gustavson CR, Nicolaus LK (1987) Taste aversion conditioning in wolves, coyotes, and other canids: retrospect and prospect. In: H.Frank (ed) Man and wolf: Advances, issues, and problems in captive wolf research, Springer Science & Business Media, 4:169–203.
Hall G, Channell S (1986) Context specificity of latent inhibition in taste aversion learning. QJEP 38:121–139
Harlander-Matauschek A, Beck P, Piepho HP (2009) Taste aversion learning to eliminate feather pecking in laying hens, Gallus gallus domesticus. Anim Behav 78:485–490. https://doi.org/10.1016/j.anbehav.2009.05.020
Hukema RK, Rademakers S, Jansen G (2008) Gustatory plasticity in C. elegans involves integration of negative cues and NaCl taste mediated by serotonin, dopamine, and glutamate. Learn Mem 15:829–836. https://doi.org/10.1101/lm.994408
Jacobs WJ, Zellner DA, LoLordo VM, Riley AL (1981) The effect of post-conditioning exposure to morphine on the retention of a morphine-induced conditioned taste aversion. Pharm Biochem Behav 14:779–785. https://doi.org/10.1016/0091-3057(81)90361-0
Kojima S, Nanakamura H, Nagayama S, Fujito Y, Ito E (1997) Enhancement of an inhibitory input to the feeding central pattern generator in Lymnaea stagnalis during conditioned taste-aversion learning. Neurosci Let 230:179–182. https://doi.org/10.1016/S0304-3940(97)00507-7
Laurent V, Westbrook RF, Balleine BW (2022) Affective valence regulates associative competition in pavlovian conditioning. Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2022.801474
Logue AW (1979) Taste aversion and the generality of the laws of learning. Psychological Bulletin 86:276–296. https://doi.org/10.1037/0033-2909.86.2.276
Loy I, Hall G (2002) Taste aversion after ingestion of lithium chloride: an associative analysis. QJEP 55B:365–380. https://doi.org/10.1080/02724990244000070
Lubow RE (2009) Conditioned taste aversion and latent inhibition: A review. In: Reilly S, Schachtman TR (eds) CTA: Behav Neural Process. Oxford University Press, pp 37–57
Maguire GS, Stojanovic D, Weston MA (2009) Conditioned taste aversion reduces fox depredation on model eggs on beaches. Wild Res 36:702–708. https://doi.org/10.1071/WR09123
Mason JR, Reidinger RF (1982) Observational learning of food aversions in red-winged blackbirds (Agelaius phoeniceus). Auk 99:548–554. https://doi.org/10.1093/auk/99.3.548
Massei G, Lyon A, Cowan DP (2003) Potential compounds for inducing conditioned taste aversion in ferrets. N Z J Zool 30:95–100. https://doi.org/10.1080/03014223.2003.9518328
Mikulka PJ, Leard B, Klein SB (1977) Illness-alone exposure as a source of interference with the acquisition and retention of a taste aversion. JEP: Anim Behav Process 3:189. https://doi.org/10.1037/0097-7403.3.2.189
Mizunami M (2021) What is learned in Pavlovian conditioning in crickets? Revisiting the SS and SR learning theories. Front Behav Neurosci 15:661225. https://doi.org/10.3389/fnbeh.2021.661225
Molero-Chamizo A (2007) Aprendizaje aversivo gustativo: características, paradigma y mecanismos cerebrales. An Psicol 23:57–64
Molero-Chamizo A (2017) Circadian-temporal context and latent inhibition of conditioned taste aversion: Effect of restriction in the intake of the conditioned taste stimulus. Learn Behav 45:157–163. https://doi.org/10.3758/s13420-016-0251-0
Nachman M (1963) Learned aversion to taste of lithium chloride and generalization to other salts. J C Physiol Psychol 56:343–349
Nakai J, Totani Y, Kojima S, Sakakibara M, Ito E (2020) Features of behavioral changes underlying conditioned taste aversion in the pond snail Lymnaea stagnalis. Invert Neurosci 20:1–11. https://doi.org/10.1007/s10158-020-00241-7
Paradis S, Cabanac M (2004) Flavor aversion learning induced by lithium chloride in reptiles but not in amphibians. Behav Process 67:11–18. https://doi.org/10.1016/j.beproc.2004.01.014
Parker LA (2003) Taste avoidance and taste aversion: evidence for two different processes. Anim Learn Behav 31:165–172. https://doi.org/10.3758/BF03195979
Price-Rees SJ, Webb JK, Shine R (2011) School for skinks: can conditioned taste aversion enable bluetongue lizards (Tiliqua scincoides) to avoid toxic cane toads (Rhinella marina) as prey? Ethol 117:749–757. https://doi.org/10.1111/j.1439-0310.2011.01935.x
Price-Rees SJ, Webb JK, Shine R (2013) Reducing the impact of a toxic invader by inducing taste aversion in an imperilled native reptile predator. Anim Conserv 16:386–394. https://doi.org/10.1111/acv.12004
Ratcliffe JM, Fenton MB, Galef BG (2003) An exception to the rule: common vampire bats do not learn taste aversion. Anim Behav 65:385–389. https://doi.org/10.1006/anbe.2003.2059
