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Article history: Despite the fact that attention undergoes protracted development, little is known about
Received 4 November 2023 how it may support memory refinements in childhood and adolescence. Here, we asked
Reviewed 15 February 2024 whether people differentially focus their attention on semantic or perceptual information
Revised 25 February 2024 over development during memory retrieval. First, we trained a multivoxel classifier to
Accepted 16 April 2024 characterize whole-brain neural patterns reflecting semantic versus perceptual attention
Action editor Gui Xue in a cued attention task. We then used this classifier to quantify how attention varied in a
Published online 8 May 2024 separate dataset in which children, adolescents, and adults retrieved autobiographical,
semantic, and episodic memories. All age groups demonstrated a semantic attentional bias
Keywords: during memory retrieval, with significant age differences in this bias during the semantic
Semantic knowledge task. Trials began with a preparatory picture cue followed by a retrieval question, which
Memory cues allowed us to ask whether attentional biases varied by trial period. Adults showed a se-
Autobiographical memory mantic bias earlier during the picture cues, whereas adolescents showed this bias during
Children the question. Adults and adolescents also engaged different brain regionsdsuperior pari-
Parietal cortex etal cortex and ventral visual regions, respectivelydduring preparatory picture cues. Our
results demonstrate that retrieval-related attention undergoes refinement beyond child-
hood. These findings suggest that alongside expanding semantic knowledge, attention-
related changes may support the maturation of factual knowledge retrieval.
© 2024 The Authors. Published by Elsevier Ltd. This is an open access article under the CC
BY-NC license (http://creativecommons.org/licenses/by-nc/4.0/).
* Corresponding author. 100 Saint George Street, Room 4020, Toronto, ON, M5S 3G3, Canada.
E-mail address: [email protected] (M.L. Schlichting).
https://doi.org/10.1016/j.cortex.2024.04.012
0010-9452/© 2024 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC license (http://
creativecommons.org/licenses/by-nc/4.0/).
78 c o r t e x 1 7 6 ( 2 0 2 4 ) 7 7 e9 3
mechanisms in the brain contribute to this improvement, ability to guide one's attention in a top-down manner. With
relatively less is known about the role of attention in the respect to the former, past work suggests that children may
emergence of adult-like memory retrieval. Here, we set out to spontaneously focus on the perceptual aspects of experience
characterize age-related differences in how particular atten- (Badger & Shapiro, 2012; Gentner & Toupin, 1986; Sloutsky
tional states are deployed as children, adolescents, and adults et al., 2007; Vendetti et al., 2015): For example, young chil-
retrieve memories. dren are more likely to make memory errors according to how
One type of attentional state with clear mnemonic conse- a word sounds (i.e., along the phonological, perceptual
quences is attention to the deeper semantic or meaning-based dimension), whereas older age groups may tend to do so based
aspects of experience rather than their surface-level percep- on their meanings (i.e., along the semantic dimension;
tual features. Semantic attention has been associated with Brainerd & Reyna, 2007; Dewhurst & Robinson, 2004). Such a
superior memory encoding at both behavioral (Challis et al., shifting bias from perceptual to semantic features may be
1996; Craik, 1977, 2010; Lockhart, 2002) and neural related to children's tendency to focus on perceptual infor-
(Fliessbach et al., 2010, 2011; Kapur et al., 1994; Schott et al., mation (Badger & Shapiro, 2012; Brainerd & Reyna, 1998;
2013; Staresina et al., 2009) levels in adults, perhaps by Fisher, 2011; Gentner, 1990; Helo et al., 2017). As to the latter,
encouraging elaboration (Addis & McAndrews, 2006; Staresina children show reduced selective attention (DeMarie-Dreblow
et al., 2009). Developmental work has shown that this memory & Miller, 1988; Enns & Cameron, 1987) in that they seem to
benefit emerges behaviorally early in life, by 3 years of age: be unable to filter out task-irrelevant information (Deng &
Both children (Ghetti & Angelini, 2008; Owings & Baumeister, Sloutsky, 2016; Plebanek & Sloutsky, 2017; Sloutsky & Fisher,
1979; Perlmutter et al., 1982; Puff et al., 1984) and adoles- 2004). For this reason, children may be less apt to attend to
cents (Andrade & Raposo, 2021; Owings & Baumeister, 1979) one dimension (semantic, perceptual) over the other, and/or
exhibit better memory when they focused on semantic as be less able than older participants to strategically guide or
compared with perceptual features of stimuli during encod- sustain their attention in accordance with current goals
ing, with the size of this memory boost increasing into young (Curtindale et al., 2007; Fisher et al., 2013; Lewis et al., 2017;
adulthood (Andrade & Raposo, 2021; Ghetti & Angelini, 2008; Plebanek & Sloutsky, 2018). Such a reduced ability to modulate
Owings & Baumeister, 1979; Perlmutter et al., 1982). Semantic attention in a top-down fashion might in part explain why
versus perceptual attention at retrieval has also been shown children benefit less from direction to attend to semantic
to influence engagement of the hippocampus (Hashimoto features during memory encoding than do adults (Andrade &
et al., 2012), a key memory structure (Scoville & Milner, Raposo, 2021; Ghetti & Angelini, 2008; Owings & Baumeister,
1957); as well as improve the accuracy of memory decisions 1979).
