Rev. Neurosci.
2017; aop
Carlos M. Gómez*, Catarina Isabel Barriga-Paulino, Elena Isabel Rodríguez-Martínez,
Ma Ángeles Rojas-Benjumea, Antonio Arjona and Jaime Gómez-González
The neurophysiology of working memory
development: from childhood to adolescence
and young adulthood
https://doi.org/10.1515/revneuro-2017-0073
Received August 23, 2017; accepted September 9, 2017
Abstract: Working memory (WM) is an important cog-
nitive function that is necessary to perform our daily
activities. The present review briefly describes the most
accepted models underlying WM and the neural networks
involved in its processing. The review focuses on how the
neurophysiological mechanisms develop with age in the
periods from childhood to adolescence and young adult-
hood. Studies using behavioral, neuroimaging, and elec-
trophysiological techniques showed the progress of WM
throughout the development. The present review focuses
on the neurophysiology of the basic processes underlying
WM operations, as indicated by electroencephalogram-
derived signals, in order to take advantage of the excellent
time resolution of this technique. Children and adults use
similar cerebral mechanisms and areas to encode, recog-
nize, and keep the stimuli in memory and update the WM
contents, although adults rely more on anterior sites. The
possibility that a functional reorganization of WM brain
processing occurs around the adolescent period is sug-
gested, and would partly justify the high prevalence of the
emergence of mental pathology in the adolescent period.
Keywords: brain oscillations; cerebral maturation; devel-
opment; event-related potentials; working memory.
*Corresponding author: Carlos M. Gómez, Laboratory of Human
Psychobiology, Department of Experimental Psychology, University
of Seville, Calle Camilo José Cela, S/N, E-41018 Sevilla, Spain,
e-mail: cgomez@us.es
Catarina Isabel Barriga-Paulino: Laboratory of Human
Psychobiology, Department of Experimental Psychology, University
of Seville, E-41018 Sevilla, Spain; and Center for Biomedical
Research, Universidade do Algarve, 8005-140 Faro, Portugal
Elena Isabel Rodríguez-Martínez, Ma Ángeles Rojas-Benjumea and
Antonio Arjona: Laboratory of Human Psychobiology, Department
of Experimental Psychology, University of Seville, E-41018 Sevilla,
Spain
Jaime Gómez-González: UGC de Salud Mental, Hospital Virgen
Macarena, Servicio Andaluz de Salud, E-41009 Sevilla, Spain
Introduction
The concept of working memory (WM) refers to the brain
system involved in temporal storage and manipulation of
information. This mechanism makes it possible to perform
complex cognitive functions (such as language, compre-
hension, learning, and reasoning) (Baddeley, 1992). WM
corresponds to a system capable of maintaining a limited
amount of information active for a short period of time (in
terms of seconds) and process this information.
In this review, we focus on the neurophysiology of WM
during development from childhood to adulthood (from
4–5 to 24–25  years old, approximately). This approach
complements excellent reviews about behavioral, struc-
tural, and blood-flow studies related to WM development
(Cowan, 2010; Simmering and Perone, 2013; Constanti-
nidis and Klingberg, 2016; Klingberg, 2016), and other
reviews that concentrate on WM and more tangentially
address the problem of WM development (Baddeley, 2012;
Luck and Vogel, 2013; D’Esposito and Postle, 2015; Eriks-
son et al., 2015; Myers et al., 2017). The neurophysiology
of infants and toddlers’ WM development (see Reynolds
and Romano, 2016, for a review) is not covered by itself,
but as previous stages of development. The behavioral,
cognitive, neuroimaging, and theoretical comments in the
present review are limited to allowing an integration of the
neurophysiology of WM and the behavioral/neuroimaging
windows of WM operations during the development. The
electroencephalographical (EEG) and magnetoencepha-
lographical (MEG) studies expand our knowledge of WM
development due to the excellent temporal resolution
offered by these techniques. In this regard, neuroimag-
ing techniques have difficulties in separating the differ-
ent processing stages of WM operation, such as encoding,
maintenance, recognition, or updating, which occur in
the range of few seconds and subseconds, whereas the
time resolution windows of MEG and EEG can account for
these fast processes.
