Skip to main content
SpringerLink
Log in

The ontogeny of continuous quantity discrimination in zebrafish larvae (Danio rerio)

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

Several studies have investigated the ontogeny of the capacity to discriminate between discrete numerical information in human and non-human animals. Contrarily, less attention has been devoted to the development of the capacity to discriminate continuous quantities. Recently, we set up a fast procedure for screening continuous quantity abilities in adult individuals of an animal model in neurodevelopmental research, the zebrafish. Two different sized holes are presented in a wall that divides the home tank in two halves and the spontaneous preference of fish for passing through the larger hole is exploited to measure their discrimination ability. We tested zebrafish larvae in the first, second and third week of life varying the relative size of the smaller circle (0.60, 0.75, 0.86, 0.91 area ratio). We found that the number of passages increased across the age. The capacity to discriminate the larger hole decreased as the ratio between the areas increased. No difference in accuracy was found as a function of age. The accuracy of larval zebrafish almost overlaps that found in adults in a previous study, suggesting a limited role of maturation and experience on the ability to estimate areas in this species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon request.

References

  • Agrillo C, Bisazza A (2014) Spontaneous versus trained numerical abilities: a comparison between the two main tools to study numerical competence in non-human animals. J Neurosci Meth 234:82–91

    Google Scholar 

  • Agrillo C, Bisazza A (2018) Understanding the origin of number sense: a review of fish studies. Philos T R Soc B 373:20160511

    Google Scholar 

  • Agrillo C, Piffer L, Adriano A (2013) Individual differences in non-symbolic numerical abilities predict mathematical achievements but contradict ATOM. Behav Brain Funct 9:26

    PubMed  PubMed Central  Google Scholar 

  • Barabassy A, Beinhoff U, Riepe MW (2010) Cognitive estimation in aged patients with major depressive disorder. Psychiat Res 176:26–29

    Google Scholar 

  • Barker AJ, Baier H (2015) Sensorimotor decision making in the zebrafish tectum. Curr Biol 25:2804–2814

    CAS  PubMed  Google Scholar 

  • Barry M, Shanas U, Brunton DH (2014) Year-round mixed-age shelter aggregations in Duvaucel's geckos (Hoplodactylus duvaucelii). Herpetologica 70:395–406

    Google Scholar 

  • Beran MJ, Parrish AE (2016) Going for more: Discrete and continuous quantity judgments by nonhuman animals. In: Continuous issues in numerical cognition. Academic Press, pp 175–192

  • Bianco IH, Kampff AR, Engert F (2011) Prey capture behavior evoked by simple visual stimuli in larval zebrafish. Front Syst Neurosci 5:101

    PubMed  PubMed Central  Google Scholar 

  • Bilotta J, Saszik S (2001) The zebrafish as a model visual system. Int J Dev Neurosci 19:621–629

    CAS  PubMed  Google Scholar 

  • Bisazza A, Manfredi S, Pilastro A (2000) Sexual competition, coercive mating and mate assessment in the one-sided livebearer, Jenynsia multidentata: are they predictive of sexual dimorphism? Ethology 106:961–978

    Google Scholar 

  • Bisazza A, Piffer L, Serena G, Agrillo C (2010) Ontogeny of numerical abilities in fish. PLoS ONE 5:e15516

    PubMed  PubMed Central  Google Scholar 

  • Brand M, Kalbe E, Fujiwara E, Huber M, Markowitsch HJ (2003) Cognitive estimation in patients with probable Alzheimer’s disease and alcoholic Korsakoff patients. Neuropsychologia 41:575–584

    PubMed  Google Scholar 

  • Brannon EM, Lutz D, Cordes S (2006) The development of area discrimination and its implications for number representation in infancy. Dev Sci 9:F59–F64

    PubMed  PubMed Central  Google Scholar 

  • Brennan CH (2011) Zebrafish behavioural assays of translational relevance for the study of psychiatric disease. Rev Neurosci 22:37–48

    PubMed  Google Scholar 

  • Buckley CE, Goldsmith P, Franklin RJ (2008) Zebrafish myelination: a transparent model for remyelination? Dis Model Mech 1:221–228