(Andrade & Raposo, 2021; Gallo et al., 2008; Ghetti & Angelini, Here, we characterized developmental differences in how
2008). Yet, how semantic versus perceptual attention is children, adolescents, and adults engaged semantic versus
deployed during an unguided memory retrieval task, and perceptual attention during memory retrieval. We trained a
whether this differs with development, remains unknown. pattern classifier to identify neural “states” associated with
We reasoned that attending to the meaning of either the semantic versus perceptual attention using data from a
memory retrieval prompts or the reactivated contents of separate task in which adults were alternately cued to attend
memory might be associated with better retrieval, particularly to each type of information (Vijayarajah & Schlichting, 2023).
on tasks that might benefit from access to semantic infor- We then applied this trained classifier to neural data from a
mation. However, we also anticipated developmental differ- developmental sample (Fynes-Clinton et al., 2019) to quantify
ences in how attention would be deployed. Broadly speaking, how they deployed attention during each of three retrieval
neural studies have shown differences in frontoparietal tasks probing autobiographical, semantic (factual), and
engagement during memory encoding (Chai et al., 2014; Maril episodic (picture) memory, respectively. Given children's dif-
et al., 2011; McAuley et al., 2007; Ofen et al., 2007; Shing et al., ficulty aligning attention in accordance with task goals, we
2016) and retrieval (Brod et al., 2017; DeMaster & Ghetti, 2013; expected age-related increases in the engagement of atten-
Fynes-Clinton et al., 2019; Ofen et al., 2012) between children tional states most related to the retrieved contentdi.e., se-
and adults, consistent with the notion that attentional dif- mantic attention during semantic retrieval, as these questions
ferences may at least in part explain age-related gains in required consideration of meaning; and perceptual attention
memory (Ghetti & Fandakova, 2020). Given the protracted during the retrieval of episodic memories, which focused on
structural and functional development of the frontoparietal perceptual details of pictures. With respect to autobiograph-
circuits (Dai et al., 2019; Fair et al., 2007; Farrant & Uddin, 2015; ical memories, we anticipated that children may show a
Wendelken et al., 2017) thought to underlie guided attention perceptual and adults a semantic bias given these memories
(Booth et al., 2003; Bowling et al., 2019; Corbetta et al., 2000; typically include a mixture of semantic and episodic details
Kastner et al., 1998; Marshall et al., 2015; Shomstein, 2012), one (King et al., 2022; Levine et al., 2002).
might expect such differences to be quite protracted, poten- As a secondary question, we also asked whether the
tially extending through adolescence. Yet, little work has been particular timecourse of attentional engagement differed over
done on attentionememory interactions in development, development. Retrieval trials were structured such that
especially during the adolescent period. questions were preceded by picture cues that hinted at the
With respect to the deployment of semantic versus topic of the upcoming question. We reasoned that children
perceptual attention more specifically, we predicted that there may be less apt to leverage these cues than adults, in line with
might be developmental differences in either (a) the tendency prior work (Hasselhorn, 1990; Heisel & Ritter, 1981;
to deploy semantic versus perceptual attention, and/or (b) the Kobasigawa, 1974; Mistry & Lange, 1985). Such a pattern would
c o r t e x 1 7 6 ( 2 0 2 4 ) 7 7 e9 3 79
also be consistent with cognitive control research, which has ensure an equal number of participants in each of the six
shown age-related increases in the tendency to engage pro- counterbalancing groups.
active (versus reactive) processes across many cognitive do-
mains (Chatham et al., 2009; Niebaum et al., 2021), including in 2.1.2. Memory Retrieval
memory (Paz-Alonso et al., 2009). Specifically, we predicted This publicly available dataset (Fynes-Clinton et al., 2019)
that while older participants (adults, adolescents) may pro- included 21 children (8 females, 13 males; mean ¼ 10.90 years;
actively engage attentional states in preparation for retrieval, 10e12 years old), 20 adolescents (11 females, 9 males;
younger ones (children) may instead wait for the particular mean ¼ 15.25 years; 14e16 years old), and 21 young adults
memory question to evoke them. (11 females, 10 males; mean ¼ 26.71 years; 20e35 years old). We
excluded the first three adults (based on their
participant number) from the final sample to serve as pilot
2. Method participants for the refinement of our analysis plan with this
dataset.
We used two independent functional magnetic resonance Participants all met a head motion inclusion criterion of
imaging (fMRI) datasets to ask how semantic versus having a framewise displacement (FD) that was less than
perceptual attention supports successful retrieval over 2 mm on average (set by Fynes-Clinton et al., 2019). Yet, even
development. In one dataset (hereafter, termed the “Atten- among this low-motion group of participants there were
tion Localizer”), young adults were cued to alternate between age-related decreases in motion (FD; children vs adolescents:
attending to semantic and perceptual features of pictures t ¼ 2.56, p ¼ .02, Cohen's d ¼ .81; children vs adults: t ¼ 4.01,
during scanning (Vijayarajah & Schlichting, 2023). We used p ¼ 2.95 104, d ¼ 1.30; adolescents vs adults: t ¼ 2.57,
this dataset to define neural semantic and perceptual p ¼ .01, d ¼ .84). We therefore performed control analyses to
attentional states, which were then compared with neural ensure age-related differences in head motion did not impact
patterns evoked in the second dataset (“Memory Retrieval”; our main results (see Supplementary materials: Accounting
publicly available data from Fynes-Clinton et al., 2019) to for age-related differences in framewise displacement).
