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Typical Crossmodal Numerosity Perception in Preterm Newborns

In: Multisensory Research
Authors:
Giovanni Anobile Department of Neuroscience, Psychology, Pharmacology and Child Health, University of Florence, 50135 Florence, Italy

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Maria C. Morrone Department of Translational Research on New Technologies in Medicine and Surgery, University of Pisa, 56123 Pisa, Italy

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Daniela Ricci National Centre of Services and Research for Prevention of Blindness and Rehabilitation of Visually Impaired, Rome, Italy
Department of Pediatrics, Catholic University of the Sacred Heart, Rome, Italy

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Francesca Gallini Department of Pediatrics, Catholic University of the Sacred Heart, Rome, Italy

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Ilaria Merusi Division of Pediatrics, Versilia Hospital, Italy

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Francesca Tinelli Department of Developmental Neuroscience, IRCCS Fondazione Stella Maris, 56128 Calambrone, Pisa, Italy

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Open Access

Abstract

Premature birth is associated with a high risk of damage in the parietal cortex, a key area for numerical and non-numerical magnitude perception and mathematical reasoning. Children born preterm have higher rates of learning difficulties for school mathematics. In this study, we investigated how preterm newborns (born at 28–34 weeks of gestation age) and full-term newborns respond to visual numerosity after habituation to auditory stimuli of different numerosities. The results show that the two groups have a similar preferential looking response to visual numerosity, both preferring the incongruent set after crossmodal habituation. These results suggest that the numerosity system is resistant to prematurity.

1. Introduction

According to the World Health Organization (World Health Organization, 2018), every year around 15 million babies are born preterm (i.e., <37 weeks of gestation age), with 1 million dying due to complications of preterm birth and many survivors developing lifetime difficulties. Prematurity in general, and extreme prematurity in particular (<32 weeks of gestation), is a well-known high-risk factor for atypical neurological development, especially for injuries within parietal areas (Isaacs et al., 2001; Padilla et al., 2015; Volpe, 2009).

Premature children often show poor performance in a variety of parietal-mediated abilities such as the visual perception of motion (Braddick et al., 2003; Guzzetta et al., 2009; MacKay et al., 2005; Taylor et al., 2009a), the perception of intervals duration (Tinelli et al., 2015), the ability to deploy visual-spatial attention (Anderson et al., 2011; Guzzetta et al., 2006; Kooiker et al., 2019; Tinelli et al., 2015; van de Weijer-Bergsma et al., 2008), amongst other abilities (for a review see Atkinson and Braddick, 2007). Beyond the perceptual deficits, prematurity is also a risk factor for academic difficulties, particularly in mathematics (Aarnoudse-Moens et al., 2009, 2011; Isaacs et al., 2001; Taylor et al., 2009b; Twilhaar et al., 2018).

In the last few years there has been increasing scientific interest in the neurocognitive foundations of numerical cognition. It has been suggested that a prerequisite for a typical development of math abilities is a well-functioning preverbal system to perceive numerosity (Butterworth, 2018; Butterworth et al., 2011; Halberda et al., 2008; Piazza, 2010; Price et al., 2007). Numerosity perception refers to the ability to estimate, quickly but roughly, the numerical quantity of objects or events, accomplished without serial counting (Dehaene, 2011). Importantly, performance on numerosity tasks often correlates with math abilities (Halberda et al., 2008; Starr et al., 2013), strongly engages parietal areas (Butterworth and Walsh, 2011; Castelli et al., 2006; Holloway and Ansari, 2010; Nieder and Dehaene, 2009) and is often impaired in people with developmental dyscalculia (Anobile et al., 2018a; Butterworth, 2018; Cicchini et al., 2019; Mazzocco et al., 2011; Piazza et al., 2010).

Numerosity covaries with many nonnumerical magnitudes and stimulus properties (Bueti and Walsh, 2009) like texture, size and density. In addition, numerosity and magnitude estimation tasks are very difficult to distinguish by manipulation of the number of items (Dakin et al., 2011; Gebuis and Reynvoet, 2012; Gebuis et al., 2016). Building on this and other evidence, a recent influential work suggests that the nature of the “number sense” should be reconsidered since it should be better interpreted as a ‘magnitude sense’ (Leibovich et al., 2017). This issue is still largely debated, particularly in studies involving newborns, where experiments cannot scan many stimulus parameters and need to be limited by the short allocation time of the attentive and cognitive resources (de Hevia et al., 2017; Leibovich et al., 2017).

