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Impaired prospective memory but intact episodic memory in intellectually average 7- to 9-
year-olds born very preterm and/or very low birth weight
Ruth M. Ford*, Sarah Griffiths, Kerryn Neulinger, Glenda Andrews, David H. K. Shum, and
Peter H. Gray
Ruth M. Ford*, Department of Psychology, Anglia Ruskin University, East Road, Cambridge, CB1 1PT, United KingdomPhone: +44 0845 196 5125 Email: ruth.ford@anglia.ac.uk
Sarah Griffiths, Menzies Health Institute Queensland and School of Applied Psychology, Griffith University, Mt Gravatt campus, Queensland 4122, AustraliaEmail: sarah.griffiths@griffithuni.edu.au
Kerryn Neulinger, Menzies Health Institute Queensland and School of Applied Psychology, Griffith University, Mt Gravatt campus, Queensland 4122, AustraliaEmail: k.neulinger@griffith.edu.au
Glenda Andrews, Menzies Health Institute Queensland and School of Applied Psychology, Griffith University, Gold Coast campus, Queensland 4222, AustraliaEmail: g.andrews@griffith.edu.au
David H. K. Shum, Menzies Health Institute Queensland and School of Applied Psychology, Griffith University, Gold Coast campus, Queensland 4222, AustraliaEmail: d.shum@griffith.edu.au
Peter H. Gray, Mater Research Institute, University of Queensland, and Mater Mothers’ Hospital, South Brisbane, Queensland 4101, AustraliaEmail: Peter.Gray@mater.org.au
*Corresponding author
Abstract
Relatively little is known about episodic memory (EM: memory for personally-experienced
events) and prospective memory (PM: memory for intended actions) in children born very
preterm (VP) or with very low birth weight (VLBW). This study evaluates EM and PM in
mainstream-schooled 7- to 9-year-olds born VP (≤ 32 weeks) and/or VLBW (< 1500 g) and
matches full-term children for comparison (n = 35 and n = 37, respectively). Additionally,
participants were assessed for verbal and non-verbal ability, executive function (EF), and theory
of mind (ToM). The results show that the VP/VLBW children were outperformed by the full-
term children on the memory tests overall, with a significant univariate group difference in PM.
Moreover, within the VP/VLBW group, the measures of PM, verbal ability and working memory
all displayed reliable negative correlations with severity of neonatal illness. PM was found to be
independent of EM and cognitive functioning, suggesting that this form of memory might
constitute a domain of specific vulnerability for VP/VLBW children.
KEYWORDS: Preterm children, Preterm birth, Very low birth weight, Episodic memory, Prospective memory,
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Up to 10% of newborn infants are very preterm (VP: < 32 weeks gestation), very low birth
weight (VLBW: < 1500 g), or both. Despite improvements in obstetric and neonatal medical care
that have lowered mortality rates and reduced the incidence of major disabilities such as cerebral
palsy, such infants remain vulnerable to brain injuries and aberrant brain maturation that can lead
to developmental delay (Aylward, 2005). Compared to full-term children of similar
socioeconomic status (SES), VP/VLBW children have lower IQs and perform more poorly at
school (Aarnoudse-Moens, Oosterlaan, Duivenvoorden, van Goudoever, & Weisglas-Kuperus,
2011; Botting, Powls, Cooke, & Marlow, 1998). Moreover, they are at higher risk of language
impairments (Woodward et al., 2009), motor and sensorimotor coordination difficulties (Bos,
Van Braeckel, Hitzert, Tanis, & Roze, 2013; Bracewell & Marlow, 2002), and executive
dysfunction (Aarnoudse-Moens, Duivenvoorden, Weisglas-Kuperus, van Goudoever, &
Oosterlaan, 2012).
Brain injuries in VP/VLBW infants are likely to reflect adverse perinatal events, including
intrauterine infection, respiratory distress syndrome, and intraventricular hemorrhage (Volpe,
2009). Magnetic resonance imaging (MRI) studies have revealed reductions of brain volume
afflicting both white and grey matter (de Kieviet, Zoetebier, Van Elburg, Vermeulen, &
Oosterlann, 2012) which foreshadow poorer neurodevelopmental outcomes (Nosarti et al., 2014).
Brain structures that are most vulnerable to damage include the hippocampus, caudate nucleus,
thalamus, corpus callosum and cerebellum (Nosarti et al., 2014). Even VP/VLBW children of
average intelligence are susceptible to impairments of more complex cognitive and motor skills
in laboratory tests, implicating the existence of subtle abnormalities of neural connectivity and
brain development (Foulder-Hughes & Cooke, 2003; Kallankari, Kaukola, Olsén, Ojaniemi, &
Hallman, 2015).
VP/VLBW children are also prone to memory problems, argued to reflect damage to the
hippocampal-cortical networks (for a review, see Nosarti & Froudist-Walsh, 2016). Such
problems are the focus of the present study, in which the memories of VP/VLBW children are
evaluated for complex events in terms of episodic memory (EM: memory for personally-
experienced events) and prospective memory (PM: memory for future intentions). Both EM and
PM are critical to successful functioning in daily life (e.g., remembering names and addresses,
remembering to pay bills and take medication on time); moreover, they are likely to play an
important role in academic success. It has been suggested that EM difficulties can impede the
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encoding and retrieval of factual knowledge (Greenberg & Verfaellie, 2010) while PM
difficulties can hinder academic performance by exacerbating behavioral disorganization, for
example if children forget to complete their homework or miss other important deadlines at
school (Mahy, Moses, & Kliegel, 2014).
The Nature and Development of Episodic and Prospective Memory
According to Tulving (2002), EM relies on the ability to encode rich contextual details regarding
when and where an event occurred, lending the retrieved memories a robust sense of time and
place. Tests of EM typically involve questions about source memory, such as asking participants
in which list they saw a particular word or in which voice they heard a particular word spoken
(also referred to as source monitoring; Johnson, Hashtroudi, & Lindsay, 1993). Tulving further
argues for the existence of two distinct forms of subjective consciousness during memory
retrieval; specifically, he distinguishes between noetic (aware) consciousness, which he believes
evokes a rudimentary sense of simply knowing that an event occurred (also called familiarity),
and autonoetic (self-aware) consciousness, which he judges to drive the phenomenal experience
of reliving one’s personal past that is typically accompanied by abundant and vivid imagery (also
termed recollection). Although some researchers dispute the idea that familiarity and recollection
are independent, preferring instead to view them as opposite ends of a continuum of memory
strength, it is generally agreed that the likelihood of recollection is enhanced given superior
encoding and retrieval of contextual and relational information (Wixted & Mickes, 2010).
Developmental research indicates that EM emerges during the preschool years and improves
until late adolescence. Older children outperform younger ones in the ability to freely recall
event-related information (Schneider & Pressley, 1997) and they demonstrate a superior capacity
for item–context binding and source-monitoring processes across a variety of paradigms
(Drummey & Newcombe, 2002; Sluzenski, Newcombe, & Kovacs, 2006). Moreover,
electrophysiological studies have identified a later onset and more protracted maturation of the
neural correlates of recollection than the neural correlates of familiarity; while recollection
processes continue to develop well into the second decade of life it appears that familiarity
processes have stabilized by middle childhood (for a review, see Ghetti & Lee, 2014). This trend
is likely to reflect maturation of the brain centers involved in EM, including the medial temporal
lobe (especially the hippocampus) and the prefrontal cortex, as well as the white matter tracts
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that connect them. Evidence suggests that the hippocampus helps to bind individual features of
events into complex representations which are integral to recollection, with the prefrontal cortex
supporting the executive processes driving the encoding and retrieval of bound representations
(for a review, see Ghetti & Bunge, 2012).