quantify attention-related engagement in children, adoles-
cents, and adults performing a series of retrieval tasks. Our 2.2. Procedure
predictions and analysis plan for this investigation were
preregistered (https://osf.io/bhg3d; analysis code can be 2.2.1. Attention Localizer task
found here: https://osf.io/6yej7), with deviations (largely for A full description of the task design can be found in Vijayarajah
simplicity) and follow-up exploratory analyses indicated and Schlichting (2023). Briefly, participants viewed 144
throughout the paper. We present analyses exactly as pre- storybook-style illustrations organized into 18 blocks of eight
registered in the Supplementary materials; briefly, they do illustrations each. Prior to each block, participants were cued
not meaningfully differ from those in the main paper. We with a simple shape (pre-trained to be associated with a
also report how we determined our sample size, all data particular task; shape-task mapping counterbalanced across
exclusions, all inclusion/exclusion criteria, whether inclu- participants; 2500 msec followed by a 500 msec inter stimulus
sion/exclusion criteria were established prior to data anal- interval [ISI]) to orient to either the semantic meaning (story) or
ysis, all manipulations, and all measures in the study. perceptual (artist style) features of the upcoming illustrations
by detecting repeats along the corresponding dimension (nine
2.1. Participants artist blocks, nine story blocks; assignment of blocks to con-
ditions was counterbalanced across participants). Illustrations
All participants (from both datasets) met the following were presented one at a time (2500 msec, 500 msec ISI), and
criteria: right-handed; free from a diagnosis of mental illness, each block contained at least one repeat along each the story
neurological disorders, and vision or hearing impairments; (consecutive illustrations that depicted the same story, but
and had no MRI contraindications. All participants also pro- were created by different artists) and artist style (different
vided consent (parents or legal guardians provided consent for stories, same artist) dimensions. Participants indicated with a
participants under 17 years of age) and were compensated for button press whether each illustration was or was not a repeat
their time ($25 CAD per hour for Attention Localizer; $30 AUD along the cued dimension.
per hour for Memory Retrieval). The experiment was divided into three scanning runs of
equal length, with three blocks from each condition per run.
2.1.1. Attention Localizer We included fixation time at the beginning (3000 msec) and
This experiment included 46 young adults (18e35 years old) end (9000 msec) of each run to account for stabilization and
from a previous investigation (Vijayarajah & Schlichting, lag of the MR signal, respectively. Participants also completed
2023). Four participants were excluded from the final sample blocks from an orthogonal baseline task which asked them to
for pilot analyses (N ¼ 1), illness in the scanner (N ¼ 1), and indicate which of three squares (left, middle, or right) a dot
poor performance on a memory test not considered here appeared in each of the eight baseline task trials (2500 msec,
(N ¼ 2). These exclusions yielded a final sample size of 42 500 msec ISI) in a block.
participants (28 females, 14 males; mean ¼ 19.80 years; 18e30
years old), which was determined a priori to both achieve 80% 2.2.2. Memory Retrieval task
power to detect an effect size of Cohen's d ¼ .45 estimated Fynes-Clinton, et al. (2019) designed the retrieval tasks to
from previous work (Aly & Turk-Browne, 2016) and also investigate whether shared or differentiated brain networks
80 c o r t e x 1 7 6 ( 2 0 2 4 ) 7 7 e9 3
support autobiographical, semantic, and episodic retrieval related content. Autobiographical questions prompted the
over development. Here, we used their dataset to ask a novel retrieval of a past experience, and participants rated the
questiondhow neural attentional states (defined in the retrieved memory for vividness. Semantic questions tested
Attention Localizer) are engaged during the successful participants' factual knowledge with multiple-choice ques-
retrieval of these different types of content in development. tions. Episodic questions tested participants' memory for de-
An in-depth description of the tasks can be found in the tails from the picture cue stimuli which had appeared in all
original paper (Fynes-Clinton et al., 2019). For consistency, we three tasks, also in a multiple-choice format (Fig. 1).
use the same task names as Fynes-Clinton et al. (2019). To The retrieval tasks were separated into three different
summarize, participants performed autobiographical, se- scanning runs and appeared in a fixed order, with the auto-
mantic, and episodic retrieval tasks that each consisted of 25 biographical task in the first run, followed by the semantic
trials made up of picture cues depicting general topics task in the second run, and lastly the episodic task in the third
(4000 msec with a 1000 msec ISI; e.g., a picture of a dentist run. The episodic task was completed last because the original
checking their patient's teeth) followed by retrieval questions authors reasoned this order would encourage participants to
(8000 msec with a jittered 800e1200 msec inter-trial interval; rely on their long-term memory for the picture cues from the
mean jitter ¼ 1000 msec) that prompted the retrieval of task- preceding tasks as opposed to their visual working memory
Fig. 1 e Memory Retrieval tasks and behavior. (A) Task paradigm based on the figure by Fynes-Clinton et al. (2019).