    CAS  PubMed  PubMed Central  Google Scholar 

  • Butterworth B, Reeve R, Reynolds F (2011) Using mental representations of space when words are unavailable: studies of enumeration and arithmetic in indigenous Australia. J Cross Cult Psychol 42:630–638

    Google Scholar 

  • Colwill RM, Creton R (2011) Locomotor behaviors in zebrafish (Danio rerio) larvae. Behav Process 86:222–229

    Google Scholar 

  • Cordes S, Brannon EM (2008) Quantitative competencies in infancy. Dev Sci 11:803–808

    PubMed  Google Scholar 

  • Ditz HM, Nieder A (2016) Numerosity representations in crows obey the Weber-Fechner law. Proc R S B Biol Sci 283(1827):20160083

    Google Scholar 

  • Dosen LD, Montgomerie R (2004) Female size influences mate preferences of male guppies. Ethology 110:245–255

    Google Scholar 

  • Eriksen CW, Hake HW (1955) Multidimensional stimulus differences and accuracy of discrimination. J Exp Psychol 50:153

    CAS  PubMed  Google Scholar 

  • Feigenson L (2007) The equality of quantity. Trends Cogn Sci 11(5):185–187

    PubMed  Google Scholar 

  • Feigenson L, Carey S, Spelke E (2002) Infants' discrimination of number vs continuous extent. Cognit Psychol 44:33–66

    PubMed  Google Scholar 

  • Fenson L, Dale PS, Reznick JS, Bates E, Thal DJ, Pethick SJ, Stiles J (1994) Variability in early communicative development. Monogr Soc Res Child 1:185

    Google Scholar 

  • Fero K, Yokogawa T, Burgess HA (2011) The behavioral repertoire of larval zebrafish. Zebrafish models in neurobehavioral research. Humana Press, Totowa, New York, pp 249–291

    Google Scholar 

  • Forsatkar MN, Safari O, Boiti C (2017) Effects of social isolation on growth, stress response, and immunity of zebrafish. Acta Etholog 20:255–261

    Google Scholar 

  • Fuiman LA, Webb PW (1988) Ontogeny of routine swimming activity and performance in zebra danios (Teleostei: Cyprinidae). Anim Behav 36:250–261

    Google Scholar 

  • Gandini D, Lemaire P, Michel BF (2009) Approximate quantification in young, healthy older adults’, and Alzheimer patients. Brain Cognition 70:53–61

    PubMed  Google Scholar 

  • Gazzola A, Vallortigara G, Pellitteri-Rosa D (2018) Continuous and discrete quantity discrimination in tortoises. Biol Lett 14:20180649

    PubMed  PubMed Central  Google Scholar 

  • Girelli L, Luzzatti C, Annoni G, Vecchi T (1999) Progressive decline of numerical skills in Alzheimer-type dementia: a case study. Brain Cognition 40:132–136

    Google Scholar 

  • Halberda J, Mazzocco MM, Feigenson L (2008) Individual differences in non-verbal number acuity correlate with maths achievement. Nature 455:665

    CAS  PubMed  Google Scholar 

  • Haug MF, Biehlmaier O, Mueller KP, Neuhauss SC (2010) Visual acuity in larval zebrafish: behavior and histology. Front Zool 7:8

    PubMed  PubMed Central  Google Scholar 

  • Henik A (ed) (2016) Continuous issues in numerical cognition: how many or how much. Academic Press, Cambridge

    Google Scholar 

  • Izard V, Sann C, Spelke ES, Streri A (2009) Newborn infants perceive abstract numbers. Proc Natl Acad Sci 106:10382–10385

    CAS  PubMed  Google Scholar 

  • Kalueff AV, Echevarria DJ, Stewart AM (2014) Gaining translational momentum: more zebrafish models for neuroscience research. Prog Neuro-psychoph 55:1–6

    Google Scholar 

  • Kulkarni P, Yellanki S, Medishetti R, Sriram D, Saxena U, Yogeeswari P (2017) Novel Zebrafish EAE model: a quick in vivo screen for multiple sclerosis. Mult Scler Relat Dis 11:32–39