There is considerable debate regarding whether PM is related to EM or constitutes a distinct
form of memory. One suggestion in line with the former view is that PM involves simulation of
future scenarios during intention formation, thus making it a forward-looking component of the
episodic system (Schacter, Addis, & Buckner, 2008). Certainly, performance on PM tasks
follows a similar developmental trajectory to EM (Mahy et al., 2014) and draws on many of the
same brain regions, including prefrontal regions, parietal regions and the hippocampus (Burgess,
Quayle, & Frith, 2001; Gordon, Shelton, Bugg, McDaniel, & Head, 2011). In children, both PM
and EM correlate positively with executive functions (EFs; Picard, Cousin, Guillery-Girard,
Eustache, & Piolino, 2012; Shum, Cross, Ford, & Ownsworth, 2008) and theory of mind (ToM;
Altgassen, Vetter, Phillips, Akgün, & Kliegel, 2014; Perner, Kloo, & Gornik, 2007). Executive
processes are thought to play an important role in EM and PM by guiding the encoding and
retrieval of target details in the face of interference from competing information (Picard et al.,
2012; West, 1996). The reason for the link between ToM and memory is controversial, but one
possibility is that ToM tests index the capacity for mental self-projection needed to recall the
past and imagine the future (Buckner & Carroll, 2007).
Episodic and Prospective Memory in Children Born VP/VLBW
Most investigations of EM in VP/VLBW children have focused on memory span and simple
forms of verbal, auditory and spatial memory rather than complex events; moreover, to the best
of the authors’ knowledge, none have evaluated PM. Studies with infants and toddlers have
revealed impaired performance on habituation and elicited imitation paradigms relative to full-
term comparison groups (Cheatham, Bauer, & Georgieff, 2006; Rose, Feldman, &
Jankowski, 2005). Similarly, school-age VP/VLBW children have been shown to perform more
poorly than full-term peers when remembering name–face associations and spatial location
(Rose & Feldman, 1996), as well as in tests of working memory (Clark & Woodward, 2010),
spatial memory span and recognition memory (Luciana, Lindeke, Georgieff, Mills, & Nelson,
1999), and verbal and visual-spatial memory and learning (Omizzolo et al., 2014). In contrast,
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two investigations have uncovered no reliable impairments on the recall and recognition-memory
tests of the NEPSY (Esbjørn, Hansen, Greisen, & Mortensen, 2006; Korkman, Liikanen, &
Fellman, 1996), while one study observed typical everyday memory as gauged by the children’s
version of the Rivermead Behavioural Memory Test (RBMT-C; Briscoe, Gathercole, & Marlow,
2001), another found that the VP/VLBW children tested equaled the attainments of full-term
children on the Rey Auditory Verbal Learning Test (RAVLT) and the Rey Complex Figure Test
(RCFT; de Amorin, de Castro Magalhãez, Malloy-Diniz, & Campos, 2013), and two others
showed normal recognition-memory performance (Brunnemann et al., 2013; Curtis, Lindeke,
Georgieff, & Nelson, 2002).
With VP/VLBW adolescents and young adults, research has shown typical match-to-sample
recognition accuracy (Curtis, Zhuang, Townsend, Hu, & Nelson, 2006), typical visual and verbal
memory (Rushe et al., 2001) and typical memory for visual paired associates despite MRI
evidence of brain injury in regions underpinning memory (Narberhaus et al., 2009). On the other
hand, one investigation found that the VP/VLBW participants were impaired on the Wechsler
Memory Scale – Third Edition (WMS-III; Aanes, Bjuland, Skranes, & Lohaugen, 2015), while
another revealed difficulties of everyday memory on the RBMT linked with decreased
hippocampal volume (Isaacs et al., 2000).
Recently, Kipp et al. (2015) pointed out that recognition-memory tests might lack the sensitivity
needed to detect memory impairments in VP/VLBW children due to the confluence of
recollection and familiarity. On the grounds that brain injuries associated with prematurity are
likely to afflict hippocampus-based processes (supporting recollection) more than hippocampus-
independent processes (supporting familiarity), Kipp et al. postulated that memory problems in
VP/VLBW participants would largely be restricted to recollection. To test this possibility, they
measured the neural correlates of recognition-memory judgments in VP/VLBW children
compared to full-term controls using event-related potentials (ERPs). Children aged 8 to 10 years
were asked to inspect color pictures of everyday objects before participating in a recognition-
memory task for which the studied objects were intermixed with novel distracters. During the
test phase, ERPs were recorded with a view to evaluating the early mid-frontal old/new effect (a
putative index of familiarity) and the subsequent parietal old/new effect (a putative index of
recollection). Despite no reliable group difference in recognition accuracy being found, the
VP/VLBW group showed a reduction in the magnitude of the parietal old/new effect
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accompanied by normal performance on the mid-frontal old/new effect. These findings are
interpreted as meaning that recollection was impaired among the VP/VLBW children but masked
on the behavioral level by intact familiarity processes. Additionally, a positive correlation
between the size of the parietal old/new effect and gestational age within the VP/VLBW group
suggests that difficulties with recollection are exacerbated among children with greater
prematurity.
The Present Study
In the present study, which relies on behavioral measures rather than ERPs, the aims are
threefold. First, there is a comparison of the performance of VP/VLBW children and full-term
children on a comprehensive set of memory tasks targeting EM and PM. Second, EM and PM
are evaluated within the VP/VLBW group as a function of neurobiological risk factors (i.e.,
illnesses such as intraventricular hemorrhage and respiratory distress that have been linked with
brain injury) and family SES. Third, the relations between memory and cognitive ability are
examined.
In total, two laboratory-based EM tasks and one PM task were administered, all modeled on
procedures used in previous research which were suitable for our target age group. The EM tasks
were designed to capture key characteristics of episodic retrieval and included measures of cued
recall and source memory (Ruffman, Rustin, Garnham, & Parkin, 2001) as well as estimates of
recollection and familiarity (Koenig, Wimmer, & Hollins, 2015), while the PM task assessed
event-based PM (McCaulay et al., 2010). Additionally, parents’ impressions of their child’s
everyday memory capabilities (incorporating both EM and PM) were solicited using a
questionnaire. The participants consisted of 7- to 9-year-olds divided into a VP/VLBW group
and a matched full-term comparison group, all of whom were of average intelligence and
enrolled in mainstream school. The age range of 7 to 9 years was chosen because EM is
developing rapidly during this period (Kipp et al., 2015) and it was decided to focus on children
without obvious co-morbidities because previous research has found that such children
nevertheless exhibit subtle cognitive impairments (Ford et al., 2011; Foulder-Hughes & Cooke,
2003; Kallankari et al., 2015). It was predicted that the VP/VLBW group would perform worse
than the full-term group on the laboratory EM tests (primarily the tests of cued recall, source
memory and recollection), as well as receiving lower parent ratings of everyday memory
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capabilities. Given the dearth of prior research on PM in VP/VLBW children, no prediction was
made regarding whether or not a similar group difference would emerge for PM.