Participants first performed an autobiographical task (fuchsia) where they retrieved past experiences related to the picture
cue (the dentist visit; this picture cue did not appear in the real experiment and is solely presented here for descriptive
purposes) and rated the vividness of the retrieved memory. In the second scanning run, participants were provided the
same picture cues and asked to retrieve a related general knowledge fact (semantic task; teal). In the final scanning run,
participants were asked about details from the picture cue which had been presented twice before this task (episodic task;
orange). Intermixed in each run were baseline task trials (depicted in D). (B) The percentage of correct trials in the semantic
and episodic tasks with age group on the x-axis and accuracy as a percentage on the y-axis. The larger circles represent
group mean; points are individual participants; intervals are standard error around the group mean. (C) The percentage of
retrieved autobiographical memories rated with high vividness depicted as in B. (D) The baseline task showed a scrambled
image cue followed by a simple perceptual judgment.
c o r t e x 1 7 6 ( 2 0 2 4 ) 7 7 e9 3 81
(Fynes-Clinton et al., 2019). Furthermore, because all trials in a functional scans during preprocessing. We additionally
given run were from the same task, participants could always calculated the temporal derivative for the standard six motion
anticipate the type of retrieval question that would appear. parameters and FD for each volume using custom Python
Participants also performed five trials from a baseline task scripts. Lastly, we included the six anatomical CompCor mo-
that were intermixed with retrieval trials in each task. The tion components (Behzadi et al., 2007) derived during
baseline task had the same structure as retrieval trials, but preprocessing.
instead presented scrambled pictures as cues followed by
non-memory-based perceptual matching questions. 2.3.5. Anatomical mask
We characterized attention-related neural engagement
2.3. MRI data acquisition and preprocessing within a group whole-brain gray-matter (GM) mask derived
from participants in both datasets. This group GM mask was
2.3.1. Attention Localizer parameters made by first creating participant-specific GM masks using the
Functional volumes were acquired with a multi-band echo- T1-weighted GM tissue-probability maps generated during
planar imaging (EPI) sequence that collected 69 oblique axial preprocessing by FSL FAST (in fMRIprep). The masks were
slices (repetition time [TR] ¼ 1500 msec, echo time then thresholded at .5 to restrict to voxels with 50% or greater
[TE] ¼ 28.0 msec, flip angle ¼ 71 , 220 220 138 mm matrix, probability of being located within GM. Participant-specific
2 mm isotropic voxels, multiband acceleration factor ¼ 3, masks were then resampled to the 2 mm functional data di-
GRAPPA factor ¼ 2). One T1-weighted 3D magnetization- mensions using nearest neighbor interpolation, combined,
prepared rapid gradient echo (MPRAGE) volume (256 and thresholded again to include only voxels that were in GM
256 160 mm matrix, 1 mm isotropic voxels) was acquired for for at least 50% of all participants for the final group mask.
spatial normalization, followed by a field map for suscepti- Subsequent analyses in both datasets were restricted to vox-
bility distortion correction (TR ¼ 700 msec, TE ¼ 4.92/ els within this group mask.
7.38 msec, flip angle ¼ 60 , 220 220 138 mm matrix, 2 mm
isotropic voxels). 2.4. Leveraging the Attention Localizer to quantify
attentional states in memory retrieval
2.3.2. Memory Retrieval parameters
Raw MRI data were retrieved from OpenNeuro (Markiewicz We first characterized semantic versus perceptual attentional
et al., 2021; https://openneuro.org/datasets/ds001748/ states from the Attention Localizer, and then used these
versions/1.0.4). Functional volumes were collected with an states to ask how children, adolescents, and adults from the
EPI sequence that consisted of 45 slices (2.5 mm isotropic Memory Retrieval dataset evoked attention during successful
voxels; TR ¼ 3000 msec; TE ¼ 30 msec; FOV ¼ 190 mm). A T1- retrieval.
weighted MPRAGE (1 mm isotropic voxels; FOV ¼ 256 mm)
volume was also acquired. More acquisition details can be 2.4.1. Data preparation
found in Fynes-Clinton et al. (2019). Prior to performing the attentional state analyses, we shifted
the condition onsets in each scanning run from both datasets
2.3.3. MRI preprocessing by 6 sec to account for hemodynamic lag in the fMRI signal.
Both datasets were preprocessed with the same fMRIprep To ensure our state analyses were restricted to task-related
pipeline (version 1.1.4; Esteban et al., 2018), with functional neural patterns, we also excluded non-task fixation time
volumes from the Memory Retrieval dataset additionally from the data. In the Attention Localizer specifically, we
resampled to the 2 mm isotropic dimensions used in the excluded 3 TRs at the onset of each attention cue to remove
Attention Localizer for our subsequent analyses. In this data associated with cue-to-condition transition periods.
pipeline, T1-weighted volumes were skull-stripped through
the ANTs brain extraction tool (Avants et al., 2011), and 2.4.2. Classifier cross-validation and training (Attention
segmented for cerebrospinal fluid, white-matter, and gray- Localizer dataset)
matter (GM) with FSL FAST (Zhang et al., 2001). These vol- Because our ultimate goal involved defining neural states in
umes were then normalized to MNI152NLin2009cAsym space one group of participants and applying them to another (i.e.,
with ANTs nonlinear registration. Functional data were cor- the Memory Retrieval dataset), we focused on identifying
rected for motion using FSL MCFLIRT and normalized to the attentional states that generalized across different individuals.