The broad conceptualization of this central cogni-
tive process makes it difficult to review all the possible
instances. In order to systematize the developmental
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2      C.M. Gómez et al.: Working memory development
issues, the discussion is organized by multicomponent,
constructive operators, and state-based models. In addi-
tion, the present review is limited to the periods of child-
hood, adolescence, and young adulthood.
WM models – their relevance
for WM development
Multicomponent model
Since the emergence of this construct, several WM theo-
ries have been proposed. One of the most extensively
studied, which describes its operations and structure,
is the WM model proposed by Baddeley and Hitch (1974;
recently reviewed in Baddeley, 2012). In this model,
the visual and verbal modalities are explicitly distin-
guished. WM is composed of a main system called the
central executive, which is assisted by two secondary
systems: the phonological loop and the visuo-spatial
sketchpad. More recently, the so-called episodic buffer,
which would make it possible to integrate the infor-
mation from the two slave systems and the long-term
memory (LTM), has been included in the model. Most
of the evidence for this model comes from interference
studies, where any of the model’s compartments can be
interfered with independently by concurrent demand-
ing tasks (Baddeley, 2012).
The central executive is defined as a system of high-
level attention control required in novel situations such
as problem solving, planning, or strategy selection. The
central executive would be able to focus and divide the
attention in order to have control over the current pro-
cesses and interface with the LTM. This component is in
charge of coordinating the attention during tasks with
immediate processing demands, and coordinating infor-
mation between the visual and verbal systems. It is also
important on complex tasks that require simultaneous
multi-task processing.
The phonological loop is responsible for the tempo-
rary storage and processing of verbal and auditory infor-
mation, which can be sustained in the form of memory
signals that spontaneously disappear (in a time frame of
2–3 s), unless it is updated (Baddeley, 1996, 1998).
The visuo-spatial sketchpad is the system responsi-
ble for the temporal retention and manipulation of visual
and spatial information (Logie et al., 1990). This compo-
nent is capable of supporting spatial information, such
as the location of an object, and information about its
visual appearance (Logie, 1995). More recently, the epi-
sodic buffer was added as an element of interconnection
between the other elements. The inclusion of this compo-
nent stems from new data indicating that phonological
and visual information are combined, and it also inte-
grates the information that comes from the LTM, creating
a multimodal and temporally ordered representation of
the current situation (Baddeley, 2012).
Constructive operator theory
An alternative structural theory of WM to the one pre-
sented by Baddeley and Hitch (1974), which was devel-
oped to respond to the ontogenetic evolution of WM,
corresponds to Pascual-Leone (Pascual-Leone and Bail-
largeon, 1994) and includes schemas as central processing
elements (figurative, more related to content, and opera-
tive, more related to processing) (reviewed in Kemps et al.,
2000). This theory also includes the so-called hardware
operators, which would correspond to certain primitive
processing, transversal to the different schemes. From the
standpoint of development, the most important capacity
would be the operational memory, which would increase
by one information unit every 2 years, reaching the capac-
ity of seven at the age of 15.
According to the constructive operator theory, cog-
nitive performance is co-determined by the interaction
between schemas and hardware operators. When an input
is given, a series of schemas are activated, and together
they constitute the ‘field of mental attention’ or WM.
The selection and activation of these schemas depends
on three mechanisms: the M-operator, the I-operator (an
operator of inhibition of the non-relevant schemas), and
the execution schemes (although Pascual-Leone’s opera-
tor theory is considerably more complex and includes up
to 10 operators). The idea of the M-operator, related to the
number of schemas that can be held simultaneously in
the mental attention, presents a certain theoretical reso-
nance to WM models that conceptualize WM as an atten-
tionally activated element of the LTM (Cowan, 1995, see
below).
State-based models
Other alternative WM models are the ‘state-based WM
models.’ These models consider WM as the activation of
semantic, perceptual, or motor LTM representations. The
information stored in the LTM is maintained active, at dif-
ferent levels of intensity, throughout the WM operation.