Information about neurobiological risk factors and family SES was used to explore sources of
individual differences in VP/VLBW children’s EM and PM. It is well documented that infants
who experience higher levels of neurobiological risk go on to attain poorer cognitive, behavioral
and neuropsychological outcomes (Curtis et al., 2002; Ford et al., 2011; Landry, Denson, &
Swank, 1997; Taylor, Klein, Schatschneider, & Hack, 1998). Moreover, a recent study with
young adults found severity of neonatal illness to be associated with worse memory (Aanes et
al., 2015). Conversely, it appears that the cognitive development of VP/VLBW children is
advantaged if they grow up in higher-SES households (Patrianakos-Hoobler, Msall, Marks, Huo,
& Schreiber, 2009), consistent with evidence that the greater levels of cognitive stimulation and
responsive parenting offered by higher-SES homes can stimulate brain maturation (Noble,
Houston, Kan, & Sowell, 2012). In the present study, a neurobiological risk score was derived
for each participant based on his or her medical history (Curtis et al., 2002; Ford et al., 2011) and
SES was gauged in terms of family income. It was hypothesized that memory functioning would
show negative correlations with neurobiological risk and positive correlations with SES.
Tests of verbal and non-verbal skills, EF and ToM were administered in order to see whether any
memory impairments in the VP/VLBW group were linked with the wider cognitive profile.
Given the substantial contribution of domain-general processes to memory performance in full-
term children, it was expected that there would be poorer EM and PM among children who
scored lower on the cognitive measures.
Method
Participants
The VP/VLBW Group
Potential participants who were very (or extremely) preterm and/or very (or extremely) low birth
weight (VP/VLBW) were identified from the database of the Growth and Development Unit at
the Mater Mothers’ Hospital, Brisbane, Australia. This database lists all VP/VLBW babies born
at the hospital, together with the contact details of parents/caregivers who consented to be
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approached in relation to future research projects on their child’s development. To be eligible for
our study, participants had to be aged 7 to 9 years, enrolled in mainstream school, free from
known physical or neurological disabilities, and still living in Brisbane. All children had a
general development quotient (GQ) of > 85 when assessed at 4 years of age on the McCarthy
Scales of Children’s Abilities.
A total of 44 families were contacted about the study (a child’s movie voucher to the value of
A$12 was offered as incentive) and recruited 35 children whose parents gave written consent for
them to participate (17 males and 18 females, 10 7-year-olds, 19 8-year-olds, and 6 9-year-olds).
These children ranged in gestation from 24 to 32 weeks (M = 27, SD = 2.18) and in birth weight
from 598 g to 1290 g (M = 893, SD = 185.44). A total of 15 children were extremely preterm (<
28 weeks) and ELBW (< 1000 g), while 8 children were extremely preterm (< 28 weeks) and
VLBW (< 1500 g), 6 children were very preterm (28 to 31 weeks) and ELBW (< 1000 g), and 4
children were very preterm and VLBW (< 1500 g). A further 2 children were mildly preterm (32
weeks) and ELBW (< 1000 g).
The Full-Term Comparison Group
Full-term participants were recruited through primary schools and afterschool care centers in the
Brisbane region by placing advertisements in school newsletters and offering a child’s movie
voucher to the value of A$12 as incentive for participation. A total of 37 participants were
recruited whose parents gave written consent for them to participate (18 males and 19 females, 9
7-year-olds, 16 8-year-olds, and 12 9-year-olds), all born after 37 weeks or more gestation and
with a birth weight of at least 2500 g.
The two groups were equivalent in terms of age (VP/VLBW M = 101.0 months, SD = 7.5; full-
term M = 101.5 months, SD = 8.7), t(70) = −0.27, p = .79, gross family income (VP/VLBW:
M = A$118,306, SD = 60,157; full-term M = A$136,000, SD = 55,614), t(70) = −1.20, p = .23,
and parental education, χ2 = 5.16, p = .27. In the VP/VLBW group, there were 7 parents with
postgraduate degrees, 9 parents with bachelor degrees, 19 parents with diploma-level further
education, 17 parents who completed Year 12 or equivalent, and 15 parents who advanced no
further than Year 10 (missing data = 3). In the full-term group, there were 9 parents with
postgraduate degrees, 14 parents with bachelor degrees, 18 parents with diploma-level further
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education, 17 parents who completed Year 12 or equivalent, and 6 parents who reached Year 10
(missing data = 10).
Materials and Procedure
The study was approved by the Human Research Ethics Committees of Griffith University and
the Mater Hospital and was conducted in compliance with the guidelines issued by the National
Health and Medical Research Council of Australia. Parents were asked to complete a
questionnaire on their child’s everyday memory capabilities, which was posted to them along
with the information sheet, consent form, and a questionnaire regarding family demographic
details (gross income and parents’ educational qualifications). Children were tested individually
in a quiet room at the university’s Psychology Clinic, their school, or an afterschool care center.
The test sessions lasted 90 to 120 minutes, including a rest break, with the tasks administered in
the same order for all children (see the Appendix).
Episodic Memory (EM)
EM was assessed using two laboratory tasks; the first involves tests of cued recall (a measure of
recollection) and source memory (a measure of children’s ability to remember item–context
bindings) and the second is designed to estimate the relative strength of recollection and
familiarity processes.
Cued Recall and Source Memory
In the first EM task, the video “Some Dogs Do” (narrated by Kevin Whately) was downloaded
from YouTube and presented to children on a laptop computer. The video lasts around 6 minutes
and tells the story of a dog named Sid who discovers that he can fly. Sid’s school friends and
teacher don’t believe his story and insist that “dogs don’t fly”, but when Sid returns home from
school his father reveals that he can fly too and the story concludes with Sid flying above his
house with his father. After watching the video, the children were informed by the researcher
that the video does not tell the whole story and that she will now recount more about Sid’s
adventures. After listening to her brief narration (see the Appendix), a retention interval was
introduced by asking children to complete other activities in the test battery for around
30 minutes. Finally, the researcher would remind the children about the video they had watched
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before conducting a memory test that comprised twenty cued-recall questions (e.g., “What color
was Sid’s house?”), followed by eight source-memory questions (e.g., “When Sid got home, his
mum gave him a lollipop to cheer him up. Did you see that happen in the video? Yes or no?”).
Four questions targeted details presented in the video and four questions targeted details
conveyed in the narrative. Prior to the source-memory questions, the researcher reminded the
children about the two potential origins of the story details: “For each of the things I say next, try
to remember whether you saw it happen in the video or whether you heard about it later when I
read it out to you”.
Recollection and Familiarity
The second EM task uses the Process Dissociation Procedure (PDP: Jacoby, 1991) to estimate
the strength of recollection and familiarity processes. In the PDP, participants are requested to
study two distinct sets of stimuli before performing successive recognition-memory tests in
which the studied items are intermixed with novel distracters. In the initial test they are asked to
endorse items from either studied set (the inclusion condition), whereas in the subsequent test
they are asked to endorse items from one set while rejecting items from the other set
(the exclusion condition). Because noetic and autonoetic processes operate in unison in the
former case but oppose each other in the latter, the results of the inclusion and exclusion
conditions can be used to yield separate estimates of recollection and familiarity.
Study and test stimuli for the PDP were presented using PowerPoint on a laptop computer.