    Google Scholar 

  • Levin BE, Llabre MM, Weiner WJ (1989) Cognitive impairments associated with early Parkinson's disease. Neurology 39:557–557

    CAS  PubMed  Google Scholar 

  • Lucon-Xiccato T, Miletto Petrazzini ME, Agrillo C, Bisazza A (2015) Guppies discriminate between two quantities of food items but prioritize item size over total amount. Anim Behav 107:183–191

    Google Scholar 

  • Maack G, Segner H (2003) Morphological development of the gonads in zebrafish. J Fish Biol 62:895–906

    Google Scholar 

  • McElligott MB, O’Malley DM (2005) Prey tracking by larval zebrafish: axial kinematics and visual control. Brain Behav Evolut 66:177–196

    Google Scholar 

  • Miletto Petrazzini ME, Agrillo C, Piffer L, Bisazza A (2014) Ontogeny of the capacity to compare discrete quantities in fish. Dev Psychobiol 56:529–536

    PubMed  Google Scholar 

  • Miletto Petrazzini ME, Fraccaroli I, Gariboldi F, Agrillo C, Bisazza A, Bertolucci C, Foà A (2017) Quantitative abilities in a reptile (Podarcis sicula). Biol Lett 1320160899

  • Miller GA (1956) The magical number seven, plus or minus two: Some limits on our capacity for processing information. Psychol Rev 63:81–97

    CAS  Google Scholar 

  • Moll FW, Nieder A (2014) The long and the short of it: Rule-based relative length discrimination in carrion crows, Corvus corone. Behav Process 107:142–149

    Google Scholar 

  • Morris JC, Storandt M, Miller JP, McKeel DW, Price JL, Rubin EH, Berg L (2001) Mild cognitive impairment represents early-stage Alzheimer disease. Arch Neurol-Chicago 58:397–405

    CAS  PubMed  Google Scholar 

  • Mueller KP, Neuhauss SC (2010) Quantitative measurements of the optokinetic response in adult fish. J Neurosci Meth 186:29–34

    Google Scholar 

  • Newman M, Ebrahimie E, Lardelli M (2014) Using the zebrafish model for Alzheimer’s disease research. Front Genet 5:189

    PubMed  PubMed Central  Google Scholar 

  • Norton WHJ (2013) Toward developmental models of psychiatric disorders in zebrafish. Front Neural Circuit 7:79

    Google Scholar 

  • Paquet D, Bhat R, Sydow A, Mandelkow EM, Berg S, Hellberg S, Haass C (2009) A zebrafish model of tauopathy allows in vivo imaging of neuronal cell death and drug evaluation. J Clin Invest 119:1382–1395

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pica P, Lemer C, Izard V, Dehaene S (2004) Exact and approximate arithmetic in an Amazonian indigene group. Science 306:499–503

    CAS  PubMed  Google Scholar 

  • Piffer L, Miletto Petrazzini ME, Agrillo C (2013) Large number discrimination in newborn fish. PLoS ONE 8:e62466

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pitcher TJ (1986) Functions of shoaling behaviour in teleosts. The behaviour of teleost fishes. Springer, Boston, pp 294–337

    Google Scholar 

  • Price GR, Palmer D, Battista C, Ansari D (2012) Nonsymbolic numerical magnitude comparison: reliability and validity of different task variants and outcome measures, and their relationship to arithmetic achievement in adults. Acta Psychol 140:50–57

    Google Scholar 

  • Revkin SK, Piazza M, Izard V, Zamarian L, Karner E, Delazer M (2008) Verbal numerosity estimation deficit in the context of spared semantic representation of numbers: a neuropsychological study of a patient with frontal lesions. Neuropsychologia 46:2463–2475

    PubMed  Google Scholar 

  • Richendrfer H, Pelkowski SD, Colwill RM, Creton R (2012) On the edge: pharmacological evidence for anxiety-related behavior in zebrafish larvae. Behav Brain Res 228:99–106