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In these types of models, attention plays a central role
as a determinant of which elements are activated in
WM, and at what intensities. Cowan (1995) and other
authors (McElree, 2006; Oberauer, 2013) have progres-
sively refined the theory and propose that certain items
can be temporarily activated in the LTM, basically in two
forms: one directly controlled by the focus of attention
(FoA) (with limited capacity), and the other activated in
a portion of the LTM (activated LTM) (with much larger
capacity). Once attention is not focused on some of the
items activated in the FoA, they are transferred to the
activated LTM, where they remain in a latent active state
and can be easily reintroduced into the FoA. This type
of model can be associated with the so-called ‘sensori­
motor recruitment,’ where the activated elements are the
sensory or motor networks that represent the perceptual
object or the motor action (D’Esposito and Postle, 2015).
Attention would play the role of maintaining activated
the representations of recently presented objects that
are important for the completion of the task. Interest-
ingly, representations can also be prospectively activated
in attentional cueing paradigms (where a cue indicates
the location of the next stimulus). This prospective acti-
vation can be observed behaviorally through a reduction
in response times in the cued location, but also through
the presence of the contingent negative variation (CNV)
(Gómez et al., 2007; Gómez and Flores, 2011), suggesting
that (as proposed by theorists of the state-based models)
attention could be a mechanism for keeping elements in
the WM activated. These types of state-based models also
resemble Fuster’s proposal (2007) for WM mechanisms,
where WM would correspond to the activation of sensory
and executive networks. In the same vein, using retrocues
(which are presented after the stimulus set presentation
and indicate the relevant features of the items stored in
the WM for future action), Myers et  al. (2017) proposed
that internal attention, driven by the retrocue, would act
in a similar manner to the biased competition model of
external attention, generating a prioritization of the ret-
rocued item to be recovered.
Baddeley (2012) reported that the difference between
the multicomponent model and the state-based models
(as proposed by Cowan, 1995) lies more in the terminol-
ogy than in fundamental processes. Thus, the control of
the episodic buffer by the central executive would not be
different from the attentional focus on the LTM. At this
point, it is critical to understand how the brain is able to
activate neural representations, and two related tasks that
have contributed to clarifying this topic are the delayed
response task (DRT) and the delayed match-to-sample
(DMTS) task.
C.M. Gómez et al.: Working memory development      3
Neural networks of WM in DRTs
and DMTS tasks
DRTs, introduced by W.S. Hunter at the beginning of the
20th century, are frequently used in the study of WM. In
these tasks, sensory stimulation and motor responses are
separated by a brief period during which sensory infor-
mation must be kept in memory in order to produce the
correct response in the test phase. Several injury studies
revealed that this type of task was a good paradigm to
study the prefrontal functions because deficits in perform-
ing the test were observed in animal subjects with damage
in the prefrontal region (e.g. Goldman-Rakic, 1971).
In the early 1970s, the first recordings were made by
Fuster and Alexander (1971) and Goldman-Rakic (1995)
on neurons of awake monkeys. Using this electrophysi-
ological technique in a DRT, these authors discovered
‘memory cells’ in the prefrontal and temporal cortex that
had high discharge rates during the delay period while the
animal maintained sensory information in the absence of
stimulation.
