Young domestic chicks spontaneously represent the absence of objects

  1. Eszter Szabó
  2. Cinzia Chiandetti
  3. Ernő Téglás
  4. Elisabetta Versace
  5. Gergely Csibra
  6. Ágnes Melinda Kovács
  7. Giorgio Vallortigara

  • Curated by eLife

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    Evaluation Summary:

    The research detailed in this manuscript investigates whether young chicks represent the absence of objects. This work is important to multiple fields of inquiry such as ethology and neuroscience, and is the first time this ability has been studied spontaneously in such a population, as opposed to after many trials of experience. The data effectively support most of the conclusions, though a few elements need clarification, especially in regards to possible sex-dependent representations of absence.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

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Abstract

Absence is a notion that is usually captured by language-related concepts like zero or negation. Whether nonlinguistic creatures encode similar thoughts is an open question, as everyday behavior marked by absence (of food, of social partners) can be explained solely by expecting presence somewhere else. We investigated 8-day-old chicks’ looking behavior in response to events violating expectations about the presence or absence of an object. We found different behavioral responses to violations of presence and absence, suggesting distinct underlying mechanisms. Importantly, chicks displayed an avian signature of novelty detection to violations of absence, namely a sex-dependent left-eye-bias. Follow-up experiments excluded accounts that would explain this bias by perceptual mismatch or by representing the object at different locations. These results suggest that the ability to spontaneously form representations about the absence of objects likely belongs to the initial cognitive repertoire of vertebrate species.

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  1. Version published to 10.7554/elife.67208 on eLife
  2. eLife

    Evaluation Summary:

    The research detailed in this manuscript investigates whether young chicks represent the absence of objects. This work is important to multiple fields of inquiry such as ethology and neuroscience, and is the first time this ability has been studied spontaneously in such a population, as opposed to after many trials of experience. The data effectively support most of the conclusions, though a few elements need clarification, especially in regards to possible sex-dependent representations of absence.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

  3. eLife

    Reviewer #1 (Public Review):

    This study is addressing a very important topic in animal cognition, namely how concepts like zero or negation can emerge in non-linguistic animals. We know that animals can represent objects when they are no longer available to their sight. But the question is whether they can represent the absence of an object. While previous research show that some species of mammals and birds can maintain object in mind even when they are occasionally occluded, there is no clear evidence that they represent absence when objects are expected to be not present at a specific location.
    Children are capable to express linguistically the absence of an object as a negation and they do so in a numerical context. These capacities emerge developmentally and seem to be linked to other faculties which rely on an approximate number system. In cognitive sciences, there are ample debates about how we represent number concepts and how we are sensitive to numerical differences, including empty sets, which may correspond to the concept of 'zero' (i.e. lack of numerosities).

    Is there any equivalent within a non-linguistic domain? This question is scientifically extremely stimulating and challenging. Neurophysiological experiments in monkeys show that there are neurons coding the presence or absence of a stimulus. Other behavioral studies also provide some evidence pointing to the possibility that some animals represent absence or understand the concept of 'zero'. However, more robust experimental evidence is still needed.

    Thus, the current study approaches this conundrum by exploiting an animal model (the chick imprinted on an object) that in the last few years has become extremely relevant to address outstanding questions related to the evolutionary origins of cognitive capacities in animals.

    Within this framework, a simple and straight forward methodology (looking behavior in a violation paradigm) has been applied in a series of experiments, which have elegantly circumvented such conceptual problem.

    Authors investigated in chicks their capacity to represent the absence of an object by assessing their looking behavior in violating expectation paradigms where experimenters manipulated the presence or absence of objects during three different phases. In a key condition, in the first phase no object was present in the arena. Then a screen was lifted to occlude the chick's view and an object was secretly introduced behind the screen. The sliding screen was then removed and it appeared in chick's view, thus violating its expectancy of absence.

    The results show sex differences in the ability of chick to represent the absence of an object with a left-eye bias. Authors interpret left-eye bias as an attempt to identify object at a location where 'nothing' was expected to be.

    Present findings are indeed an original contribution to the field even though some of the results are somehow difficult to interpret. For example, males do not show any effect. According to one hypothesis females would be more interested to social stimuli. However, previous studies show females' left-eye bias for novel object and right-eye bias for conspecifics. Thus, if the left-eye bias is a signature of an attempt to identify a social stimulus one should have expected to find right-eye bias for the object stimulus presented in these experiments. The interpretation of present findings therefore seems not always in line with the literature.

    One way to clarify this would be that of exposing chicks to different categories of imprinting stimuli (e.g. social vs non-social). This critical experiment would help in understanding if the females' stronger capacity to encode absence than males is due to their higher sensitivity to social stimuli.

    From an evolutionary perspective, if females' left-eye bias is a chicks' signature to identify the unexpectedly appearing object, given its survival importance, such early competence should be present in males' chicks too.

  4. eLife

    Reviewer #2 (Public Review):

    The research detailed in this manuscript investigates whether young chicks represent the absence of objects. This is the first time this ability has been studied spontaneously in such a population, as opposed to after many trials of experience. It may also be the first experiment to measure chicks' looking time in violation of expectation paradigms.

    The overall idea that chicks may represent absence and that the eye side looking bias (e.g., Lateralization Index) might be sensitive to violations of expectation regarding the absence of objects, but not regarding the presence of objects, is very interesting. Study 2 is particularly impressive in its controls.

    Some additional background material and details about methodology/analyses would better enable the reader to evaluate whether the data support all conclusions, especially those regarding sex-dependent representation of absence. In particular:

    1. Previous research with rooks in this domain is mentioned briefly in one sentence near the end of the Introduction. It would be helpful to know that, if this or similar research has already been conducted with another bird species, how the current research in chicks further significantly advances knowledge.

    2. More background review on eye usage with respect to novelty would be useful to the reader in the Introduction: e.g., the theory behind why this occurs, whether it is specific to birds, etc.

    3. It would be important to know why 8-day-old chicks were the age chosen to use in these particular experiments.

    4. It is unclear why sex was a factor in the ANOVAs-statements of plans or predictions in this regard would be helpful. This is especially true since so much of the Discussion unexpectedly focuses on findings related to such analyses.

    5. In Study 2, there are no untransformed mean looking time results given in the text, as there were for Study 1. To evaluate whether conclusions are supported by the data, these data would be helpful to include.

    With the clarifications summarized above, this could contribute substantial new knowledge to the fields of ethology, cognitive psychology, and neuroscience.

  5. eLife

    Reviewer #3 (Public Review):

    Szabó et al tested the representation of absence of objects in 8-day-old chicks, using a violation of expectation paradigms, in an elegant series of four experiments. The Authors designed a new paradigm to assess this fresh topic, obtaining data that support their conclusions. A deeper integration of this evidence with the previous literature on object permanence and numerical comprehension would help in understanding even better the relevance of these findings. In general, the study was conducted at high standards and I did not detect any objective errors in the paper.

  6. Version published to 10.1101/2021.01.20.427266v1 on bioRxiv