Also, the link between numerosity perception and the development of symbolic arithmetical skills is far from clear, with some evidence pointing to no numerosity deficit in dyscalculia (De Smedt and Gilmore, 2011; Landerl and Kölle, 2009; Rousselle and Noël, 2007; Szucs et al., 2013), null or weak correlations among neurotypicals participants (Chen and Li, 2014; Schneider et al., 2017) and no clear causal link between the two performances. Recent evidence converges to suggest that numerosity and symbolic numbers should be considered as independent constructs (Núñez, 2017). The developmental stage could also be crucial in modulating the link between numerosity perception and symbolic numeracy. While during early developmental stages non-symbolic quantities and numbers may be more strongly linked, probably mapping on to each other, in adults this mapping might become weaker or annulled (Anobile et al., 2018b; Lyons et al., 2012).

As with the perception of numerosity, many non-numerical continuous features like quantities and symbolic arithmetical tasks largely involves parietal areas (Bueti and Walsh, 2009; Castaldi et al., 2019; Harvey and Dumoulin, 2017; Harvey et al., 2013, 2015; Piazza and Eger, 2016) that mature slowly with age, making it interesting to measure the functionality of the system underlying magnitude perception in newborns. In this work we compared typical term newborns with preterm newborns, a population at high risk for deficits in the key brain areas subtending this function and characterized by a relatively high rate of arithmetic learning difficulties. Investigating numerosity representation in preterm babies, particularly at the earliest stage of life, could provide indirect information about the early functionality of brain areas involved in mathematical learning, opening up the possibility of developing targeted and effective intervention strategies.

To this aim, we adapted a crossmodal behavioural test developed by Izard and colleagues (Coubart et al., 2014; Izard et al., 2009). In their study, full-term newborns (0–4 days) were stimulated with sound sequences containing a fixed number of syllables (sound containing repetition of 12 or four syllables). Newborns were then sequentially presented with visuo-spatial arrays containing 12 or four images, while the sound sequences still played in the background. In this respect the paradigm is different from the classical habituation design, where the habituation stimulus is not presented in overlap with the test stimulus. With this paradigm the authors consistently observed that newborns looked longer when the visual arrays matched the auditory stimulation in numerosity, suggesting that human newborns are equipped with the ability to recognize numerical differences between senses and stimuli formats (sequential–auditory/spatial–visual).

This technique is simple and well suited for use with preterm newborns to assess whether numerosity perception is impaired at birth. In addition, given its multisensory nature it is also informative on the role of prematurity on the ability to combine information across senses (vision and audition in this case).

2. Material and Methods

2.1. Methods

Newborns were recruited directly inside the maternity ward, with the authorization of the director of the maternity department at Neonatal Unit, Catholic University in Rome and at Pediatrics and Neonatology Division, Versilia Hospital in Viareggio. The research was approved by the Institutional Review Board of Stella Maris Scientific Institute in Pisa and informed consent was obtained from parents before testing.

2.2. Power Analyses

Sample size was calculated with a-priori Power analyses using G*Power software (version 3.1; Faul et al., 2007). As the main goal of the current experiment was to detect a numerosity habituation effect in full-term and preterm newborns, the Power analyses aimed to calculate the required sample size of each group to reliably detect a difference between two dependent means (one-tailed paired t-test). The means here refers to the average looking time at the congruent and the incongruent visual stimuli. The effect size was estimated from Izard et al. (2009) taking the parameters from the same experimental condition used in the current study: the looking time at four versus 12 elements (d = 1.12). With an α = 0.05 and a Power of 0.8, the analyses revealed a required sample size of seven (lower than that recruited here, 12 for each group, see below).