During the study phase, children viewed 24 black-and-white pictures of objects and animals
(drawn from Snodgrass & Vanderwart, 1980). Specifically, 12 pictures were displayed against a
plain yellow background and 12 pictures were displayed against a background of rainbows. To
encourage children to look carefully at the pictures, they were asked to identify each item and
state where they would usually find such an object or animal. After a retention interval of around
15 minutes, children participated in the inclusion test. They were shown a PowerPoint
presentation comprising a series of 48 pictures (24 studied pictures and 24 distractors, presented
in a random order), all displayed on white backgrounds. It was made clear to children that some
pictures would be identical to those they had studied earlier whereas other pictures would be
novel. Children were asked to respond “yes” or “no” to each picture to indicate whether they
remembered seeing it during the study phase.
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After a further retention interval of around 15 minutes, the exclusion test was administered.
Children were shown a PowerPoint presentation with the same 48 pictures from the inclusion test
but this time arranged in a different random order. They were advised that they would be seeing
the same pictures again but that this time they would be asked to recall whether or not each
picture had been presented originally on a yellow background. It was made clear to children that
they should respond “yes” only if they were certain that a particular picture had been presented
on a yellow background and that they should respond “no” if they thought that the picture had
been presented on a background of rainbows or, alternatively, that it was one of the pictures not
presented at all during the study phase. As each slide was presented the experimenter asked:
“Was this picture on a yellow background the first time you saw it—yes or no?”.
Following Jacoby (1991), separate scores were calculated for recollection and familiarity.
Recollection was calculated as the proportion of “yes” responses to pictures with a background
of rainbows in the inclusion test minus the proportion of “yes” responses to the same pictures in
the exclusion test. Familiarity was calculated as the proportion of “yes” responses to pictures
with a background of rainbows in the exclusion test divided by 1 minus the recollection score.
Prospective Memory (PM)
Based on the protocol devised by McCaulay et al. (2010), children were advised at the start of
the test session that they had the opportunity to earn points that could be traded in for stickers at
the conclusion of testing. Specifically, they were informed that whenever the researcher said,
“Let’s try something different” (i.e., the PM cue), they could earn a sticker simply by saying,
“Give me a point!” (i.e., the PM response). To ensure that children understood the instructions
and were confident in producing the response, the PM procedure was practiced at least once prior
to the start of testing. That is, the researcher asked, “Now, what are you supposed to do if you
hear me say ‘Let’s try something different’?” (before prompting the desired response, if
necessary, and providing additional practice). Finally, children were allowed to inspect the sheet
of stickers to increase their motivation for the task. The four cues were interspersed throughout
the test session, beginning around 15 minutes into the session and always at least 20 minutes
apart to discourage rehearsal of the task in working memory and thus tax genuine PM rather than
vigilance. The maximum possible PM score is 4.
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Everyday Memory
Parents were asked to complete the Parent Memory Questionnaire (PMQ; Kadis, Stollstorff,
Elliot, Lach, & Smith, 2004), a 28-item Likert scale measure with half of the items phrased
positively and the remainder phrased negatively comprising questions about their child’s ability
to remember information and events in the context of everyday routines (these questions target
various aspects of everyday memory, including EM, PM, working memory, factual knowledge,
and memory for names and faces). The scores for all items range from 0 to 4, leading to a
maximum possible score of 112.
Verbal and Non-verbal Ability
Verbal and non-verbal abilities were assessed using the Wechsler Intelligence Scale for Children
– Fourth Edition, Australian Standardised Edition (WISC-IV; Wechsler, 2005). The children
completed two subtests: the Vocabulary subtest (from the Verbal Comprehension Scale) and the
Matrix Reasoning subtest (from the Perceptual Reasoning Scale).
Executive Function (EF)
EF was measured in terms of working memory and inhibitory control. Working memory was
assessed using the Digit Span Backward subtest of the WISC-IV Australian Edition (Wechsler,
2005). Inhibitory control was gauged using a computer-based version of the Happy/Sad Stroop
Task (Lagattuta, Sayfan, & Monsour, 2011) during which children were shown a series of
schematic faces on the computer monitor, each with either a happy or a sad expression. During
the first phase of the task (the warm-up), they were asked to press the “happy face” key on the
keyboard whenever they saw a happy face (indicated by a sticker showing a happy face), or the
“sad face” key on the keyboard whenever they saw a sad face (indicated by a sticker showing a
sad face). A practice session of five faces was followed by 80 test trials (presented in random
order), which children were asked to complete as quickly and accurately as possible. During the
second phase of the task, used to assess inhibitory control, response contingencies were reversed
such that children were asked to press the “sad face” key whenever a happy face appeared and
the “happy face” key whenever a sad face appeared. Once again they had a practice session with
five faces before being asked to complete 80 test trials (in random order) as quickly and
accurately as possible. Their performance was gauged in terms of errors and reaction times.
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Theory of Mind (ToM)
ToM was assessed using four false-belief tests comprising two standard false-belief tests (stories
1 and 5 from Liddle & Nettle, 2006) and two higher-order false-belief tests (the ice-cream-van
story from Perner & Wimmer, 1985, and one story of the authors’ own devising) (see the
Appendix). Additionally, children were presented with seven stories (specifically, stories 1, 2, 4,
5, 6, 9, & 10) from the child version of the Faux Pas Test (Baron-Cohen, O’Riordan, Jones,
Stone, & Plaisted, 1999). For each story, children were questioned to ascertain whether they
detected the faux pas (pass = 1, fail = 0) and identified the false belief leading to the faux pas
(pass = 1, fail = 0). They received a score out of 4 for false-belief understanding and a score out
of 14 for accuracy on the Faux Pas Test.
Data Analysis
All children completed all laboratory tests apart from one full-term child who failed to complete
the Matrix Reasoning task due to lack of time. All variables had distributions that were
acceptably normal and all data were retained for the analyses. Given a sample size of 35
VP/VLBW children and 37 full-term children, this study has 80% power to detect an effect size
of 0.67 (α = .05 2-tailed, SD = 1). In total, four sets of analyses were conducted. First, between-
groups t-tests were used to compare the performance of the VP/VLBW children and the full-term
children on the cognitive variables (verbal and non-verbal ability, EF and ToM). Second, a
multivariate analysis of variance (MANOVA) was used to compare the groups for overall
memory functioning, controlling for group differences in cognitive ability as necessary using an
analysis of covariance (ANCOVA). Third, Pearson correlations were used to evaluate memory
and cognitive ability within the VP/VLBW group as a function of neurobiological risk and SES;
in instances where outcomes were predicted by the overall risk score, t-tests were used to
compare the performance of children who did versus did not experience each individual risk
factor. Fourth, Pearson correlations and partial correlations were used to explore the associations
between the memory and cognitive variables separately for the two groups.
Results
Table 1 shows descriptive statistics of memory and cognitive ability for each group. The results for the Vocabulary subtest, the Matrix Reasoning subtest and working memory (Digit Span
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Backward) are standard scores (with a mean of 10 and an SD of 3 in the general population). Results for inhibitory control (from the Happy/Sad task) are response latencies (RTs) in milliseconds and errors. The results for the ToM tests are raw scores (maximum possible scores: False Belief = 4, Faux Pas = 14). Of the memory measures, the results for everyday memory (from the PMQ) are raw scores (maximum possible score = 112), and the results for recollection and familiarity (from the PDP) are the scores derived by the Jacoby (1991). The results for the remaining tests are proportional accuracy.
