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The Neural Correlates of Inhibitory Control in 10-Month-Old Infants: a Functional Near- Infrared Spectroscopy Study Abigail Fisk

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The Neural Correlates of Inhibitory Control in 10-Month-Old Infants: a Functional Near- Infrared Spectroscopy Study Abigail Fisk The neural correlates of inhibitory control in 10-month-old infants: a functional near- infrared spectroscopy study Abigail Fiske1*, Carina de Klerk2, Katie Y. K. Lui3, Liam Collins-Jones4, Alexandra Hendry1, Isobel Greenhalgh5, Anna Hall1, Gaia Scerif1, Henrik Dvergsdal6, Karla Holmboe1 1 Department of Experimental Psychology, University of Oxford, United Kingdom 2 Department of Psychology, University of Essex, United Kingdom 3 Department of Psychology, University of Bath, United Kingdom 4 Department of Medical Physics & Biomedical Engineering, University College London, United Kingdom 5 Child and Adolescent Mental Health Services, Oxford Health NHS Foundation Trust, Oxford, United Kingdom 6 Nord University Business School, Department of Entrepreneurship, Innovation and Organisation, Bodø, Norway *Corresponding author: Abigail Fiske, Department of Experimental Psychology, University of Oxford, United Kingdom. Email: [email protected] Acknowledgements We would like to acknowledge Alison Jordan for her role in recruiting participants and organising test sessions, and Robert Cooper for his contribution to the custom probe design and code development used in this study. We also thank Jun Yin for sharing analysis scripts. 1 We offer our gratitude to the families who have continued to support and contribute to this project. This research was funded by the UK Medical Research Council (MR/N008626/1, PI: Karla Holmboe) and by AF’s UK Medical Research Council Industrial Collaborative Awards in Science and Engineering (iCASE) studentship. The funder was not involved in the conceptualisation, design, data collection, analysis, decision to publish, or preparation of the manuscript. Author Contributions KH conceptualised the idea for the study and the original ECITT task design, and KH, CdK and HD designed the fNIRS version of the ECITT. AF, CdK and KH formulated the analysis plan. AF, CdK, GS and KH wrote the pre-registration relating to the individual differences analyses. KH, AF, AHa, IG, AHe and KL collected the data. AF and KL designed the video coding protocols and coded the videos. AF, KH and HD curated the data. AF and CdK processed and analysed the fNIRS data. AF, CdK and KH conducted the statistical analyses of the final data set. LCJ and AF visualised the data. HD programmed the ECITT software, and LCJ developed the pipeline to reconstruct the data and to plot/display the resulting reconstructed images. AF wrote the original draft. AF, KH, CdK, AHe, AHa, HD, and LCJ reviewed and edited the original draft. KH, CdK and GS supervised the study, and KH undertook the overall management and project administration of the larger project that this study was part of. KH acquired the funding for the study. 2 Abstract Inhibitory control, a core executive function, emerges in infancy and develops rapidly across childhood. Methodological limitations have meant that studies investigating the neural correlates underlying inhibitory control in infancy are rare. Employing functional near- infrared spectroscopy alongside a novel touchscreen task that measures response inhibition, this study aimed to uncover the neural underpinnings of inhibitory control in 10-month-old infants (N = 135). We found that when inhibition is required, the right prefrontal and parietal cortices were more activated than when there is no inhibitory demand. Further, activation in right prefrontal areas was associated with individual differences in response inhibition performance. This demonstrates that inhibitory control in infants as young as 10 months of age is supported by similar brain areas as in older children and adults. With this study we have lowered the age-boundary for localising the neural substrates of response inhibition to the first year of life. 3 The early years of life represent a fundamental period in the development of executive functions (EFs), a set of core cognitive skills that facilitate the control of attention and behaviour in order to meet an adaptive goal. Executive function components such as inhibitory control, working memory and cognitive flexibility develop slowly across infancy and toddlerhood before improving rapidly in early childhood (Berg et al., 2020; Friedman et al., 2011; Garon et al., 2008, 2014; Howard et al., 2017; Wiebe et al., 2012; for reviews see, Fiske & Holmboe, 2019 and Hendry et al., 2016). Accompanying these cognitive advances are important structural and functional maturation processes in the prefrontal cortex (PFC), a region of the brain consistently associated with EFs (Diamond, 2002; Fiske & Holmboe, 2019). Although there is some insight into the