Radon is a naturally occurring gas that contributes significantly to radiation in the environment and is the second leading cause of lung cancer globally. Previous studies have shown that other environmental toxins have deleterious effects on brain development, though radon has not been studied as thoroughly in this context. This study examined the impact of home radon exposure on the neural oscillatory activity serving attention reorientation in youths. Fifty-six participants (ages 6–14 years) completed a classic Posner cuing task during magnetoencephalography (MEG), and home radon levels were measured for each participant. Time-frequency spectrograms indicated stronger theta (3–7 Hz, 300–800 ms), alpha (9–13 Hz, 400–900 ms), and beta responses (14–24 Hz, 400–900 ms) during the task relative to baseline. Source reconstruction of each significant oscillatory response was performed, and validity maps were computed by subtracting the task conditions (invalidly cued – validly cued). These validity maps were examined for associations with radon exposure, age, and their interaction in a linear regression design. Children with greater radon exposure showed aberrant oscillatory activity across distributed regions critical for attentional processing and attention reorientation (e.g., dorsolateral prefrontal cortex, and anterior cingulate cortex). Generally, youths with greater radon exposure exhibited a reverse neural validity effect in almost all regions and showed greater overall power relative to peers with lesser radon exposure.
1. Introduction
Attentional orienting and reorienting are imperative to daily functioning as we must be able to attend to important stimuli within our environment, and subsequently shift our attention elsewhere as competing stimuli emerge. This process must be quick and dynamic to serve efficient and complete processing of our surroundings. Attention develops rapidly throughout childhood and early adolescence, which is perhaps unsurprising given the notable development in neural substrates implicated in attentional processing (Abundis-Gutiérrez et al., 2014; Flores et al., 2010; Konrad et al., 2005). Using neurocognitive tasks involving valid and invalid cues that direct a participant correctly or incorrectly to the location of a target (i.e., the Posner paradigm and Attentional Network Task; Petersen and Posner, 2012; Posner, 1980; Fan et al. 2002), multiple neuroimaging studies have detected neural networks important for attentional reorientation. For example, research using fMRI has repeatedly implicated the superior parietal lobe, the temporoparietal junction, and the intraparietal sulcus in the process of attentional reorientation (Petersen and Posner, 2012; Posner, 2012; Vossel et al., 2006). Along with parietal activation, frontal cortices, including the frontal eye fields (FEF) as well as inferior and middle frontal gyri, have been shown to play a strong role in orienting and reorienting (Petersen and Posner, 2012; Posner, 2012; Vossel et al., 2006).
Similar findings have been demonstrated using magneto- and electroencephalographic (M/EEG) methods probing the temporally-sensitive dynamics (e.g., Gómez et al. 2008). For instance, in healthy adult populations, neural oscillatory activity related to attentional reorienting in the theta (4–8 Hz), alpha (8–14 Hz), and beta (14–24 Hz) bands has been detected in the superior parietal and intraparietal sulcus, along with the FEF, inferior frontal gyrus, and prefrontal cortices (Arif et al., 2020a; Proskovec et al., 2018a). Generally speaking, adult studies tend to show stronger increases in theta power (i.e., stronger oscillations) during attentional reorientation, and more dynamic conditional differences in alpha and beta power that vary by time and location (e.g., Proskovec et al. 2018). Among children and adolescents, recent work has identified that the neural dynamics underlying attentional reorientation are developmentally sensitive. Specifically, during reorienting, youths showed stronger theta activity across multiple areas of the right prefrontal cortex and stronger alpha/beta responses over the left motor cortex and right cuneus as a function of increasing age (Picci et al., 2023). These findings compliment a breadth of literature reporting age-related alterations in attention- and high order cognition-related neural dynamics (e.g., Killanin et al. 2020, Taylor et al. 2021, 2020), suggesting that these oscillatory responses are robustly sensitive to developmental processes during childhood and adolescence.
The maturational sensitivity of the functional brain dynamics serving attentional processing is of great importance when considering that youths are regularly exposed to a wide array of environmental toxins that could impact these developmental trajectories (Bearer, 1995; Perera et al., 2006). A growing literature evidences a myriad of negative outcomes in the neurodevelopment of children connected to various exposures, ranging from lead and other toxic metals (Sanders et al., 2015; Silver et al., 2016) to inhaled air pollutants (Chiu et al., 2016; Peterson et al., 2015). For instance, studies have demonstrated a relationship between increased exposure to a broad range of toxins and increased risk for anxiety and mood disorders (Bornschein et al. 2006), ADHD (Myhre et al., 2018), and learning and neurocognitive disorders (Sanders et al., 2015). Even low level toxin exposure has been related to impaired cognitive functioning and lowered intelligence in youth, including decreased attention and memory functioning (Chiu et al., 2016; Liu and Lewis, 2014; Perera et al., 2006; Sanders et al., 2015). Despite this growing body of research detailing the neurocognitive impacts of environmental toxins on the developing brain, the effects of some of the most common household toxins have not yet been characterized, most notably radon.
Radon is a ubiquitous gas that forms from the decay of naturally occurring uranium (Clement et al., 2010; Darby et al., 2005; Kang et al., 2019; Vogeltanz-Holm and Schwartz, 2018), and it can accumulate to hazardous levels in homes (Laquatra and Laquatra, 2018; Riudavets et al., 2022; Sethi et al., 2012; Vogeltanz-Holm and Schwartz, 2018). In fact, 1 in 15 homes in the United States is estimated to have radon levels exceeding the action limit recommended by the Environmental Protection Agency, which is an indoor concentration equal to or greater than 4.0 pCi/L (United States Environmental Protection Agency, 2016). Further, in the state of Nebraska, more than half of radon tests have results above 4.0 pCi/L (NDHHS, 2024). Despite the guidance from the EPA and Department of Health and Human Services, the public's knowledge of radon and its hazardous effects is severely lacking. Past research has linked radon exposure to multiple health concerns, including lung cancer (Sethi et al., 2012; Vogeltanz-Holm and Schwartz, 2018) and neurodegenerative diseases in adulthood (Gómez-Anca and Barros-Dios, 2020; Zhang et al., 2022). Further, recent work in children demonstrated robust links between home radon exposure and increases in specific biomarkers of inflammation (Taylor et al., 2022) that are regularly associated with detriments to neurocognitive development in youths (Ehrlich et al., 2021; Loftis et al., 2020; Miller et al., 2009). Despite such clear connections between radon exposure and health consequences ranging from chronic inflammation to cancer and neurodegenerative disease, few studies have investigated other deleterious effects that radon may have, including in the realm of neurocognitive development. Particularly lacking is research involving youths, despite children being highly vulnerable to the effects of toxic exposures, and thus potentially more vulnerable to the damaging effects of radon (Kendall et al., 2021).
In the present study, we investigated the impact of home radon exposure on the neural oscillatory dynamics serving attentional reorienting in typically developing children and adolescents. To measure the neural processing underlying attentional reorienting, youths completed a classic Posner paradigm during high-density MEG. Home radon test kits were used to measure indoor radon concentrations in the family home. We hypothesized that the effects of radon exposure would be most notable in the theta, alpha, and beta range given their known developmental sensitivity in this paradigm and other higher order cognitive tasks. We predicted that chronic home radon exposure would be related to aberrations in task performance and neural oscillations within attention networks, such that children with higher radon exposure would exhibit both behavioral and neural decrements in attentional reorienting. Further, given the known exceptional sensitivity of these developing networks to environmental toxins, we explored potential interactions between age and radon exposure to see whether radon may be modulating expected developmental trajectories of these neural dynamics.