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Characterizing ontogeny of quantity discrimination in zebrafish

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Proceedings of the Royal Society B
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Eva Sheardown
Eva Sheardown
Eva Sheardown
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Jose Vicente Torres Pérez at University of Valencia
Jose Vicente Torres Pérez
Sofia Anagianni
Sofia Anagianni
Sofia Anagianni
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Scott Fraser at University of Southern California
Scott Fraser
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Abstract

A sense of non-symbolic numerical magnitudes is widespread in the animal kingdom and has been documented in adult zebrafish. Here, we investigated the ontogeny of this ability using a group size preference (GSP) task in juvenile zebrafish. Fish showed GSP from 21 days post-fertilization and reliably chose the larger group when presented with discriminations of between 1 versus 3, 2 versus 5 and 2 versus 3 conspecifics but not 2 versus 4 conspecifics. When the ratio between the number of conspecifics in each group was maintained at 1 : 2, fish could discriminate between 1 versus 2 individuals and 3 versus 6, but again, not when given a choice between 2 versus 4 individuals. These findings are in agreement with studies in other species, suggesting the systems involved in quantity representation do not operate separately from other cognitive mechanisms. Rather they suggest quantity processing in fishes may be the result of an interplay between attentional, cognitive and memory-related mechanisms as in humans and other animals. Our results emphasize the potential of the use of zebrafish to explore the genetic and neural processes underlying the ontogeny and function of number cognition.
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Research
Cite this article: Sheardown E, Torres-Perez
JV, Anagianni S, Fraser SE, Vallortigara G,
Butterworth B, Miletto-Petrazzini ME, Brennan
CH. 2022 Characterizing ontogeny of quantity
discrimination in zebrafish. Proc. R. Soc. B 289:
20212544.
https://doi.org/10.1098/rspb.2021.2544
Received: 22 November 2021
Accepted: 7 January 2022
Subject Category:
Behaviour
Subject Areas:
behaviour, cognition
Keywords:
zebrafish, numerical cognition, ontogeny,
quantity discrimination
Authors for correspondence:
Maria Elena Miletto-Petrazzini
e-mail: mariaelena.milettopetrazzini@gmail.
com
Caroline H. Brennan
e-mail: c.h.brennan@qmul.ac.uk
Characterizing ontogeny of quantity
discrimination in zebrafish
Eva Sheardown
1,3
, Jose Vicente Torres-Perez
2,3
, Sofia Anagianni
3
,
Scott E. Fraser
4
, Giorgio Vallortigara
5
, Brian Butterworth
6
,
Maria Elena Miletto-Petrazzini
3,7
and Caroline H. Brennan
3
1
Centre for Developmental Neurobiology, Institute of Psychiatry, Psychology and Neuroscience, Kings College
London, New Hunt’s House, Guy’s Campus, London SE1 1UL, UK
2
Departament de Biologia Cellular, Biologia Funcional i Antropologia física, Fac. de CC. Biològiques, Universitat
de València, C/ Dr. Moliner 50, 46100 Burjassot (València), Spain
3
School of Biological and Behavioural Sciences, Queen Mary University of London, Mile End Road, London,
E1 4NS, UK
4
Michelson Center for Convergent Bioscience, University of Southern California, Los Angeles, USA
5
Center for Mind/Brain Sciences, University of Trento, Rovereto, Italy
6
UCL Institute of Cognitive Neuroscience, 17 Queen Square, London WC1N 3AZ, UK
7
Department of General Psychology, University of Padova, 35131 Padova, Italy
ES, 0000-0002-1801-7025; JVT-P, 0000-0001-6390-9690; SA, 0000-0001-5784-582X;
SEF, 0000-0002-5377-0223; GV, 0000-0001-8192-9062; BB, 0000-0001-8201-3347;
MEM-P, 0000-0002-5204-5863; CHB, 0000-0002-4169-4083
A sense of non-symbolic numerical magnitudes is widespread in the animal
kingdom and has been documented in adult zebrafish. Here, we investi-
gated the ontogeny of this ability using a group size preference (GSP) task
in juvenile zebrafish. Fish showed GSP from 21 days post-fertilization and
reliably chose the larger group when presented with discriminations of
between 1 versus 3, 2 versus 5 and 2 versus 3 conspecifics but not 2
versus 4 conspecifics. When the ratio between the number of conspecifics
in each group was maintained at 1 : 2, fish could discriminate between 1
versus 2 individuals and 3 versus 6, but again, not when given a choice
between 2 versus 4 individuals. These findings are in agreement with studies
in other species, suggesting the systems involved in quantity representation
do not operate separately from other cognitive mechanisms. Rather they
suggest quantity processing in fishes may be the result of an interplay
between attentional, cognitive and memory-related mechanisms as in
humans and other animals. Our results emphasize the potential of the use
of zebrafish to explore the genetic and neural processes underlying the onto-
geny and function of number cognition.
1. Introduction
One aspect of quantity discrimination is the evaluation of the number of items
in a group, the numerosity. Although quantitative abilities of many species
have been studied [1–3], research into the ontogeny of the ability to assess
numerosity has been restricted so far to humans [4,5], fish (Poecilia reticulata)
and domestic chicks (Gallus gallus) [6,7]. Typically, in species other than
chicks, which are a precocial species, the ability to assess numerosity changes
with age until individuals reach adulthood. However, 1-day-old guppies
(P. reticulata) can distinguish between a small number of conspecifics in a
similar way to 40-day-old guppies [8].