Rescorla RA (1973) Effects of US habituation following conditioning. J Comp Physiol Psychol 82(1):137. https://doi.org/10.1037/h0033815
Riley AL, Jacobs WJ, LoLordo VM (1976) Drug exposure and the acquisition and retention of a conditioned taste aversion. J C Physiol Psychol 90:799. https://doi.org/10.1037/h0077251
Rosas JM, García-Gutiérrez A, Callejas-Aguilera JE (2007) AAB and ABA renewal as a function of the number of extinction trials in conditioned taste aversion. Psicológica 28:129–150
Sahley C, Rudy JW, Gelperin A (1981) An analysis of associative learning in a terrestrial mollusc. J Comp Physiol 144:1–8. https://doi.org/10.1007/BF00612791
Selonen V, Banks PB, Tobajas J, Laaksonen T (2022) Protecting prey by deceiving predators: A field experiment testing chemical camouflage and conditioned food aversion. Biol Conserv 27:109749. https://doi.org/10.1016/j.biocon.2022.109749
Steinfeld MR, Bouton ME (2020) Context and renewal of habits and goal-directed actions after extinction. J Exp Psychol: Anim Learn Cogn 46:408. https://doi.org/10.1037/xan0000247
Steinfeld MR, Bouton ME (2021) Renewal of goal direction with a context change after habit learning. Behav Neurosci 135:79. https://doi.org/10.1037/bne0000422
Tobajas J, Gómez-Ramírez P, María-Mojica P, Navas I, García-Fernández AJ, Ferreras P, Mateo R (2019) Conditioned food aversion mediated by odour cue and microencapsulated levamisole to avoid predation by canids. E J Wild Res 65:1–8. https://doi.org/10.1007/s10344-019-1271-9
Tobajas J, Descalzo E, Mateo R, Ferreras P (2020) Reducing nest predation of ground-nesting birds through conditioned food aversion. Biol Conserv 242:108405. https://doi.org/10.1016/j.biocon.2020.108405
Ungless MA (2001) Dissociation of food-finding and tentacle-lowering, following food- attraction conditioning in the snail, Helix aspersa. Behav Process 53:97–101. https://doi.org/10.1016/S0376-6357(01)00136-X
Van Damme S, De Fruyt N, Watteyne J, Kenis S, Peymen K, Schoofs L, Beets I (2021) Neuromodulatory pathways in learning and memory: lessons from invertebrates. J Neuroend 33:e12911. https://doi.org/10.1111/jne.12911
Verendeev A, Riley AL (2012) Conditioned taste aversion and drugs of abuse: history and interpretation. Neurosci Biobehav Rev 36:2193–2205. https://doi.org/10.1016/j.neubiorev.2012.08.004
Ward-Fear G, Thomas J, Webb JK, Pearson DJ, Shine R (2017) Eliciting conditioned taste aversion in lizards: live toxic prey are more effective than scent and taste cues alone. Integrav Zool 12:112–120. https://doi.org/10.1111/1749-4877.12226
Welzl H, D’Adamo P, Lipp HP (2001) Conditioned taste aversion as a learning and memory paradigm. Behav Brain Res 125:205–213. https://doi.org/10.1016/S0166-4328(01)00302-3
Yamamoto T, Fujimoto Y (1991) Brain mechanisms of taste aversion learning in the rat. Brain Res Bull 27:403–406. https://doi.org/10.1016/0361-9230(91)90133-5
Yamamoto T, Shimura T, Sako N, Yasoshima Y, Sakai N (1994) Neural substrates for conditioned taste aversion in the rat. Behav Brain Res 65:123–137. https://doi.org/10.1016/0166-4328(94)90097-3
Yamamoto T, Fujimoto Y, Shimura T, Sakai N (1995) Conditioned taste aversion in rats with excitotoxic brain lesions. Neurosci Res 22:31–49. https://doi.org/10.1016/0168-0102(95)00875-T
Ziegler JM, Gustavson CR, Holzer GA, Gruber D (1983) Anthelmintic-based taste aversions in wolves (Canis lupus). Appl Anim Ethol 9:373–377. https://doi.org/10.1016/0304-3762(83)90017-2
Acknowledgements
We are very grateful to Guillermo Cárcaba and Iria Prieto for their participation; Dra. Clara Muñiz-Diez for her comments; and Pablo Rubio for his participation and comments. Also, we deeply thank Dr. Rodrigo Pérez Lorido for his review of the linguistic aspects of this manuscript.
Funding
This research was supported by Vicerrectorado de Investigación de la Universidad de Oviedo, ayudas pre-doctorales (Ref: PAPI-21-PF-26).
Author information
Authors and Affiliations
Contributions
Authors’ participation was equal.
Corresponding author
Ethics declarations
Conflict of interest
Authors have no conflict of interest.
Ethical approval
There are no studies with human participants. The standards for laboratory animal protection form 2010/63/UE and RD53/2013 and all applicable international, national, and/or institutional guidelines for the care and use of invertebrates were followed.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Muñiz Moreno, J., Loy, I. Taste aversion learning in the snail Cornu aspersum. Anim Cogn 26, 1097–1102 (2023). https://doi.org/10.1007/s10071-023-01760-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-023-01760-7