The ‘recognition memory’ task, also called the DMTS
task, consists of memorizing a stimulus sample at the
beginning of the trial; after a delay period, the same stim-
ulus is presented again in conjunction with other distinct
stimuli (Fuster and Jervey, 1981). The aim of the task is
to recognize and identify memorized stimuli (Löw et al.,
1999). In the trained animal, the sample stimulus (in this
case visual), which appears at the beginning of each trial,
activates an extensive network encompassing the neural
representations of perception and action associated with
the stimulus; both perceptual and motor memories are
activated. In this way, the stimulus excites cells in the
posterior cortex, involved in the processing of the sample
stimulus to be retained, and in frontal areas, related to
the processing of the motor response. An example was
observed by Fuster and Jervey (1982) on a task where the
monkey had to squeeze a lever of a similar color to the one
previously presented. These authors observed a neural
activation in the inferotemporal lobe during the delay
period, which could reach 15 s in duration, suggesting that
these neurons are participating in the memory of the pre-
viously presented visual stimulus. Given that the monkey
had to retain this stimulus during the delay period and
then respond correctly, the network representing the stim-
ulus has to remain active during that period, and, there-
fore, the inferotemporal memory cells are active during
the retention period. In addition, because the stimulus is
an indicator for future action, it selects a motor memory
that activates the prefrontal network while it is being held
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4      C.M. Gómez et al.: Working memory development
in memory (Fuster, 1997). Therefore, the shared activation
observed in the inferotemporal and prefrontal neurons,
using the visual DMTS, reflects the interactions within the
vast memory network of the frontal and posterior cortex
in the visual WM. Thus, it can be postulated that, on this
type of task, the memorandum consisting of a stimulus
to be retained for future action causes the activation of
a large network with two main components: an infero­
temporal network representing the visual memo and a
prefrontal network prospectively representing the motor
response at the end of each trial (Fuster, 1999; Fuster and
Bressler, 2014).
A couple of points should be added to the
neurophysiology of the DMTS: (i) the perceptual neural
representation of the items to be maintained in memory
would be distributed in cortices specialized in processing
these types of stimulus (visual, auditory, somatosensory,
etc.); (ii) the mechanisms for maintaining the items in
WM are still disputed; they could be in the reverberating
activity between prefrontal and specialized cortices, as
suggested by the impairment in WM operation after cooling
the prefrontal cortex (Fuster, 1997) and in which brain
oscillations would be a determinant mechanism (Bressler
and Richter, 2015), or they could be based in molecular-­
synaptic changes that maintain persistent neural activities
in the network (reviewed in D’Esposito and Postle, 2015).
The idea of the synaptic changes related to experience
being ubiquitous in the brain would provide support for
the state-based models of WM.
Human neuroimaging studies have extensively ana-
lyzed neural activation during WM tasks. Frontal, cin-
gulate, parietal, visual, and cerebellar areas have been
described as activated during WM tasks (Cabeza and
Nyberg, 2000). The possibility has been proposed that the
processes related to the maintenance of information are
based on frontal networks and broadly distributed areas
related to the content to be maintained. This notion, pre-
viously suggested by Fuster (2007), has been extended
to humans by studying the effects of transcranial mag-
netic stimulation in control subjects and in patients with
frontal strokes, who lose the capacity to focus attention
and select the maintained items (D’Esposito and Postle,
2015). However, by using multi-voxel pattern analysis,
the idea that content information representation during
WM tasks could be more distributed in the cortex (includ-
ing frontal areas) was recently proposed (Lee and Baker,
2016). By contrast, a recent review (Leavitt et  al., 2017)
examining the electrophysiological and BOLD signals
across the cortex during WM tasks suggested the prefer-
ence for sustained activity to be implemented in prefron-
tal and sensory association cortices.
Behavioral development of WM
Although there is a large amount of literature showing an
increase in WM performance with age (Luciana et al., 2005;
Conklin et al., 2007; Tamnes et al., 2013; Pelegrina et al.,
2015), the present review is focused on the type of WM
models described in the previous section, and more specif-
ically, WM neurophysiological development during child-
hood, adolescence, and young adulthood, rather than in
infancy. The interest in this age stems from the fact that
during the transition from childhood to young adulthood,
there is a second burst of brain and behavioral changes that
are important not only for the maturational understanding
of WM, but also to understand and prevent psychopatholo-
gies that frequently arise at these ages (Paus et al., 2008).
The development of WM can be analyzed through behavio-
ral parameters (obtained from reaction times on the DMTS
and other WM tasks as the N-back) or through the scores
obtained on the Working Memory Test Battery for Children
(WMTB-C), developed by Pickering and Gathercole (2001)
to operationalize the Baddeley and Hitch model, as well
as many other psychometric tests. The Pasqual-Leone WM
model has been studied through the Mr. Peanut test, built
by DeAvila (1974) and Diaz (1974).