{Table 1. Group Means and SDs on the Memory and Cognitive Measures}
Group Comparisons of Cognitive Ability
Verbal and Non-verbal Ability
The two groups showed equivalent non-verbal ability, t(69) = −0.09, p = .93, ηp2 = .00,
Cohen’s d = 0.03, but the full-term children outperformed the VP/VLBW children in terms of
verbal ability, t(70) = −3.98, p < .001, ηp2 = .19, Cohen’s d = 0.87. Nevertheless, the VP/VLBW
children achieved average levels of vocabulary relative to normative data.
Executive Function (EF)
RTs and errors on the Happy/Sad task were converted to z-scores and averaged to create a
composite score for inhibition (VP/VLBW group: M = 0.07, SD = 0.63; full-term
group: M = −0.07, SD = 0.69). Although EF performance was marginally better in the
VP/VLBW children, the group differences were not significant: Working Memory:
t(70) = 0.29, p = .77, ηp2 = .00, Cohen’s d = 0.19; Inhibition: t(70) = 0.92, p = .36,ηp
2 = .01,
Cohen’s d = 0.21.
Theory of Mind (ToM)
Scores for false-belief performance and faux-pas performance were converted to z-scores and
averaged to create a composite score for ToM (VP/VLBW group: M = −0.11SD = 0.67; full-term
group: M = 0.10, SD = 0.52). There was no reliable group difference in overall
ToM, t(70) = −1.44, p = .15, ηp2 = .03, Cohen’s d = 0.35.
15
Group Comparisons of Memory
As can be seen from Table 1, the memory tests are of an appropriate level of difficulty with no
floor or ceiling effects. Due to missing data for the PMQ (which was completed by 35 parents in
the VP/VLBW group and 32 parents in the full-term group), results for this variable were
analyzed separately. A between-groups t-test found that parent ratings of everyday memory were
equivalent for the two groups, t(65) = −1.61, p = .11,ηp2 = .04, Cohen’s d = 0.39.
Group differences in memory performance on the laboratory tests were examined using a
MANOVA which revealed a significant overall effect of group favoring the full-term children,
Wilks’ λ = 0.83, F(5, 66) = 2.75, p = . 03, ηp2 = .17. Tests of the univariate main effects indicate
that the full-term group outperformed the VP/VLBW group on PM in particular, F(1,
70) = 6.85, p = .01, ηp2 = .09, Cohen’s d = 0.62. A subsequent ANCOVA found that the group
difference in PM remains reliable after controlling for Vocabulary, F(1,
69) = 4.89, p = .03, ηp2 = .07 (VP/VLBW group Madj. = .45, full-term group Madj. = .69).
Given the VP/VLBW children’s inferior performance on the measure of PM, the results for PM
were examined in detail. There is no evidence that the groups diverge mainly in their responses
to one particular cue; rather, for both groups the proportion of correct PM responses is relatively
constant across the four cues (VP/VLBW group: Cue 1 = .43, Cue 2 = .34, Cue 3 = .49, Cue
4 = .51; full-term group: Cue 1 = .65, Cue 2 = .70, Cue 3 = .73, Cue 4 = .70). Also, most children
responded to at least one PM cue (VP/VLBW group n = 21, full-term group n = 30). Even
among the children who produced a PM response on at least one occasion, the proportion of cues
that were detected in total was reliably lower in the VP/VLBW group than the full-term group
(VP/VLBW group: M = 0.74, SD = 0.28; full-term group: M = 0.86, SD = 0.22),
t(44) = −1.70, p = .047 1-tailed, Cohen’s d = 0.48.
Additionally, the results on the PMQ were inspected solely for items that pertain to PM to see
whether the significant group difference in laboratory PM was replicated in everyday PM as
reported by the parents. Three questions are identified as relating to children’s success in
remembering to carry out an intention in the future: (Q4: “My child remembers to tell people
things that they had planned to tell them”; Q9: “My child remembers to return things that they
have borrowed”; and Q14: “When my child decides to do something in another room, they can’t
remember what they were going to do once they get there”). A t-test that compared the groups on
16
responses to these questions revealed reliably lower ratings for the VP/VLBW children
(VP/VLBW group:M = 2.78, SD = 0.75; full-term group: M = 3.20, SD = 0.68),
t(65) = −2.39, p = .02,ηp2 = .08, Cohen’s d = 0.59. However, no significant correlation was found
between parent ratings of everyday PM and children’s performance on laboratory PM,
r(67) = .02, p = .87.
Effects of Neurobiological Risk and SES in the VP/VLBW Group
Information regarding the neurobiological risk factors for the VP/VLBW group was gleaned
from their neonatal medical histories by a pediatrician, and information regarding SES (gross
family income) was extracted from the demographics questionnaire (with the information being
supplied by 31 participants). Using the same procedures as previous research (Ford et al., 2011),
the neurobiological risk was estimated according to whether or not the participants had
respiratory distress syndrome (RDS, n = 31), chronic lung disease (CLD, n = 11), were
discharged on oxygen (n = 8), patent ductus arteriosus (PDA, n = 16), periventricular
leukomalacia (PVL,n = 0), ventricular dilation (VDL, n = 0), periventricular hemorrhage
(PVH, n = 9), and necrotizing enterocolitis (NEC, n = 1), along with the number of days on
intermittent positive pressure ventilation (IPPV, M = 7.27, SD = 12.54, range = 0 to 44). A
single score was calculated for neurobiological risk by summing the results for the above
variables (where yes = 1 and no = 0 with regard to the presence of each condition). As the IPPV
variable was continuous, it was converted to a 0-to-1 scale by dividing each child’s score by the
maximum score (i.e., 44 days). The maximum possible score for neurobiological risk was 9 and
the mean score was 2.33 (SD = 1.56).
Neurobiological risk is negatively correlated with gestational age, r(35) = −.66, p < .001, and
birth weight, r(35) = −.43, p = .001, while gestational age and birth weight are positively
correlated with one another, r(35) = .41, p = .02. No significant correlation was found between
neurobiological risk and either chronological age, r(35) = .02,p = .92, or family
SES, r(31) = −.24, p = .19.
Table 2 presents Pearson correlations between (1) overall neurobiological risk and SES, and (2)
outcomes on the measures of memory and cognitive ability. As can be seen, higher SES is
associated with better cued recall, source memory, vocabulary, matrix reasoning, and working
memory. In contrast, higher neurobiological risk is associated with worse PM, vocabulary, and
17
working memory. The negative correlation between neurobiological risk and PM remains
significant after controlling for the Vocabulary subtest, r(32) = −.35, p = .04, and is marginally
significant after controlling for working memory, r(32) = −.33, p = .05.
{Table 2. Pearson Correlations between (1) Neurobiological Risk and Family SES and (2) Memory and Cognitive Ability for the VP/VLBW Group}
The relations between neurobiological risk and PM, the Vocabulary subtest and working
memory were examined further by evaluating mean levels of performance in children who did
versus did not experience each risk factor (Table 3); where possible (i.e., given sufficient
numbers in each subgroup), the results were compared using t-tests. As can be seen, most risk
factors are associated with poorer cognitive outcomes. Children who experienced CLD
performed significantly worse than children without CLD in terms of PM,
t(33) = −2.14, p = .04, ηp2 = .12, Cohen’s d = 0.77, Vocabulary, t(33) = −2.24, p = .03, ηp
2 = .13,
Cohen’s d = 0.81, and working memory, t(33) = −3.70, p = .001, ηp2 = .29, Cohen’s d = 1.33.