Interestingly, guppies show no ratio effect for contrasts between numeros-
ities 1 to 4, but the familiar ratio effect, Weber’s Law, for larger numerosities
[9]. Similar findings have been observed in human infants [10–14] suggesting
the existence of conserved mechanisms of numerosity discrimination, though
little is known about either the neural or genetic bases of these abilities (for a
recent review see Lorenzi et al. [15]).
© 2022 The Author(s) Published by the Royal Society. All rights reserved.
... By expressing a nuclear-localized calcium indicator (H2B-jGCaMP7f) (Dana et al., 2019a), we were able to monitor brain-wide neuronal activity in response to non-symbolic, visual numerical stimuli. While no studies have shown any ability to discriminate different numerosities at an early age (<7 days post-fertilization (dpf)) in zebrafish, it must develop before the behavior becomes apparent (Adam et al., 2024;Lorenzi et al., 2023;Lucon-Xiccato et al., 2023;Sheardown et al., 2022a). Here, we aim to identify these number-neurons, across the brain, in real time as the animal processes a visual number stimulus, in an effort to improve our understanding of the neural basis of number sense. ...
... Consistent with studies using chick models (Kobylkov et al., 2022) and human infants (Izard et al., 2009;Xu & Spelke, 2000), we detected number-selective neurons during early post-embryonic (equivalent to post-natal) stages in zebrafish. Notably, the existence of these number-selective neurons at 3 dpf precedes any known numerically-driven behaviors such as hunting and shoaling (which start at 5 and~24 dpf, respectively) (Adam et al., 2024;Borla et al., 2002;Lucon-Xiccato et al., 2023;Sheardown et al., 2022a), underscoring the fundamental role and necessity of early numerical cognition for survival. ...
Neural Basis of Number Sense in Larval Zebrafish
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View
... The zebrafish is a widespread model in developmental biology and genetics and is one of the best available models for studying the ontogenetic development of numerical cognition [42]. Thanks to the development of neurobiological techniques and the evidence collected on the neural basis of number in this species (see Messina et al. (2022) [5]), our results may provide behavioral techniques useful for studying the neural circuitry underpinning proto-arithmetic abilities in zebrafish. ...
View
... Smaller ratios from 0.25 to 0.33 were quite easy for them to distinguish while ratios of 0.50 and higher were unequally harder or not possible to distinguish for these larvae (Fig. 5a). This coincides with the findings of Sheardown et al. (2022) that juvenile zebrafish at the age of 21-33 dpf reliably choose the larger group of different numerosities within ratios of 0.25 and 0.33 and that more difficult comparisons (ratio 0.67) are only feasible for older zebrafish starting from 27 dpf. Once this ability is reached, it seems to stay consistent over time since adult zebrafish have also been shown to be able to discriminate small numerosities with a ratio of up to 0.67, but failed to discriminate between numerosities with a ratio of 0.75 (Potrich et al. 2015). ...
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View
... The study with guppies showed an innate capacity to discriminate between social groups differing by one individual up to three vs four units (0.75 ratio), the same numerical acuity shown by adults tested in similar conditions (Bisazza et al. 2010). Zebrafish tested between age 21 and 33 dpf and showed an age effect in the most difficult comparison, two versus three (0.67 ratio), which was discriminated only by the oldest larvae (Sheardown et al. 2022). Although in this case, the cognitive ability under investigation (i.e. ...
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... This finding indicates that the ability of number sense in amphibians can be underestimated or misinterpreted. Plasticity in this aspect of number sense is already known in other taxa (e.g., in fish, Bisazza et al. 2010;Sheardown et al. 2022). When measuring the number competence of frogs and toads, it will be crucial to consider ontogeny and plasticity. ...
Grouping rule in tadpole: is quantity more or size assortment more important?
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  • Sep 2023
  • ANIM COGN
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View
... This nding indicates that numerical abilities in amphibians can be underestimated or misinterpreted. Plasticity in this aspect of number sense is already known in other taxa (e.g., in sh, Bisazza et al., 2010;Sheardown et al., 2022). When measuring the number competence of frogs and toads, it will be crucial to consider ontogeny and plasticity. ...
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Preprint
Full-text available
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View
... However, if the numerical information is excluded and the two stimuli differ only in their continuous property (cumulative area) guppies no longer discriminate between them (Miletto Petrazzini et al. 2014;Piffer et al. 2013). Findings of a recent study of young zebra fish (Danio rerio) are consistent with these results, at least in terms of number discrimination (Sheardown et al. 2022). In contrast with this, tadpoles of the two anuran species tested (Bufotes balearicus and Pelophylax esculentus) seem to have the capacity to discriminate between only small numbers (Balestrieri et al. 2019), suggesting that they rely more on the OFS, whereas fishes might operate on both. ...
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... In the aforementioned situations, pure numerical abilities provide reliable information for adaptive decisions. Therefore, it is not difficult to explain their presence in animals that are requested to perform such decisions, including adult and juvenile zebrafish 58,59 . What is puzzling, is the presence of numerical abilities in zebrafish at an early developmental stage when they seem to have reasonably no functional role. ...
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... However, we see evidence for the preference for the larger shoal both in the case of 4 versus 2 and 6 versus 3 dichotomous trials through trajectory density analysis, where the more dense regions were near the larger shoal. Previous studies on shoaling preference report that zebrafish can discriminate between shoal sizes of 6 versus 3 in dichotomous choices, although many studies indicate a failure to discriminate 4 versus 2 shoal sizes 39,51 .However, both those studies also use a different rectangular three-tank shoal choice set up from ours, and one 39 used a perforated divider through which shoaling decisions were based on olfactory and not just visual cues from the display fish. ...
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