WM plays a very important role in the development
of cognition in the child. With regard to the multicom-
ponent model of WM, studies in children from 5–6 to
11–12  years old showed that the greatest increase in the
efficacy of this cognitive function occurs after 7 years of
age (Hitch et al., 1989). Gathercole (1998) states that, after
age 7, the WM resembles that of adults in the organiza-
tion and strategies used. The way to code the retained
information changes during development (Hitch et  al.,
1989; Miles et al., 1996). Young children use the specific
characteristics of objects, such as shape, orientation, and
arrangement of details, but after 8 years of age, the use of
phonological verbal coding is implemented. This mecha-
nism could be an important contributor to the higher effi-
cacy of visuo-spatial WM as age increases. Thus, a crucial
period of developmental change occurs around 7  years
old. Children under 7  years old rely more on the visual
store of short-term memory (to remember materials such
as family photos and nameable objects), and from the age
of 7 onwards, children prefer to rely on the phonological
loop, by recoding the pictorial forms into the associated
spoken names. The increase in the rehearsal rate would
facilitate the increase in the capacity in the phonological
loop and in the verbally recoded visuo-spatial sketchpad
(Gathercole et al., 2004).
The stimuli used in the visuo-spatial tests of the
WMTB-C are selected on the basis of being very difficult
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to recodify verbally because they do not correspond to
namable family objects. On tasks involving such materi-
als, older children and adults maintain confidence in non-
verbal forms of the short-term memory store. The current
understanding about the development of the central
executive and the non-verbally coded visuo-spatial
memory is less advanced than the knowledge about the
development of the phonological loop (Pickering, 2001).
The consistent findings from many studies show that per-
formance on WM tests increases steadily throughout the
childhood years, with performance at 15 years old nearing
the adult level, and the central executive component
reaching maturation later than the other components. It
has been proposed that the processing efficiency of the
central executive improves with age, which would allow
the release of space for the storage of memory items (Case
et  al., 1982). This improvement in the central executive
would facilitate the increased performance in the slave
sub-components. However, particularly on complex tasks
that take a long time to complete, an increase in the time
that a particular item can be maintained in the WM would
be another factor explaining the improvement with age.
This latter aspect can be studied through the DMTS tasks,
which make it possible to control the time duration of the
delay period.
Because WM development studies have focused
largely on the changes taking place within the individual
components of the model, relatively little is known about
the internal structure of the WM system in general, and
whether it changes with age. A natural way to study this
particular aspect is to obtain the pattern of performance
covariation in the different components of the model as
age progresses. A small number of studies have inves-
tigated the relationships between WM components in
children. The data provided by Pickering et  al. (1998)
indicate that between the ages of 5 and 8, the phonologi-
cal loop and visuo-spatial sketchpad are independent
from one another. In a study of 6- and 7-year-old children,
Gathercole and Pickering (2000) reported evidence that
the central executive and the phonological loop were
separable, but moderately associated with each other,
which is consistent with the adult WM model. Short-term
visual-spatial memory, on the other hand, was not dis-
sociable from the central executive function, suggesting
that it cannot represent an independent entity (at least
at this point in development) (see also Wilson et  al.,
1987). Jarvis and Gathercole (2003) evaluated children
between 11 and 14  years of age on complex verbal and
visual-spatial memory capacity, and, at both ages, these
two aspects (whether based on complex capacity or only
on storage measures) were independent from each other.
C.M. Gómez et al.: Working memory development      5
In a confirmatory factorial analysis study with subjects
ranging from 6 to 15  years old, Gathercole et  al. (2004)
found that the structure of a three-multicomponent model
is already present in the youngest group, which is consist-
ent with the different neural networks supporting each of
these components.