Similarly, children who were discharged on oxygen performed significantly worse than children
who were not discharged on oxygen in terms of PM, t(33) = −2.02, p = .05, ηp2 = .11,
Cohen’s d = 0.85, Vocabulary, t(33) = −2.54, p = .02, ηp2 = .16, Cohen’s d = 1.20, and working
memory, t(33) = −3.28, p = .002, ηp2 = .24, Cohen’s d = 1.27.
{Table 3. Descriptive Statistics of Verbal Ability, Working Memory, and PM as a Function of Individual Risk Factors in the VP/VLBW Group}
Relations between Memory and Cognitive Ability in the VP/VLBW Group
Table 4 shows the Pearson correlations between memory (cued recall, source memory,
recollection, familiarity, PM, and everyday memory) and cognitive ability (the Vocabulary
subtest, the Matrix Reasoning subtest, working memory, inhibition, and ToM) in the VP/VLBW
group. Because memory performance was not affected by age, all p values > .05, it was decided
not to partial out the effects of age. Cued recall shows reliable correlations with Vocabulary and
ToM, source memory shows reliable correlations with Vocabulary, Matrix Reasoning and ToM,
recollection shows a reliable correlation with Matrix Reasoning, and everyday memory shows
reliable correlations with inhibition and ToM. However, none of the cognitive variables are
correlated significantly with either familiarity or PM, p values > .05. For comparison purposes,
the analyses were repeated in the full-term group; here, the only reliable correlations are between
18
everyday memory and Matrix Reasoning, r(31) = .54, p < .01, and between everyday memory
and working memory, r(32) = .42, p = .02.
{Table 4. Pearson Correlations between Measures in the VP/VLBW Group}
In cases where two or more cognitive variables are associated with memory in the VP/VLBW
group, their unique contributions were examined using partial correlations. For cued recall, the
results show a unique contribution of Vocabulary after controlling for ToM,
partial r(32) = .48, p < .01, and a unique contribution of ToM after controlling for Vocabulary,
partial r(32) = .52, p < .01. For source memory, there is a unique contribution of Matrix
Reasoning after controlling for ToM, partial r(32) = .51, p < .01, and a unique contribution of
ToM after controlling for Matrix Reasoning, partial r(32) = .42, p = .01. For everyday memory,
there is a unique contribution of inhibition after controlling for ToM, partial r(32) = .35, p = .04,
and a unique contribution of ToM after controlling for inhibition, partial r(32) = .37, p = .03.
Finally, correlates of PM as reported by parents on the PMQ were explored. Whereas everyday
PM is not associated with cognitive ability in the full-term group, p values > .05, it is associated
with inhibition in the VP/VLBW group, r(35) = .57, p < .001.
Discussion
EM and PM were assessed in VP/VLBW 7- to 9-year-olds of average intellectual ability who
were progressing normally in mainstream school; furthermore, the possibility of subtle memory
problems linked with neurobiological risk factors was explored. Overall, the findings suggest
that memory impairment is unlikely to be a salient characteristic of such children. Despite a
significant group difference in global memory performance favoring the full-term group, the
effect was only reliable at the level of individual tests for PM. Whereas PM performance showed
a negative relation with severity of neonatal illness, there was no effect of neurobiological risk
on EM.
Kipp et al. (2015) suggest that EM impairments in VP/VLBW children reflect injury to the
hippocampus and thus could be masked on the behavioral level in tests that emphasize mere
familiarity processes (hippocampus-independent) over the feature-binding processes that
contribute to recollection (hippocampus-dependent). Because in the present study memory tasks
19
specifically designed to tax source monitoring and recollection were used, the lack of reliable
group differences on the individual measures of EM could mean that the VP/VLBW group had
largely not suffered hippocampal damage. This suggestion receives support from the low
incidence of serious neonatal medical events in the present sample (no cases of either PVL or
VDL and only one case of NEC), coupled with the finding that EM performance was unrelated
to the neurobiological risk scores (despite the fact that such scores were predictive of both verbal
ability and working memory). On the other hand, it is possible that the EM tests in the present
study were not sufficiently sensitive to detect impairment, perhaps because the retention intervals
were too short. It has been proposed that much of the information encoded into hippocampal
representations is subject to rapid decay, with the formation of enduring event memories relying
on the transfer of information to neocortical brain regions—a process known as system-level
consolidation (Moscovitch & Nadel, 1998; Winocur, Moscovitch, & Bontempi, 2010). If
hippocampal damage disrupts the processes underpinning memory consolidation then it follows
that evidence of EM difficulties in VP/VLBW children will be hard to find at shorter test delays.
Some researchers have posited that EM development following hippocampal injury might be
subject to compensatory mechanisms (Narberhaus et al., 2009), for example, drawing more
heavily than usual on domain-general cognitive regions (Nosarti & Froudist-Walsh, 2016). Such
a proposal is compatible with the present findings of robust links between EM and the measures
of general ability, EF, and ToM in the VP/VLBW children that are not mirrored in the full-term
children, because it suggests that the involvement of domain-general processes in EM is
augmented for the former group. Episodic retrieval is argued to involve an act of pattern
completion whereby coherent event memories are reconstructed from details distributed over an
extensive network of brain regions (McClelland, McNaughton, & O’Reilly, 1995). Such a
flexible, integrative operation is likely to engage EF and numerous other cognitive processes
(Schacter & Addis, 2007; Wheeler, Stuss, & Tulving, 1997). Additionally, neuroimaging
research has identified an important role of general-purpose structures in EM encoding (Köhler,
Moscovitch, Winocur, Houle, & McIntosh, 1998).
In line with the present results, Briscoe et al. (2001) observed that language ability in VP/VLBW
children is a reliable predictor of their memory as gauged by the RBMT-C. Because the present
study assessed a broader range of cognitive skills, it was possible to show that verbal ability,
non-verbal ability, EF and ToM all have a significant impact on memory function. Interestingly,
20
the strongest influence on memory was ToM, which explained unique variance in cued recall,
source memory, and everyday memory. This finding mimics results from previous research (e.g.,
Perner et al., 2007) but the reasons for the link between ToM and EM are unclear. One
possibility is that measures of ToM are sensitive to the capacity for self-projection, as needed for
mental time travel (Buckner & Carroll, 2007). Alternatively, ToM tests might simply gauge
social processes inherent in the memory paradigms. In the present study, for example, children
might have found it easier to encode and retrieve episodic memories if they considered others’
mental states (i.e., the motivations and feelings of the story characters).
In the context of similar cognitive profiles and EM performance between the two groups, the
finding of a significant discrepancy in PM is striking. On average, the VP/VLBW children
responded to one fewer PM cue than their full-term peers (i.e., a reduction in accuracy of 25%).
Among children who had experienced more severe neonatal illness, PM dropped to near-floor
levels and barely exceeded a response rate of one in four among children with CLD, children
who were discharged on oxygen, and children with PDA. Although neonatal illness similarly
showed a negative association with verbal ability and working memory (see also Clark &
Woodward, 2010), the correlation between illness and PM was not underpinned by either verbal
ability or working memory. Poor PM performance within the VP/VLBW group is apparent
despite the fact that rigorous steps were taken to ensure that all participants encoded and
understood the PM instructions. Indeed, most children responded accurately at least once during
the test session, indicating that they remembered the PM intention, while the group difference in
PM remained reliable even after excluding children who failed to make any PM responses at all.