    CAS  PubMed  Google Scholar 

  • Rugani R, Fontanari L, Simoni E, Regolin L, Vallortigara G (2009) Arithmetic in newborn chicks. Proc R Soc B-Biol Sci 276:2451–2460

    Google Scholar 

  • Rugani R, Regolin L, Vallortigara G (2007) Rudimental numerical competence in 5-day-old domestic chicks (Gallus gallus): identification of ordinal position. J Exp Psychol Anim B 33:21

    Google Scholar 

  • Rugani R, Vallortigara G, Regolin L (2015) At the root of the left–right asymmetries in spatial–numerical processing: from domestic chicks to human subjects. J Cogn Psychol 27:388–399

    Google Scholar 

  • Rule SJ (1969) Subject difference in exponents from circle size, numerousness, and line length. Psychon Sci 15:284–285

    Google Scholar 

  • Santacà M, Caja T, Miletto Petrazzini ME, Agrillo C, Bisazza A (2020) Size discrimination in adult zebrafish (Danio rerio): Normative data and individual variation. Sci Rep-UK 10:1–12

    Google Scholar 

  • Sarvaiya VN, Sadariya KA, Rana MP, Thaker AM (2014) Zebrafish as model organism for drug discovery and toxicity testing: a review. Vet Clin Sci 2:31–38

    Google Scholar 

  • Schusterman RJ, Kellogg WN, Rice CE (1965) Underwater visual discrimination by the California sea lion. Science 147:1594–1596

    CAS  PubMed  Google Scholar 

  • Tappeiner C, Gerber S, Enzmann V, Balmer J, Jazwinska A, Tschopp M (2012) Visual acuity and contrast sensitivity of adult zebrafish. Front Zool 9:10

    PubMed  PubMed Central  Google Scholar 

  • Xi Y, Noble S, Ekker M (2011) Modeling neurodegeneration in zebrafish. Curr Neurol Neurosci 11:274–282

    CAS  Google Scholar 

  • Xu F, Arriaga RI (2007) Number discrimination in 10-month-old infants. Brit J Dev Psychol 25:103–108

    Google Scholar 

  • Xu F, Spelke ES (2000) Large number discrimination in 6-month-old infants. Cognition 74:B1–B11

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Stefano Massaccesi for his help in setting up the experimental apparatus and Denisa Margjonaj for her help with testing the animals and with the video analyses. This research was supported by “PRIN 2015” (prot.: 2015FFATB7) to A.B. from Università di Padova, by “Stars@unipd” Grant (ANIM_ILLUS) to C.A. from Università di Padova and by “Marie Sklodowska-Curie Action” (MSCA 750200) to M.E.M.P. We performed the present work within the scope of the research grant ‘Dipartimenti di Eccellenza’ entitled ‘Innovative methods or technologies for assessment, intervention, or enhancement of psychological functions (cognitive, emotional or behavioural)’.

Author information

Authors and Affiliations

  1. Department of General Psychology, University of Padova, Via Venezia 8, 35131, Padua, Italy

    Maria Santacà, Christian Agrillo & Angelo Bisazza

  2. Padova Neuroscience Center, University of Padova, Padua, Italy

    Christian Agrillo & Angelo Bisazza

  3. School of Biological and Chemical Sciences, Queen Mary University of London, London, UK

    Maria Elena Miletto Petrazzini

Authors
  1. Maria Santacà
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christian Agrillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maria Elena Miletto Petrazzini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Angelo Bisazza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Santacà.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

The experiments were approved by the Ethical Committee of the Università di Padova (protocol no. 61/2018) and adhered to the current legislation of the country in which they were performed (Italy, Decreto Legislativo 4 Marzo 2014, no. 26).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file 1 (DOCX 25 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Santacà, M., Agrillo, C., Miletto Petrazzini, M.E. et al. The ontogeny of continuous quantity discrimination in zebrafish larvae (Danio rerio). Anim Cogn 23, 731–739 (2020). https://doi.org/10.1007/s10071-020-01384-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-020-01384-1

Keywords

Search

Navigation