The maturational growth in M-capacity, defined as the
maximum number of schemes that can be simultaneously
activated by attentional resources (Pascual-Leone and
Baillargeon, 1994), accounts for evolutionary changes in
cognitive performance, such as language (Johnson et al.,
1989), motor performance (Todor, 1979), and moral judg-
ment (Stewart and Pascual-Leone, 1992). The prediction
of a validated quantitative increase in the WM capacity,
related to age, has been empirically demonstrated. Accord-
ing to Pascual-Leone and Baillargeon (1994), cognitive
development is determined by a gradual increase in one
unit of M-capacity every 2  years, from 3  years of age to
late adolescence. This increase in capacity is one of the
distinctive aspects of the constructive operator theory.
Some studies have suggested that the constructive operator
theory, which considers the M-operator as central to WM
operations, and the multicomponent model of WM, may be
complementary (Kemps et al. 2000). The ­M-operator would
account more parsimoniously for the increase in capacity,
whereas the multicomponent model would more easily
accommodate the structure of WM. In fact, the increase in
capacity with age, the interference in spatial information
coded on the Mr. Peanut test by articulatory concurrent
tasks in older children, and the interference in Mr. Peanut
task performance by a concurrent Corsi Block task at any
age suggest: (i) an increase in available WM space with age
(M-operator) and (ii) the existence of two slave systems
that can interact through the verbal recoding of spatial
information in the phonological loop (multicomponent
model) around the age of 8 (Kemps et al. 2000).
DMTS tasks are closely related to the state-based
models, for instance, in the WM model proposal by Fuster
(2007), where the transient activation of long-term repre-
sentations of items in different sensory cortices is central
to understanding the representational role of WM. With
regard to the study of WM development using DMTS
tasks, the issue about the evolution of the encoding,
retention, and matching (recognition) phases has hardly
been addressed (Paule et al., 1998). The questions about
the changes with age have mostly been related to: (i) how
many items can be held in memory (WM span) and (ii)
how the delay period affects performance (transient atten-
tion span).
Luciana et  al. (2005) analyzed non-verbal tasks,
including a facial recognition memory test and a spatial
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6      C.M. Gómez et al.: Working memory development
delayed response test, in subjects aged 9 to 20. The authors
observed that on the visual recognition test, the perfor-
mance with respect to precision (percentage of correct
responses) did not change with age, indicating that rec-
ognition memory for non-verbal (visual) stimuli seems to
mature early, before the age of 9. On more complex tasks,
such as the spatial delayed response test, which also
includes the recall operation (remembering where the dot
target was displayed), the performance in the group of
older subjects (18–20 years) was significantly better than
in the other age groups (9–10, 11–12, and 13–15  years),
but it was not different from the group of 16–17 year olds.
The latter group performed better than the 9- to 10-year-
old and 11- to 12-year-old groups, but it was only slightly
better than the 13- to 15-year-old group. For the 9–10, 11–12,
and 13–15 age groups, there were no differences in perfor-
mance. Reaction times did not vary between groups when
there was no delay period between stimuli. The same
study also showed that the spatial memory span contin-
ues to improve until adolescence. This study suggests ado-
lescence as an end point for maturation of WM in DMTS
tasks.
Regarding the problem of the transient attention
span, in this same study (Luciana et al., 2005), when two
interval levels between the stimuli (500 and 8000  ms)
were analyzed, the authors observed that the youngest
group of subjects (9–10 years old) was significantly less
accurate in the longer interval (8000  ms) compared to
the other four age groups (which showed no differences
between them), suggesting that the ability to sustain the
target position for long periods of time does not show
developmental changes after the age of 11–12. Therefore,
this study suggests that recall and transient attention
span operations mature later than the recognition function.
The ability to increase the time that items can be held
in WM with age would be explained by the time-based
resource-sharing model, which proposes that attention
must switch from the maintenance to the processing
processes in WM. The increase in processing efficiency
with age would allow more frequent engagement of attention
toward the maintenance operation, thus increasing the
time that items are held in the WM (­Barrouillet et  al.,
2009).