Although PM was evaluated using only one laboratory procedure, parents’ reports regarding
children’s PM in everyday life (as gauged by three questions on the PMQ) similarly show a
significant advantage for the full-term group. It thus seems reasonable to suggest that the
laboratory test unveiled a genuine weakness of PM in the VP/VLBW children, notwithstanding
the lack of a robust correlation between laboratory-tested and parent-reported PM. Interestingly,
parent-reported PM is predicted by EF, in line with everyday memory as indexed by the
questionnaire as a whole. While this might mean that parents’ perceptions of their child’s
memory were tainted by the child’s general distractibility and powers of self-regulation, this
finding is consistent with an extensive body of research linking EF with both EM and PM (West,
1996; Wheeler et al., 1997). PM in children has been reported as depending heavily on inhibitory
21
control, most likely reflecting the need to divert attention away from current activities in order to
respond to the PM cue when it appears (for a review, see Mahy et al., 2014). Accordingly, the
lack of any significant loading of EF on results for the laboratory PM test could be explained by
the fact that there was no requirement for task interruption. PM cues were delivered instead at
natural breaks in the proceedings after children finished one test and were waiting to start the
next one. Previous research has indicated that the contribution of EF to PM performance is
diminished when children do not need to interrupt an ongoing activity to make their PM response
(Ford, Driscoll, Shum, & Macaulay, 2012).
PM in the VP/VLBW group was unrelated to family SES, unlike the cases of verbal and non-
verbal ability, working memory, cued recall and source memory. In previous research, higher
SES has been linked with a greater frequency of parenting behaviors that foster children’s
cognitive development (for a review, see Hoff, Laursen, & Tardif, 2002). For example, parents
who talk and read more often to their children help to promote vocabulary acquisition (Sohr-
Preston et al., 2013), parents who engage their children more often in responsive, scaffolded
interactions promote EF (Landry, Loncar, Smith, & Swank, 2002), parents who expose their
children to more mental-state language promote ToM (Shatz, Diesendruck, Martinez-Beck, &
Akar, 2003), and parents who encourage their children to recall and discuss events promote EM
(Reese, Haden, & Fivush, 1993). Of course, the lack of impact of SES on PM in the present
sample need not mean that the development of PM is immune to nurture; PM might involve
environmentally-sensitive processes that can be practiced but that are not closely tied to those
parenting behaviors normally indexed by SES.
Neither was PM performance significantly correlated with the measures of EM and cognitive
ability, raising the possibility that PM difficulties following VP/VLBW birth could reflect
damage to a relatively circumscribed brain area. One candidate is the rostral prefrontal cortex
(rPFC) or Brodmann Area 10 (BA10), a region that is activated by a wide variety of PM
paradigms (Burgess, Dumontheil, & Gilbert, 2007) and associated with PM impairment
following brain injury despite no adverse impact on retrospective memory for the intention itself
(Uretzky & Gilboa, 2010). This suggestion could be explored further in future research using
brain imaging and electrophysiological techniques. Neuroimaging studies would help to reveal
whether PM impairments in VP/VLBW children are linked with damage to the rPFC and/or the
hippocampus whereas electrophysiological investigations could be used to pinpoint which stages
22
of PM are most compromised in VP/VLBW children. It has been argued that PM comprises a
series of steps, including (1) forming an intention, (2) maintaining the intention in memory while
engaged in other activities, (3) detecting the PM cue in the environment when it eventually
appears (i.e., the prospective component), (4) retrieving the content of the intention in response
to the cue (i.e., the retrospective component), and (5) executing the desired response at the
appropriate moment (Kliegel, McDaniel, & Einstein, 2000). Given evidence that age-related
improvements in PM reflect development of the retrospective component (i.e., parietal positivity)
more than the prospective component (i.e., the N300, e.g., Zöllig et al., 2007), it would be worth
examining whether the same pattern emerges when comparing the PM of VP/VLBW and full-
term children.
On a behavioral level, PM could be evaluated as a function of a greater variety of EF measures,
including planning and task-switching. Results should also be compared for event-based PM
(i.e., remembering to enact the intention in response to a particular environmental cue, as was the
case in the present study) and time-based PM (i.e., remembering to enact the intention at a
particular time in the absence of visible cues). In clinical groups with memory disorders, such as
schizophrenia patients, it has been reported that time-based PM is more severely impaired
(Shum, Ungvari, Tang, & Leung, 2004), raising the possibility that PM difficulties in VP/VLBW
children could be exacerbated given tasks that require self-initiated responses. Finally, measures
of EM could be augmented with tests of autobiographical memories; that is, enduring episodic
memories that have been retained as part of one’s personal life history. Autobiographical
memories are central to the ability to select and pursue long-term goals and typically they are
recollected with a high degree of specificity (Conway & Pleydell-Pearce, 2000). Cooper,
Vargha-Khadem, Gadian, and Maguire (2011) observed that school-age children with known
hippocampal injury due to neonatal hypoxia/ischemia reported impoverished autobiographical
memories compared to healthy comparison children which are characterized by fewer
spatiotemporal and perceptual details, suggesting that the autobiographical memories of
VP/VLBW children might likewise be compromised.
In summary, memory functioning has been explored in intellectually average VP/VLBW
children focusing on key attributes of EM, as well as a first-time evaluation of PM. Memory is
crucial to the successful performance of a myriad of tasks in everyday life, as well as playing a
vital role in school learning as children strive to acquire academic skills, apply them in the
23
appropriate contexts, form study-related intentions, and organize their time effectively. Given
that this study has a small sample size and uses only one PM paradigm, its novel finding of
impaired PM in the VP/VLBW group warrants further investigation. Future studies that aim to
enhance understanding of the nature and locus of PM difficulties in VP/VLBW children may
eventually lead to the development of interventions designed to support them in using this
important form of memory.
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Appendix
Order of Tests
1. PDP study phase;2. Vocabulary subtest;3. PDP inclusion test;4. PM test 1;5. False-belief tests;6. PDP exclusion test;7. “Some Dogs Do” study phase;8. PM test 2;9. Happy/Sad test;10. Digit Span Backward;11. PM test 3;12. Rest and refreshment break;13. “Some Dogs Do” cued-recall test;14. “Some Dogs Do” source-memory test;15. Matrix Reasoning subtest;16. Faux Pas test;17. PM test 4;18. Sticker collection.
“Some Dogs Do”
Source material: https://www.youtube.com/watch?v=9PBH7lFN_Yc
Post-video summary narrative: Sid the dog lived with his mum and dad. His mum was called Sally and his dad was called Jake. Sid was a brown and white dog and he went to school in a nearby town called Woof Town. One day Sid was running late for school. He hurried out the door—but his mum Sally came chasing after him calling, “Wait, Sid! You forgot your lunchbox!” So she put the lunchbox in his bag and then Sid was on his way. Sid felt very happy as he was walking to school, and to his surprise he started to float up into the air. He was flying! He did some turns and swoops—it was great fun! A huge black bird flew up to Sid and said, “Dogs don’t fly!” “Oh yes they do!” replied Sid. When Sid got to school he couldn’t wait to tell his friends that he could fly—but nobody would believe him! The other dogs tried to get Sid to fly in the school playground but he couldn’t. He even climbed up a tree and jumped off the branch—but instead of flying he just came crashing to the ground. Even Sid’s teacher wouldn’t believe him. “Dogs don’t fly”, she said. When Sid got home he looked very sad and so his mum
34
gave him a lollipop to cheer him up. But Sid didn’t feel happy again until his dad Jake showed him that he could fly too. At the end of the story, Sid started flying above his house.