2 mm isotropic template space using nonlinear registration To do this, we had a sparse multinomial logistic regression
via the T1 anatomical (boundary-based registration; 9 degrees (SMLR) classifier (PyMVPA; default parameters; no feature se-
of freedom; using BBREGISTER in FreeSurfer; Greve & Fischl, lection was performed; Hanke et al., 2009) decode semantic
2009). All transformations were computed, concatenated, versus perceptual attentional states across all 42 participants
and applied in a single step using antsApplyTransforms and in the Attention Localizer using leave-one-participant-out-
Lanczos interpolation in ANTs. cross-validation. In this cross-validation, we trained the clas-
sifier on condition-labeled TRs from the semantic (story) and
2.3.4. Nuisance regressors perceptual (artist style) attention conditions from all but six
We calculated motion nuisance regressors using fMRIprep participantsdholding out one from each of the six counter-
and custom scripts. The standard six motion parameters (x, y, balancing groupsdand tested the accuracy of the classifier's
z, yaw, pitch, roll) and framewise displacement (FD) for each predictions on the six held-out participants. This decision was
functional volume were derived from motion correction of made to ensure the training dataset was balanced in terms of
82 c o r t e x 1 7 6 ( 2 0 2 4 ) 7 7 e9 3
the assignment of cues to condition. We repeated this process (calculated with the emmeans package; Searle et al., 2023) to test
seven times (42/6) so that the classifier was tested on each for reliable evidence of attentional bias (i.e., a difference score
participant once. We found that we could decode semantic significantly above or below 0), age group differences, and con-
versus perceptual attentional states across different partici- dition differences. Our focus on results predicting the difference
pants significantly above chance (mean ¼ .64; 95% CI [.62, .66]; between classifier evidence for semantic versus perceptual
t-test vs .50; t ¼ 13.20, p ¼ 2.23 1016, d ¼ 2.04). attention rather than evidence for each state is a deviation from
We used a classifier trained on neural data from all 42 our preregistered analysis. Our reasons for this deviation were
participants to interrogate attentional states evoked in the to both simplify our results section and ensure independence of
Memory Retrieval dataset. We additionally included baseline the observations going into our mixed modelsdsuch that each
task neural data in this classifier training solely to reduce correct retrieval trial contributed exactly one data point within
dependency in the neural patterns characterized as semantic the model. We report our preregistered analysis of semantic
versus perceptual attention across people. This classifier versus perceptual evidence as separate levels of a categorical
could decode neural patterns reflective of semantic attention, predictor in the Supplementary materials.
perceptual attention, and the baseline task across different In our preregistered follow-up analyses, we examined
participants significantly above chance (mean ¼ .75; 95% CI whether there were age-related differences in how semantic
[.74, .76]; t-test vs .33; t ¼ 61.20, p ¼ 6.90 1042, d ¼ 9.42) using versus perceptual attentional states were evoked when
the same cross-validation approach. considering different trial periods within each taskdi.e., in
preparation for retrieval (picture cue) versus during retrieval
2.4.3. Classifier application to memory retrieval (Memory prompts (retrieval question).
Retrieval dataset)
We applied the trained classifier to functional data from each 2.5. Exploratory general linear model (GLM) analyses for
retrieval task to test for age- and task-related differences in univariate engagement during retrieval trial periods
attentional states. This classifier yielded prediction probabil-
ities for both attentional states on a TR-by-TR basis for each We used univariate contrasts to identify brain regions that
participant, and for each retrieval task. These prediction mirrored the age-related attention differences in semantic
probabilities were then log odds transformed to correct for retrieval we uncovered in the classification analysis that
non-normality in the distribution of raw classification proba- separately considered picture cue and question periods. To
bilities for all TRs (as done in Richter et al., 2016; using the logit do this, we modeled univariate engagement separately for
function a part of the car package; Fox & Weisberg, 2015), and picture cues and retrieval questions in correct versus incor-
averaged across TRs within the same trial to derive one clas- rect trials from the semantic task. Picture cues were modeled
sifier estimate for each attentional state for every trial. We for a duration of 4000 msec while question periods were
additionally restricted our analysis to baseline and retrieval modeled for an 8000 msec duration; all events were then
task trials that were correctdor in the case of the autobio- convolved with the double-gamma hemodynamic response
graphical task, rated with high vividnessdto capture atten- function. We also included temporal derivatives for all task
tional state engagement associated with successful retrievals. regressors along with the 18 volume-wise nuisance re-
gressors derived during preprocessing in these GLMs. Tem-
2.4.4. Testing age group differences in attention during poral autocorrelation correction was performed using FILM
retrieval prewhitening. These GLMs resulted in participant-specific
We used (generalized) linear mixed-effects models (lme4 pack- statistic images for each trial period in correct and incor-
age version 1.1e26; Bates et al., 2015) implemented in R version rect trials from the semantic task and the baseline task. With
4.0.4 (Team, 2021) to test whether classifier evidence for se- these statistic images we modeled our contrasts of interest
mantic versus perceptual attentional states varied as a function (semantic task picture cue > retrieval question and retrieval
of (1) memory retrieval (across all three retrieval tasks) versus question > picture cue, both restricted to correct trials) in
the baseline task in each age group, (2) the different retrieval each participant.
