Neurophysiology Of Sustained Attention in Early Infancy: Investigating Longitudinal Relations With Recognition Memory Outcomes Part 1
Aug 25, 2023
Abstract
The ability to sustain attention is a critical cognitive domain that emerges in infancy and is predictive of a multitude of cognitive processes. Here, we used a heart rate (HR) defined measure of sustained attention to assess corresponding changes in frontal electroencephalography (EEG) power at 3 months of age. Second, we examined how the neural underpinnings of HR-defined sustained attention were associated with sustained attention engagement.
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Third, we evaluated if neural or behavioral sustained attention measures at 3 months predicted subsequent recognition memory scores at 9 months of age. Seventy-five infants were included at 3 months of age and provided usable attention and EEG data and 25 infants returned to the lab at 9 months and provided usable recognition memory data.
The current study focuses on oscillatory power in the theta (4–6 Hz) frequency band during phases of HR-defined sustained attention and inattention phases. Results revealed that theta power was significantly higher during phases of sustained attention. Second, higher theta power during sustained attention was positively associated with the proportion of time in sustained attention.
Third, longitudinal analyses indicated a significant positive association between theta power during sustained attention on 9-month visual paired comparison scores such that higher theta power predicted higher visual paired comparison scores at 9 months. These results highlight the interrelation of the attention and arousal systems which have longitudinal implications for subsequent recognition memory processes.
Keywords
Infant Attention; EEG; Development; Recognition Memory.
1. Introduction
The ability to sustain attention is a critical cognitive domain that emerges in infancy and is
predictive of a multitude of cognitive outcomes across child development (Brandes-Aitken et
al., 2019; Johansson et al., 2015, Pérez-Edgar et al., 2010). The majority of existing research
looking at predictors and longitudinal associations of infant sustained attention has relied
on behavioral methodology.
However, the use of psychophysiology and neuroimaging may increase our ability to predict individual differences in cognitive outcomes, longitudinally (Farah, 2018). This article has three research questions.
First, does a heart rate (HR) defined measure of sustained attention correspond to changes in neural oscillations at 3 months of age? Second, how do neural measures of sustained attention correlate with engagement in HR-defined sustained attention? Third, do individual differences in sustained attention and neurophysiology at 3 months predict recognition memory outcomes at 9 months of age?
Attention is a multidimensional cognitive domain, composed of both exogenous (reflexive) and endogenous (non-reflexive) cognitive mechanisms. Sustained attention is a critical manifestation of endogenous attention referring to the ability to focus attention on a given stimulus for a prolonged period in the presence of distractors.
Sustained attention shares considerable neurobiological substrates with the general physiological arousal system (Richards, 2011). In general, the autonomic nervous system (ANS) is known to modulate fronto-cortical brain regions that support sustained attention processes (Arnsten, 1998, 2009; Arnsten & Li, 2005). This relation is cortically-mediated via connectivity between the brainstem, thalamus, and cholinergic inputs with the frontal cortex (Reynolds et al., 2013, Reynolds et al., 2013; Sarter et al., 2001).
Thus, activation of the ANS triggers downstream effects on an infant’s state of arousal which can lead to optimal or suboptimal ranges for attention and deeper processing to occur.
The interplay of arousal and attentional systems is reflected in distinct and measurable phases of attention (Reynolds & Romano, 2016; Richards, 2011). In particular, a reliable psychophysiological method for measuring sustained attention is characterizing heart-rate decelerations (Richards and Casey, 1991). Richards (1989) found that during periods of heart rate deceleration, 2-month-old infants take twice as long to shift their visual attention away from a central stimulus to a peripheral stimulus, indicating increased focus and decreased distractibility.