Paule et  al. (1998) carried out a study with children
between 4 and 12 years old using a DMTS-type paradigm
with six different waiting periods (between 1 and 32 s), in
order to determine how normal development affects the
latency of the response, the encoding, and the stimulus
retention. The results showed that response accuracy
increased as the children grew, whereas the variability
decreased with age, with the largest decreases occurring
between 7 and 9 years of age. The rate of decay in preci-
sion, as the delay time increased, was more pronounced
for younger children, indicating worse retention of the
stimulus. In 4-year-old children, precision decreased
by 20% between the shortest delay period (1  s) and the
longest delay period (32  s). Instead, for the 11-year-old
children, during the same delay periods, the decline was
only 3%. Older children were more accurate at recogniz-
ing the correct stimulus in the shortest delay period (1 s)
compared to younger children, indicating better encoding
of the stimulus. These data indicate that there are differ-
ences in encoding and retention of stimuli in children of
different ages; more specifically, younger children appear
to have more difficulty with encoding and retaining
information.
Closely related to WM studies with DMTS tasks are
those that fall under the umbrella of the visual WM. In the
latter concept, the focus is on the retention process rather
than in WM items processing. In the change detection
paradigm, the subject must recognize the change of one
item in an array. This type of paradigm finds a capacity
saturation at around 3 or 4 items (Luck and Vogel, 2013).
Ross-Sheehy et al. (2010) showed that this limit capacity
would be already in place at the age of 10 months. A dis-
cussion of the continuous (resource-sharing models) and
slots models (available discrete WM slots) for WM attained
by the use of this paradigm is not relevant to the present
review (see Luck and Vogel, 2013).
It can be concluded that performance on WM tasks
improves with age (capacity, speed, retention time and
accuracy). Children’s rate of improvement (increase
in accuracy and decrease in reaction times) is greater
at younger ages (Chelonis et  al., 2000). However, as
Simmering and Perone (2013) indicated, the huge
­
variability across tasks and modalities during development
generates difficulties in interpreting the processes underlying
WM. In particular, the variability in WM capacity results
on different tasks is illustrated in tables 1–4 by S­ immering
and Perone (2013). In the opinion of these authors, rather
than regarding capacity as a constitutive factor of WM, it
should be viewed as the result of the interaction between
dynamic systems at the behavioral and cognitive levels
that change during development, with capacity changing
as a by-product of the interaction. In any case, the increase
in capacity and maintenance time with age remains an
important characteristic of WM development (Gathercole
et  al., 2004; Barrouillet et  al., 2009; Cowan, 2010). The
interesting question of how changing higher-order strate-
gies in WM operations (e.g. chunking) would be related to
the increase in WM performance with age is beyond the
scope of the present review.
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Neuroimaging studies of WM
development
The relationship between anatomical and physiological
brain maturation and WM development has been ana-
lyzed through magnetic resonance studies. Neuroimaging
studies using functional magnetic resonance have shown
that similar brain structures are involved in children
and adults during WM operations, but children present
a lower level of activation (Kwon et al., 2002; Klingberg,
2006). Increased activity in lateral areas of the prefrontal
cortex (Brodmann areas 9, 46) was observed during a
visuo-­spatial memory recall task in adults and 5- to 6-year-
old children (Tsujimoto et  al., 2004), indicating that the
areas and characteristics of this activity are similar in
adults and pre-school children. These authors have dem-
onstrated that the lateral prefrontal cortex of pre-school
children is active during the WM process, revealing that,
at 5–6 years of age, this brain structure has already devel-
oped the processing of this important cognitive function.
The performance of 8- to 10-year-old children on a
spatial N-back task activated the same regions observed
in adults, including the right dorsolateral prefrontal and
parietal cortices (Thomas et  al., 1999). Using the same
type of test (a visuo-spatial N-2 back) in subjects between
the ages of 7 and 22, Kwon et al. (2002) observed that the
degree of activation of some areas in the prefrontal and
parietal cortex of both hemispheres increases with age.