tasks (autobiographical, semantic, episodic) in each age group, Parameter estimates for these contrasts were then sub-
and (3) the different age groups within each retrieval task. Each mitted to higher-level FEAT GLMs (Woolrich et al., 2004) that
model predicted the difference between classifier evidence for estimated the univariate response for each contrast across
semantic versus perceptual attentional states (semantic participants, while accounting for between-participant vari-
perceptual evidence) to ask whether there was reliable evidence ance (mixed-effects FLAME 1). These higher-level GLMs were
for a semantic (semantic > perceptual, or semantic perceptual tested for the interaction of age group on voxels activated for
difference score above 0) or perceptual (perceptual > semantic; picture cues versus retrieval questions, at the whole brain
semantic perceptual below 0) attentional bias, while ac- level (correction for multiple comparisons was performed
counting for within-participant random effects using random using cluster-based Gaussian random field theory [Worsley
intercepts (when interrogating differences within the same et al., 2002], with a cluster-forming threshold of z 3.1 and
task) or slopes (when interrogating task differences). Models whole-brain corrected cluster significance level of p < .05). For
that interrogated age group differences in attention also the clusters that emerged at this threshold, we extracted their
included age group as an ordered categorical predictor cluster activation from each trial period and age group in
(adults > adolescents > children) to test changes in attention order to perform follow-up pairwise t-tests that revealed the
over development. We performed follow-up pairwise compari- condition differences that contributed to the age group and
sons with the estimated marginal means from these models trial period interaction.
c o r t e x 1 7 6 ( 2 0 2 4 ) 7 7 e9 3 83
Fig. 2 e Age-related differences in attentional bias during each retrieval task. Attentional bias (y axis) is depicted as a
function of the retrieval tasks (x axis; autobiographical in fuchsia, semantic in teal, and episodic in orange) and age group
(children in light colors, adolescents in medium-dark colors, and adults in dark colors). Larger circles represent the group
estimated marginal means; points are individual participants; intervals are standard error around the estimated marginal
mean. Asterisk denotes the significant age group difference in attentional bias within the semantic task. Asterisk above the
age group means denote significant evidence of an attentional bias in that task. *p < .05, ***p < .001, ****p < .001.
Indeed, attentional bias varied by age group and trial period the autobiographical task (b ¼ .43, SE ¼ .08, t ¼ 5.56,
in the semantic task (F ¼ 3.27, p ¼ .04; Fig. 3)dan overall p ¼ 2.78 105), with all ages showing a significant semantic
interaction that was driven by adults showing a pattern that attentional bias during the question period (children: t ¼ 6.03,
was significantly different from adolescents (b ¼ .20, SE ¼ .09, p < 1.00 104; adolescents: t ¼ 5.01, p < 1.00 104; adults:
t ¼ 2.30, p ¼ .02; interaction when excluding the child group) t ¼ 4.69, p < 1.00 104) but not picture cue (all p > .42). There
and marginally so from children (b ¼ .18, SE ¼ .09, t ¼ 1.96, was no effect of trial period on attentional bias in the episodic
p ¼ .05; interaction when excluding the adolescent group); task (p ¼ .47).
children and adolescents were not significantly different from Furthermore, the semantic task results were also robust to
one another when adults were dropped from consideration control analyses that account for age group differences in
(p ¼ .35). Specifically, adults demonstrated a reliable semantic head motion and response times (reported in the
attentional bias during the picture cue (t ¼ 3.33, p ¼ 1.50 103) Supplementary materials). Therefore, despite no reliable dif-
but not question period (p ¼ .88), while adolescents demon- ference between adolescents and adults in either semantic
strated the opposite pattern, showing a semantic bias during task behavior (Fig. 1) or attentional biases when we considered
the question period (t ¼ 3.53, p ¼ 6.00 104) but not picture cue the entire semantic retrieval trial as a whole (Fig. 2), separately
(p ¼ .10). Children did not show a reliable attentional bias at considering picture cue and retrieval questions showed that
either trial period (both p > .28). Moreover, comparing across the two groups evoked this bias at different periods to retrieve
age groups revealed that adolescents showed significantly the same factual knowledge.
greater semantic bias during the question period when
compared to the other age groups (adults: t ¼ 2.38, p ¼ .01; 3.5. Neural mechanisms that mirror attentional state
children: t ¼ 1.99, p ¼ .05). During the picture cue, adults differences in picture cues versus question periods from the
showed a greater semantic bias relative to children (t ¼ 2.23, semantic task
p ¼ .03) but not adolescents (p ¼ .23).
