Longitudinal fNIRS and EEG metrics of habituation and novelty detection are correlated in 1-18-month-old infants

Abstract

Introduction: Habituation and novelty detection are two fundamental and widely studied neurocognitive processes. Whilst neural responses to repetitive and novel sensory input have been well-documented across a range of neuroimaging modalities, it is not yet fully understood how well these different modalities are able to describe consistent neural response patterns. This is particularly true for infants and young children, as different assessment modalities might show differential sensitivity to underlying neural processes across age. Thus far, many neurodevelopmental studies are limited in either sample size, longitudinal scope or breadth of measures employed, impeding investigations of how well common developmental trends can be captured via different methods.

Method: This study assessed habituation and novelty detection in N = 204 infants using EEG and fNIRS measured in two separate paradigms, but within the same study visit, at 1, 5 and 18 months of age in an infant cohort in rural Gambia. EEG was acquired during an auditory oddball paradigm during which infants were presented with Frequent, Infrequent and Trial Unique sounds. In the fNIRS paradigm, infants were familiarised to a sentence of infant-directed speech, novelty detection was assessed via a change in speaker. Indices for habituation and novelty detection were extracted for both EEG and NIRS RESULTS: We found evidence for weak to medium positive correlations between responses on the fNIRS and the EEG paradigms for indices of both habituation and novelty detection at most age points. Habituation indices correlated across modalities at 1 month and 5 months but not 18 months of age, and novelty responses were significantly correlated at 5 months and 18 months, but not at 1 month. Infants who showed robust habituation responses also showed robust novelty responses across both assessment modalities.

Discussion: This study is the first to examine concurrent correlations across two neuroimaging modalities across several longitudinal age points. Examining habituation and novelty detection, we show that despite the use of two different testing modalities, stimuli and timescale, it is possible to extract common neural metrics across a wide age range in infants. We suggest that these positive correlations might be strongest at times of greatest developmental change.

Keywords: EEG; Habituation; Neurodevelopment; Novelty detection; fNIRS.

Fig. 1

Adapted from Katus et al., 2020. Schematic of stimulus presentation in EEG paradigm. Sounds of three categories were presented: Frequent sounds at a probability of 0.8, consisting of 500 Hz pure tones, Infrequent sounds, presented at 0.1 probability and consisting of short segments of white noise, and Trial Unique sounds, presented at 0.1 probability and consisting of a range of sounds (e.g., vocalisations, digitised syllables, pure tones). Sounds were presented for 100 ms with a 5 ms ramp up and down time, and an ISI of mean length 700 ms, jittered between 650 and 750 ms. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Schematic of stimulus presentation in fNIRS paradigm. Stimuli consisted of 8-second-long sentences of infant directed speech, presented for 25 trials. For the first 15 familiarisation trials (Trials 1–5 = Fam1_NIRS, Trials 6–10 = Fam2_NIRS, Trials 11–15 Fam3_NIRS), the sentence was spoken by a female speaker, followed by 5 trials spoken by a male speaker (Trials 16–20 – Novelty Trials). The final 5 trials were spoken by the same female speaker as for the Familiarisation trials (Post-test Trials). Between each trial, a 10 s silent baseline was presented. Image copyright: Ian Farrell (right hand side photo). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 3

fNIRS channel configuration at the 1-, 5- and 18-month age points. Highlighted are channels contributing to the ROI's at each point as identified by cluster permutation analyses. At the 1-month age point (top panel), a significant ROI based on the Fam1_NIRS trials was found over bilateral middle temporal regions (yellow). At the 5-month age point (middle panel), a significant ROI spanning middle to posterior temporal regions was found for the Fam1_NIRS trials (orange) and Novelty trials (light green). At the 18-month age point (bottom panel) ROI's were found over middle to posterior temporal regions for the Fam1_NIRS (red) and Novelty (dark green) trials. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 4

Rates of data exclusion / retention at the 1-, 5- and 18-month age point and reasons for exclusion. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 5

ERP responses at 1-month (a), 5-months (b) and 18-months (c) of age for Frequent (blue), Infrequent (red) and Trial Unique (yellow) sounds. Here, time courses of all infants contributing valid data for each cross-sectional age point are included. Figures including only infants contributing EEG data to all three age points (N = 74) can be found in Supplementary Figure 1. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 6

fNIRS time courses at 1 month (light orange), 5 months (orange) and 18 months (dark orange) across Fam1_NIRS (a), Fam2_NIRS (b), Fam3_NIRS (c), Novelty (d) and Post-test (e) epochs. Here, time courses of all infants contributing valid data for each cross-sectional age point are shown. Figures including only infants contributing fNIRS data to all three age points (N = 60) can be found in Supplementary Figure 2. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 7

Longitudinal EEG and fNIRS responses across repeated trials per age point. Here, only infants contributing data at all age points are included. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 8

Longitudinal Habituation (top row) and Novelty (bottom row) responses during the EEG (left) and fNIRS (right) paradigm across the 1-, 5- and 18-month age points. Here, only infants contributing data at all age points are included. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 9

Correlations between EEG (y-axis) and fNIRS (x-axis) habituation (top row) and novelty (bottom row) metric for the 1-, 5-, and 18-month age points. Each data point represents an individual participant's neural response on the EEG and fNIRS paradigm. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 10

Correlations between EEG (y-axis) and fNIRS (x-axis) novelty metric stratified by habituation responses for the 1-, 5-, and 18-month age points. Each data point represents an individual participant's neural response on the EEG and fNIRS paradigm. A larger number of infants who show a habituation response in either NIRS or EEG (yellow triangles) or both NIRS and EEG (green square) also show a novelty response in both NIRS and EEG (top right quadrant) at the 5 and the 18 month age points. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 11

Breakdown of infants showing novelty or habituation responses per modality (NIRS/EEG) and age point (1, 5, 18 months). As can be seen, the proportion of infants showing robust novelty and habituation responses in both NIRS and EEG increases with age. The proportion of infants who show a habituation or novelty response in only NIRS or EEG decreases with age, as does the proportion who shows no novelty or habituation response in either modality. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)