Integrating observable measures with physiological ones provides a more objective window into periods of active engagement (i.e., versus only measuring looking behavior, which may not reflect engagement) and an added level of specificity about the type of attention that is being indexed. This close relation between heart rate and looking behaviors further emphasizes the physiological underpinnings of sustained attention development. By 3 months of age, associations between HR deceleration and sustained attention become evident, as infants’ anterior attention system and cardiac regulation systems begin to mature and co-modulate with one another (Reynolds & Richards, 2008).
At 3 months of age, periods of sustained attention are more likely driven by maturing alerting systems (i.e., arousal) than executive systems (i.e., task-driven, top-down, and volitional), because executive skills do not emerge before the end of the first year (Colombo, 2002; Ruff & Rothbart, 2001). Looking at cortical mechanisms in conjunction with ANS mechanisms supporting arousal-attention associations may elucidate information not otherwise evident from measuring behavior alone early in infancy.
Electroencephalography (EEG) is a popular neuroimaging method for characterizing direct neural activity underlying cognitive processes particularly within infancy. EEG measures neural synchronization by indexing oscillatory power in distinct frequency bands that are linked with specific cognitive processes.
With regards to sustained attention, theta synchronization (4–7 Hz; Orekhova et al., 1999), and alpha desynchronization (6–9 Hz; Ward, 2003) are most commonly examined. Xie and Richards (2017) examined relations between infant-sustained attention, indexed through HR deceleration, and EEG oscillations. Using a cross-sectional sample of infants at ages 6, 8, 10, and 12 months, the authors found that 10- and 12-month-old infants’ demonstrated theta synchronization and alpha desynchronization during sustained attention episodes relative to inattention episodes.
These findings built off of past work from Richards and Reynolds linking heart-rate-defined sustained attention with event-related EEG components (Reynolds, Courage, & Richards, 2011; Richards, 2003). This is an important study because it was the first to demonstrate developmental differences in neural oscillatory power associated with heart-rate-defined phases of sustained attention.
Further research is needed to connect the brain to observable attention behavior.
Characterizing the biological basis of sustained attention early in life is critical as infant attention is found to be predictive of a range of cognitive outcomes (Brandes-Aitken et al., 2019, 2020; Johansson et al., 2015). The development of attention is one of the most central and pervasive processes active during infancy (Brandes-Aitken et al., 2019; Diamond, 2009).
Attention cascades across development into a multitude of more complex developmental domains including executive functions (Johansson et al., 2015), emotion regulation (Brandes-Aitken et al., 2021; Pérez-Edgar et al., 2010), memory, language, and social communication (Mundy & Jarrold, 2010; Salley et al., 2016). Existing studies looking at the hierarchical nature of sustained attention have studied behavioral measures of observed sustained attention starting around 10 months (Frick et al., 2018; Johansson et al., 2015; Johansson et al., 2016).
However, the neural architecture supporting emerging sustained attention in the first few months of life infancy may set the foundation for higher-order cognitive abilities longitudinally.
1.1. The current study
In the current study, we investigated patterns of HR-defined sustained attention and neural activity at 3 months of age and longitudinal associations with subsequent recognition memory abilities at 9 months of age. The current study has three research questions:
1. Do HR-defined measures of sustained attention characterize differentiated neural oscillations at 3 months of age? We hypothesized that neural activity would be higher during phases of HR-defined sustained attention.
2. Do HR-defined neural oscillations correspond with engagement in HR-defined sustained attention? We hypothesized that neural activity would be associated with greater sustained attention engagement.
3. Do HR-defined measures of sustained attention and corresponding neural activity at 3 months predict longitudinal recognition memory outcomes at 9 months of age? We hypothesized that greater neural activity during HR-defined sustained attention at 3 months would be associated with higher recognition memory scores at 9 months.
2. Methods
2.1. Participants
The initial sample included 100 infants (63 males; age M = 3.46 months, SD = 0.38) recruited from community events, family services, health care providers, and flyers posted at local businesses around New York City. The final sample only included infants who provided usable EEG data (N = 75; See protocol for attrition-related data). Participants were excluded from participating in the present study based on birth before 36 weeks gestation, multiple births, or the presence of developmental disorders.