2.3. Participants

Thirty-nine babies (20 preterm and 19 full-term newborns) were recruited, but 15 of them (eight preterm and seven full-term) were not able to conclude the task (mainly because they fell asleep or cried). The final sample (Table 1) was composed of 12 preterm (seven females; gestational age range: 28+6–34 weeks; range of weight: 1190–2100 g) and 12 newborns born at term (gestational age range: 38+5–41+6 weeks; range of weight: 2740–4110 g, see Table 1). Six preterm babies were tested at around 35 weeks of gestational age (range 34+5–35+2) after exposure to external environment of only a few days (range: 8–19 days; mean: 15 days); six other preterm babies were tested at equivalent term age (range: 38–40+3) after exposure to external environment of a longer period (range: 59–78 days; mean: 65 days). Full-term newborns were tested within three days after birth.

Table 1.
Table 1.

Sample demographical characteristics

Citation: Multisensory Research 34, 7 (2021) ; 10.1163/22134808-bja10051

Inclusion criteria were absence of auditory disorders (we enrolled only neonates with a response of ‘pass bilateral’ to auditory screening) and absence of visual disorders due to retinopathy of prematurity (ROP) more than stage II (in our sample only one subject had a ROP II).

More details about Apgar indexes at 5’, presence or not of breathing distress, ultrasounds and complications at birth are reported in Table 2.

Table 2.
Table 2.

Sample clinical characteristics

Citation: Multisensory Research 34, 7 (2021) ; 10.1163/22134808-bja10051

2.4. Task and Procedures

Participants were tested in the hospital where they were born. The newborns were seated in an infant seat, ≈60 cm from a 22-inch monitor, and their gaze and overall orientation were continuously recorded by a high-sensitivity camera positioned over the visual display. The task was a modified version of that used by Izard et al. (2009) and is depicted in Fig. 1. Each infant was stimulated with an auditory stream consisting of sequences of syllables (one minute), each repeated four or twelve times (played by speakers located below the screen). During this phase, the screen was black. After this phase (one minute), the newborns were presented with two consecutive test images (while the auditory stimulus continued to play), one congruent in numerosity and the other incongruent for a maximum of two minutes or until the infant diverted their gaze from the stimulus for 2 s (first block hereafter). After this phase, the screen turned black again and a second habituation phase started (second block). This second auditory habituation contained the opposite numerosity relative to the first habituation phase (twelve if the first contained four and vice versa) and lasted 30 s instead of one minute (Fig. 1). This second habituation was again followed by two test trials, one congruent and one incongruent (random order across trials). Table 3 show the four habituation test conditions and the overall number of tests for each group. The conditions were balanced across participants except for a small imbalance between C2 and C3, reflecting the imbalance between groups of the infants that did not complete the test (eight preterm and seven full-term infants). The images stayed on the screen until the infant looked away for 2 s, or after 60 s of looking. We used a shorter habituation time in the second block given that the attentional allocation of preterms is very short and a longer exposition would decrease the possibility of acquiring the visual looking time. With this shorter duration we were able to record the second block data in all except one preterm infant.

Figure 1.
Figure 1.

Illustration of the procedure. Along the entire experiment, infants were stimulated with auditory sequences containing a fixed number of sounds (4 or 12 syllables). In the first one minute of auditory stimulation the screen remained black, then two consecutive images were displayed containing the same or a different number of items (4 or 12 in a random order). Then a second block of trials started, with the auditory sequences containing the opposite number of sounds compared to the first block and with the habituation lasting 30 s instead of one minute.

Citation: Multisensory Research 34, 7 (2021) ; 10.1163/22134808-bja10051

Table 3.
Table 3.

Condition order and sample size

Citation: Multisensory Research 34, 7 (2021) ; 10.1163/22134808-bja10051

Looking times were recorded online by a trained observer observing the child from about 60 cm behind the screen and hidden by a black cloth with an eye slit. This online score was to detect the time that the baby looked at the screen. To this aim, the operator kept the space-bar pressed until the infant looked away for 2 s; release of the button automatically triggered the disappearance of the current stimulus and the appearance of the new visual stimulus (or the beginning of the second habituation phase). An additional scoring of slow-motion videos was performed offline by the same experimenter and another observer also blind to experimental conditions. Since the duration of the visual stimuli was determined by the operator recording online, the purpose of this se