neural mechanisms involved in the development of working memory in infants and toddlers (Reyes et al., 2020; Wijeakumar et al., 2019), studies that identify the specific areas of the brain that are functionally associated with inhibitory control in infancy are rare. As such, knowledge about the neural substrates of EF across this period of infancy and early childhood is limited. From its emergence in infancy, inhibitory control is an essential EF that supports the deployment of cognitive control over goal irrelevant, non-adaptive behaviour (Friedman & Miyake, 2017; Miyake et al., 2000; Miyake & Friedman, 2012). One important form of inhibitory control is response inhibition; the ability to inhibit a prepotent or well-learned response which is often motoric in nature (Friedman & Miyake, 2004). Whilst response inhibition abilities are immature during infancy, it is possible to reliably measure early forms of response inhibition from the second half of the first year of life (Hendry et al., 2021; Holmboe et al., 2008, 2018, 2020). However, very little is known about the brain mechanisms supporting response inhibition in infancy and toddlerhood. The reason for this is twofold: a lack of age-appropriate tasks (Holmboe et al. 2020), and the difficulty in using neuroimaging techniques for measuring the awake infant brain in non-clinical settings (Lloyd-Fox et al., 4 2010). In studies with older children and adults, canonical tasks such as the Stop-Signal (Logan & Cowan, 1984) and the Go/No-Go task (e.g., Drewe, 1975) have frequently been used alongside functional magnetic resonance imaging (fMRI) to investigate the brain regions associated with response inhibition (Aron et al., 2007; Aron & Poldrack, 2006; Booth et al., 2003; Cope et al., 2020; Durston et al., 2002; Hampshire et al., 2010; Wager et al., 2005). These well-established experimental paradigms provide a reliable measure of the neural correlates of response inhibition for older children and adults, but are unsuitable for the assessment of response inhibition skills as they emerge in infancy. This is because many of these tasks contain high working memory and language comprehension demands (Holmboe et al., 2020) and neuroimaging modalities such as fMRI are not suitable for infants and young children. Whilst there have been efforts to adapt or simplify EF tasks for use with toddlers (Bernier et al., 2010; Garon et al., 2014; Mulder et al., 2014) and young children (Berg et al., 2020; Howard & Melhuish, 2017; Zelazo et al., 2013), there still exists a paucity of tasks that specifically assess response inhibition and the associated neural substrates in children under the age of two. Commendable efforts have been made in the EEG literature, whereby researchers have studied broad indices of neural activation (such as alpha power over frontal channels) to investigate inhibition-related brain activation in infancy. However, EEG has limited spatial resolution and, in contrast to gold-standard adult response inhibition paradigms, such as the Go/No-Go and Stop-signal tasks, these tasks are typically passive looking tasks that also place substantial demands on working memory (Bell & Fox, 1992; Cuevas et al., 2012; Whedon et al., 2020). The relatively recent addition of functional near-infrared spectroscopy (fNIRS) into the developmental researcher’s toolkit has made it possible to investigate neural activation in specific brain areas during the early stages of development (Fiske & Holmboe, 2019; Lloyd- 5 Fox et al., 2010; Wilcox & Biondi, 2015). fNIRS is a non-invasive, optical imaging technique that uses near-infrared light to measure the haemodynamic response; increases of oxygenated haemoglobin and decreases in deoxygenated haemoglobin concentrations in the cortex of the brain. Evidencing the feasibility and growing popularity of this technique in developmental research, growing numbers of studies are using fNIRS to investigate the neural correlates of EF in preschool and school-age children (Buss et al., 2014; Kerr-German & Buss, 2020; Monden et al., 2015; Moriguchi et al., 2018; Reyes et al., 2020; Wijeakumar et al., 2019; Yanaoka et al., 2020). Studies using fNIRS to investigate response inhibition in this age group have found increased right lateral PFC activation when inhibition was successful (Moriguchi and Shinohara, 2019), and that children and adults showed activation in the same areas (right PFC and parietal cortex) where inhibition was required, although children had a more immature response pattern (Mehnert et al., 2013). This evidence is consistent with existing fMRI and transcranial magnetic stimulation (TMS) research showing that regions of the PFC and parietal lobe are activated during tasks of inhibitory control in both adults and children (Bunge et al., 2002; Cope et al., 2020; Durston et al., 2002, 2006; Tamm et al., 2002; van Belle et al., 2014). Specifically, the right dorsolateral prefrontal
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