Families were invited to participate in the study when infants were 3 months of age. See Table 1 for participant demographics on the analytic sample. The present study was conducted according to guidelines laid down in the Declaration of Helsinki, with written informed consent obtained from a parent or guardian for each child before any assessment or data collection. All research procedures were approved by the [MASKED FOR BLINDING] IRB.
2.2. Protocol
Infants and their caregivers visited the lab at 3 (Age M = 3.48, SD = 0.39) and 9 months (Age M = 9.48, SD = 0.53). At the 3-month time point infant EEG and ECG were recorded during an attention task and at rest, and responses to socio-demographic questionnaires were collected. At the 9-month time point, a visual recognition memory task was administered, and infant-looking data was recorded.
Out of the initial sample (N = 100), 7 infants did not provide EEG data due to behavioral issues, 8 EEG files were lost due to data acquisition technical problems, 7 EEG files were unusable due to excessive artifacts, and 3 did not provide sufficient sustained attention EEG data (See Section 2.3.4). Thus, the analytic sample included 75 infants at 3 months.
At the 9-month time point, a subset of 25 infants returned to the lab and provided usable recognition memory data. Attrition in the study sample is primarily attributed to the onset of the COVID-19 pandemic. Testing for the current study began in March 2018 and was halted in March 2020. To assess for attrition-related bias, we ran t-tests to assess for differences in covariates between each time point. The 3-month infant sample that returned at 9 months did not significantly differ from the 3-month sample that did not return in terms of income-to-needs, maternal education, or EEG power (t≤1.1, p≥.23).
2.3. Materials and measures
2.3.1. Family and household characteristics
Families were given questionnaires to obtain demographic information including maternal and infant age, race, and ethnicity. Caregivers also reported on their highest level of education attained and annual household income. The family income-to-needs ratio (ITN) is the total household income divided by the federal poverty line for the corresponding number of adults and children in the home and is used as the measure of socioeconomic status within the analyses.
2.3.2. HR-defined sustained attention measure
This study uses the same stimuli and procedure as Xie et al. (2017) to measure sustained attention. Participants sat on their caregivers’ laps while they were presented with a dynamic Sesame Street video on a large computer monitor. A camera in front of the infant recorded the infant’s face, while a camera behind the participants recorded the stimulus. The 4-minute video consisted of several characters from Sesame Street, such as ‘Elmo’ and ‘Big Bird,’ that moved from side to side, disappeared, sang, and danced.
These videos have been repeatedly demonstrated to elicit periods of sustained attention in young infants (Xie et al., 2017). Visual attention to stimuli was manually coded retroactively with the Net Station 5.1 software. Heart rate data was edited and processed using the software QRSTool to remove artifacts and identify heartbeats. The inter-beat intervals (IBIs, or the time in milliseconds between heartbeats) were used to evaluate heart rates with longer IBIs indicating slower heart rates, and vice versa.
Periods of infant sustained attention were categorized based on infant looking and heart rate deceleration. The criteria for categorizing periods of infant sustained attention required infant visual fixation to the stimulus paired with decreased heart rate (Richards, 2011). Specifically, HR-defined sustained attention phases began when the infant was looking at the screen and the median of five consecutive IBI values was lower than the median of the five IBIs preceding a look onset.
HR-defined sustained attention phases ended (and inattention phases began) when the median of five consecutive IBI values was higher than the median of the five IBIs preceding a look onset. All phases of attention occur during looks at the experimental stimuli. To characterize sustained attention engagement, we calculated the proportion of time in HR-defined sustained attention phases (seconds in sustained attention/total seconds of visual looking (Tonnsen et al., 2018; Xie & Richards, 2016). We also calculate look-defined sustained attention and inattention phases (based on the infant looking or not looking at the computer stimuli) to evaluate the value added by incorporating HR deceleration into our characterization of sustained attention.
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