Cued-Recall Questions:
What color was Sid’s backpack?What color was Sid’s house?What was the name of Sid’s mum?What was the name of Sid’s dad?Please put your hand over your eye to show me where Sid had a brown patch on his face (R/L)What did Sid forget in the morning?What made Sid fly?What color was the bird that spoke to Sid while he was flying?Why couldn’t Sid fly at school?Who were some of Sid’s friends at school?What was the name of Sid’s teacher?There was a picture near the blackboard in Sid’s school. What was on the picture?What was the name of the town where Sid’s school was?When Sid tried to fly at school, what did he jump off?Did Sid fly or walk home from school?What did Sid’s mum give him when he got home?What did Sid play on when he went outside his house?Where was Sid when his father came outside?What did Sid say when his father asked him what the matter was?Who was flying at the end of the story?
Source-Memory Questions:
Sid had a red backpack. Did you see Sid’s red backpack in the video? (Yes/No)
Sid forgot his lunchbox in the morning and his mum had to run after him and give it to him. Did you see that happen in the video? (Yes/No)
Sid lived in a blue house. Did you see Sid’s blue house in the video? (Yes/No)
While Sid was in the air on the way to school, a big black bird flew up to him and said, “Dogs don’t fly!”. Did you see that happen in the video? (Yes/No)
At school, Sid wanted to show his friends that he could fly. He climbed up a tree and jumped off the branch—but crashed to the ground. Did you see that happen in the video? (Yes/No)
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When Sid got home, his mum gave him a lollipop to cheer him up. Did you see that happen in the video? (Yes/No)
When Sid went outside, he played for a while on his swing. Did you see that happen in the video? (Yes/No)
At the end, there were three dogs flying—Sid, his dad, and his mum. Did you see that happen in the video? (Yes/No)
Prospective Memory
PM test 1: “That wasn’t hard, was it? [Pause for response]. Let’s try something different. Come back to the other table with me and we’ll do a new activity.”
PM test 2: “Did you enjoy the story? [Pause for response]. Let’s try something different. I’ve now got a computer game for you to play.”
PM test 3: “You must be tired after that. Let’s try something different. Are you hungry or thirsty? Would you like a break? We can go back to the reception area.”
PM test 4: “You did a good job on those stories. Let’s try something different. Come back to the computer desk and we’ll do another task over there.”
Higher-Order False-Belief Test
Story: Two friends, Hannah and Jack, were sitting in the kitchen at Jack’s house. They were talking and eating biscuits. There were only two biscuits left, so Jack said, “Let’s save these biscuits for later—we can go outside to play and eat the biscuits when we come back.” So, Jack put the last two biscuits in a container and then put the container in the kitchen cupboard. Just then Jack’s mother called him and he had to leave the room for a while. When he got back he didn’t go into the kitchen straight away. Instead, he peeked through the keyhole of the kitchen door to see what Hannah was doing. She didn’t know he was watching her. Hannah opened the cupboard, got out the biscuit container and ate one of the biscuits—leaving only one left. Then she put the container back in the cupboard and sat down at the table. Then Jack came back into the room.
Memory Question 1: Where did Jack put the biscuits?
Memory Question 2: Why did Jack leave the room?
Higher-Order False-Belief Question: How many biscuits does Hannah think that Jack thinks are left in the container?
36
Disclosure Statement
No potential conflict of interest was reported by the authors.
37
Table 1. Group Means and SDs on the Memory and Cognitive Measures
VP/VLBW group Full-term group
M SD M SD
Cued Recall 0.66 0.13 0.70 0.10
Source Memory 0.88 0.17 0.95 0.10
Recollection 0.39 0.18 0.47 0.19
Familiarity 0.94 0.15 0.98 0.08
Prospective Memory 0.44 0.42 0.70 0.40
Everyday Memory 78.77 13.03 84.03 13.76
Vocabulary Subtest 9.97 2.86 12.16 2.10
Matrix Reasoning Subtest 10.86 2.90 10.94 2.97
Working Memory (DSB) 10.91 1.85 10.57 1.77
Inhibition (RTs) 1180.21 305.26 1307.65 575.03
Inhibition (Errors) 7.29 11.04 7.41 6.15
False Belief 2.86 1.03 2.89 0.81
Faux Pas 10.54 2.57 11.76 2.03
Note. DSB = Digit Span Backwards; RTs = reaction times
38
Table 2. Pearson Correlations between (1) Neurobiological Risk and Family SES and (2) Memory and Cognitive Ability for the VP/VLBW Group
Measure Risk SES
Memory Measures
Cued Recall −.09 .53**
Source Memory −.05 .49**
Recollection .08 .08
Familiarity −.05 .23
Prospective Memory −.38* .16
Everyday Memory −.02 .21
Cognitive Measures
Vocabulary Subtest −.34* .52**
Matrix Reasoning Subtest −.05 .41*
Working Memory −.53*** .49**
Inhibition −.18 −.28
Theory of Mind −.20 .33
Note. *p < .05; **p < .01; ***p < .001. Bold font denotes significant correlations.
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Table 3. Descriptive Statistics of Verbal Ability, Working Memory, and PM as a Function of Individual Risk Factors in the VP/VLBW Group
Neurobiological Risk Factors Factor Presence n Vocabulary Subtest Digit Span Backward PM
Respiratory Distress Syndrome Yes 31 10.0 (2.94) 10.71 (1.87) .42 (.42)
No 4 9.75 (2.50) 12.50 (0.58) .63 (.48)
Chronic Lung Disease Yes 11 8.45 (2.77) 9.45 (1.63) .23 (.39)
No 24 10.67 (2.68) 11.58 (1.56) .54 (.41)
Discharged on Oxygen Yes 8 7.88 (1.24) 9.25 (1.83) .19 (.35)
No 27 10.59 (2.93) 11.41 (1.57) .52 (.42)
Patent Ductus arteriosus Yes 16 9.19 (3.23) 10.56 (1.71) .30 (.44)
No 19 10.63 (2.41) 11.21 (1.96) .57 (.38)
Periventricular Hemorrhage Yes 9 9.44 (3.32) 10.11 (2.09) .39 (.42)
No 26 10.15 (2.74) 11.19 (1.72) .46 (.43)
Necrotizing Enterocolitis Yes 1 8.00 (–) 8.00 (–) .00 (–)
No 34 10.03 (2.89) 11.00 (1.81) .46 (.42)
Note. Means are given with SDs in parentheses.
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Table 4. Pearson Correlations between Measures in the VP/VLBW Group
Variables 1 2 3 4 5 6 7 8 9 10 11
1. Age –
2. Vocabulary Subtest .11 –
3. Matrix Reasoning Subtest
.28 .19 –
4. Working Memory .06 .30 .31 –
5. Inhibition .20 .00 .00 .27 –
6. Theory of Mind .05 .52*** .26 .30 .09 –
7. Cued Recall .20 .65*** .29 .20 −.06 .70*** –
8. Source Memory .07 .33* .56*** .17 .02 .49** .55*** –
9. Recollection .16 .09 .37* −.08 .03 .10 .39* .11 –
10. Familiarity .11 .25 .00 −.01 −.08 .23 .23 .16 −.12 –
11. Prospective Memory −.07 .16 .23 .20 −.06 .22 .26 .18 .11 .17 –
12. Everyday Memory .10 .23 −.01 .02 .36* .38* .40* .31 .03 −.12 .02
Note. *p < .05; **p < .01; ***p < .001. Significant correlations are shown in bold.
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