Age-related differences in the timecourse of attentional We carried out follow-up exploratory analyses (that were not
bias were only observed in the semantic task: There was no pre-registered) to identify brain regions that may underlie the
interaction of age group and trial period on attentional bias in observed interaction between age group and trial period on
the autobiographical (p ¼ .33; Fig. S2) or episodic (p ¼ .75; attentional biases in the semantic task (Fig. 3). Specifically, we
Fig. S3) tasks. Instead, attentional bias varied by trial period in performed a univariate whole-brain contrast to determine
c o r t e x 1 7 6 ( 2 0 2 4 ) 7 7 e9 3 85
Fig. 3 e Age group differences in attentional bias during the semantic task trial periods. Attentional bias is depicted as a
function of the semantic task trial periods (picture cue with open circles, retrieval question as closed circles) and age with
color (children in light teal, adolescents in medium-dark teal, and adults in the darkest teal). Larger circles represent group
estimated marginal means; points are individual participants; intervals are standard error around the estimated marginal
mean. Tensor product symbol denotes significant interaction of age group and trial period on attentional bias. Asterisks
above the trial period means denote significant evidence of an attentional bias in that trial period, for that age group.
*p < .05, **p < .01, ***p < .001.
where in the brain univariate engagement varied by this differently engaged ventral visual and superior parietal cortex
interaction (i.e., age [adults vs adolescents] trial period regions during the preparatory picture cue period of semantic
[picture cue vs question period]). We focused on comparing factual retrieval trials.
only adolescents and adults as these were the only two groups
to show a significant semantic attentional bias during either
trial period. This analysis revealed two clusters sensitive to 4. Discussion
these age group differences: one spanning ventral visual and
lateral temporal cortex, and the other in right superior parietal Here, we characterized how attention shapes the develop-
cortex (Fig. 4A). While both age groups engaged ventral visual ment of successful memory retrieval. We first identified se-
regions more during the picture cue than question period mantic versus perceptual attentional states that successfully
(adolescents: t ¼ 5.18, p ¼ 5.39 105, d ¼ 1.16; adults: t ¼ 2.52, generalized across different individuals. With these atten-
p ¼ 2.15 102, d ¼ .03), adolescents engaged this region more tional states, we examined age group differences in attention
than adults during the picture cue (t ¼ 4.57, p ¼ 5.29 105, during the successful retrieval of autobiographical memories,
d ¼ 1.46; Fig. 4B). In contrast, adolescents engaged right su- semantic factual knowledge, and episodic picture details in an
perior parietal cortex more during the question versus picture independent group of children, adolescents, and adults. All
cue (t ¼ 5.18, p ¼ 5.39 105), while adult showed no reliable age groups demonstrated a semantic attentional bias during
activation difference between these trial periods (p ¼ .92). memory retrieval compared with non-memory judgments in
However, adults did recruit this region more during the pic- the baseline task. However, there were age-related changes in
ture cue than adolescents (t ¼ 3.90, p ¼ 3.88 104, d ¼ 1.25; this bias during the semantic retrieval task, such that a reli-
Fig. 4C). These findings show that adolescents and adults able semantic bias was observed in adolescents and adults but
86 c o r t e x 1 7 6 ( 2 0 2 4 ) 7 7 e9 3
childhood to adolescence may reflect immaturity in how information (Martin et al., 2023; Thompson et al., 2017). We
children's general knowledge is structured, how accessible speculate that while adolescents may possess the knowledge
relevant knowledge is during retrieval, or a combination of required to answer the factual questions, underdeveloped
both. While such protracted development may seem incon- attention control mechanisms may prevent easy access to this
sistent with previous frameworks that suggests semantic information, such that specific retrieval prompts are neces-
structures mature first to lay the foundation for highly sary for this semantic attentional engagement.
contextual episodic and autobiographical memories (Conway Adults and adolescents also engaged superior parietal
& Pleydell-Pearce, 2000; Keresztes et al., 2017), the nature of cortex and ventral visual regions differently over the time-
the semantic content participants retrieved here aligned more course of factual knowledge retrieval. Adolescents engaged
with specialized factual knowledge that is slowly accumu- ventral visual regions during picture cues more than adults,
lated over one's lifetime (Conway & Pleydell-Pearce, 2000; Lin which may reflect their enhanced perceptual processing (e.g.,
& Murphy, 2001; Voss et al., 1986). Less experience with the Fisch et al., 2009; Hiramatsu et al., 2011; Kim et al., 2020) of the
specialized knowledge domains tested in the semantic task cue over using its content to guide their attention. Adults
may contribute to age group differences in how this knowl- instead engaged superior parietal cortex more during the
edge is structured (Favarotto et al., 2014; Gobbo & Chi, 1986; picture cue in comparison to adolescents. Adults' enhanced
Siew & Guru, 2023) and the accessibility of this knowledge recruitment of parietal cortex during these preparatory
during retrieval (Horgan & Morgan, 1990). Unlike previous retrieval periods could potentially reflect their use of parietal
work that assessed age-related differences in knowledge mechanisms that support (1) memory searches through past
structure using participants' self-report responses (e.g., Lin & knowledge for the relevant information (Humphreys &
Murphy, 2001; Unger et al., 2016; Unger & Fisher, 2019), here, Lambon Ralph, 2015), (2) the reactivation of the related
we demonstrate developmental changes in this knowledge knowledge (Jonker et al., 2018; Kuhl & Chun, 2014; Kuhl et al.,
using objective measures that were characterized in a 2013), and/or (3) internal memory signals about the degree to
completely different experiment and set of participants. which the relevant information has been successfully
Age-related differences in semantic attention during retrieved (Vilberg & Rugg, 2008). In contrast, adolescents may
factual knowledge retrieval were also evident in its time- not be able to leverage the same mechanisms because of
course. Despite adults and adolescents showing no reliable immaturity in their parietal-based cognitive control networks
difference in accuracy or response times on average in the (Chai et al., 2017; Ciesielski et al., 2006; Farrant & Uddin, 2015;
semantic task, these age groups engaged attention during Solis et al., 2021), memory retrieval systems (Daugherty et al.,
different periods to access the same knowledge: Adults pro- 2017; Keresztes et al., 2017; Lee et al., 2014, 2020; Ofen et al.,
actively engaged semantic attention in preparation for 2007; Schlichting et al., 2022; Selmeczy et al., 2019), or the
knowledge retrieval (i.e., showed significant evidence of a interaction of both.
semantic attention bias during the picture period) while ado- One limitation of this work is that we characterized se-
lescents instead engaged these states when provided the mantic attentional states within a group of adults. Poten-
retrieval question. While it may be puzzling that adults and tially, children may not demonstrate reliable differences in
adolescents demonstrate different neural approaches during attention during factual retrieval in the current experiment
factual knowledge retrieval yet achieve similar behavior, one because they evoke a more age-group specific semantic
possibility is that high performance on this task (average ac- cognitive state our classifier was not trained to detect. Given
curacy in adults and adolescents ¼ 93.85%) obscures our our approach relies upon the generalization of attentional
ability to characterize behavioral differences between these states across age groups, we are not poised to detect if these
age groups that relate to the observed neural differences. states were specific to a particular age group. However, it is
Future work using a semantic task that encourages more er- important to note that our classifier did successfully gener-
rors in adults and/or adolescents may reveal nuanced re- alize to attentional states evoked by children for some
lationships between semantic retrieval behavior and the retrieval types. More specifically, children demonstrated a
neural changes characterized here. reliable semantic bias during memory retrieval (collapsed
This timecourse difference between adolescents and across all three retrieval tasks) in comparison to the
adults is consistent with work demonstrating age-related in- orthogonal baseline task (Fig. S1). Furthermore, there were
creases during childhood in the proactive engagement of no reliable age group differences in this attentional bias in
control mechanisms for many different cognitive tasks the autobiographical or episodic tasks. These findings sug-
(Chatham et al., 2009; DeMarie-Dreblow & Miller, 1988; gest that our classifier trained on adult states could suc-
Niebaum et al., 2021; Paz-Alonso et al., 2009), but also extends cessfully characterize attentional states in children, with age
this idea by demonstrating that such improvements continue group differences in these states observed during semantic
into adolescence (Calabro et al., 2020; Larsen & Luna, 2018; knowledge retrieval. Nevertheless, it is possible that the
Luna et al., 2010; Ravindranath et al., 2020) and in the domain nature of our classifier trained on adult data can at least in
of memory. One potential explanation as to why we see these part explain why we saw no evidence of a semantic bias in
proactive versus reactive retrieval-related attention differ- children during the semantic task. Namely, it might be that:
ences is the protracted development of frontoparietal control (1) children are simply more variable in their neural semantic
networks (Crone, 2009; Hwang et al., 2010; Rohr et al., 2018; retrieval states, leading to a null effect on average; (2) se-
Tooley et al., 2022) that broadly support the strategic deploy- mantic retrieval states in children may not be generalizable
ment of attention in service of task goals (Scolari et al., 2015; because of differences in factual knowledge; and/or (3) chil-
Szczepanski et al., 2013) and the retrieval of semantic dren may leverage a very different approach to perform the
88 c o r t e x 1 7 6 ( 2 0 2 4 ) 7 7 e9 3
semantic task that does not map onto our attentional states. Writing e review & editing. Margaret L. Schlichting: Funding
Future work that examines how age-specific semantic acquisition, Methodology, Resources, Software, Supervision,
attentional states relate to successful retrieval is needed to Visualization, Writing e review & editing, Conceptualization.
test these possibilities.
Our novel approach of characterizing developmental The authors declare no competing financial interests.
changes in the types of attention that support retrieval
revealed nuanced differences in semantic retrieval that
persisted through adolescence. Specifically, we found Acknowledgments
continued refinement in attention during the retrieval of
factual knowledge from childhood to adolescence, in com- We thank A. Finn, M. Mack, M. Moscovitch, S. Allidina, and
parison to episodic and autobiographical retrieval that did members of the Budding Minds lab for helpful discussions.
not show these age group differences. Developmental
refinement was also observed in the timecourse of semantic
retrieval: Adults evoked attention in preparation for this Supplementary data
retrieval while adolescents used explicit retrieval prompts to
guide their attention, with this timecourse difference re- Supplementary data to this article can be found online at
flected in differential engagement of superior parietal cortex https://doi.org/10.1016/j.cortex.2024.04.012.
and ventral visual regions. Both the accumulation of general
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