In this study, although the task performed was visuo-
spatial, the increase in activation in the left hemisphere
was observed in areas related to the phonological loop, in
particular the Broca area. The authors argued that this is
due to the development of a strategy that allows the verbal
coding of visual information at the age of 7. These observa-
tions revealed that visual and verbal processing, through
mnemonic processes and their neural representations,
develop at the same time during childhood and adoles-
cence, and into young adulthood. Similarly, Klingberg
et al. (2002) and Schweinsburg et al. (2005) observed that
the increase in visual-spatial WM in the 9–18 age period
is correlated with increased activity in frontal and pari-
etal areas, as well as progressive maturation, due to the
myelination of the pathways that interconnect these two
structures.
Focusing only on the development of non-spatial
WM in three age groups (8–12, 13–17, and 18–25 years old),
Crone et al. (2006) observed that the younger group had
lower performance than the other two groups, but no
differences were observed in the ventrolateral prefron-
tal cortex activation patterns (a region associated with
C.M. Gómez et al.: Working memory development      7
the online maintenance of the object). Using near infra-
red spectroscopy during a spatial WM task, an increase
in activity in the dorsolateral prefrontal cortex from 3 to
7 years old has also been observed (Perlman et al., 2016).
Taken together, previous results suggest that the fronto-
parietal-temporal networks, which are crucial for WM
operation in adults, begin to be recruited early in child-
hood (from the age of at least 6).
WM behavioral improvement with age has also been
associated with neuroanatomical changes. The increase
in structural connectivity between frontal and parietal
areas (Ostby et  al., 2011; Vestergaard et  al., 2011) and
inside frontal areas (Zhou et  al., 2014) has been related
to better WM performance. The increase of myelin in the
superior longitudinal fasciculus and the cortical thin-
ning in fronto-parietal areas (probably due to synaptic
pruning) are independent predictors of WM performance
with age (Ostby et al., 2011).
Results seem to agree about the use of similar struc-
tures in children and adults for WM computations.
However, this view must be reconciled with the fact that,
during development, different structures could be partici-
pating in WM. There is some evidence that children would
use some different structures from adults to perform the
WM functions. Goldman-Rakic (1971) injured the dor-
solateral frontal cortex of monkeys in infant and adult-
juvenile ages and subjected them to a DRT task. She found
that small monkeys did the job well, and, interestingly,
monkeys injured in adulthood performed the task with
low accuracy. This implies that, in small monkeys, the WM
task is performed in structures that are not exactly similar
to the dorsolateral frontal cortex. In addition, when the
injured infant monkeys grew, they performed the task
worse than in the infantile stage, probably because the
transfer of the function to the dorsolateral frontal cortex
became problematic due to the previous lesion in this
area. This experiment indicates that the transfer of WM
processes between different brain areas is programmed
and must be executed during the development. The same
argument about different functional brain areas of spe-
cialization can be derived from the work by Crone et  al.
(2006) on an object WM task. They found that the ventro-
lateral prefrontal cortex participated in the maintenance
of items in the WM in both children and adults, whereas
the dorsolateral prefrontal cortex was involved in the
manipulation of items in the WM in children older than
12 and adults. The youngest subjects in the experiment
(8–12  years old) did not recruit the dorsolateral prefron-
tal cortex for item manipulation. This view of different
areas contributing to the WM functions during develop-
ment has also been observed in a decrease with age in the
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8      C.M. Gómez et al.: Working memory development
contribution of the hippocampus to WM, whereas the pre-
frontal cortex becomes more crucial during adolescence
(Finn et  al., 2010). The maturational trend is consistent
with the general view that during development there is
a more distributed processing that becomes increasingly
focused (Durston et al., 2006).
Event-related potentials associated
with WM development
The event related potential (ERP) technique, applied to
understand the cerebral mechanisms of WM process-
ing of information, is useful for making inferences about
the timing and anatomical location of these processes in
memory. The development of WM depends on several pro-
cesses, including the processing of information specific
to each modality, its coding and retention in memory,
the ability to recognize the stored items, and the updat-
ing of the contents in the WM. These processes can be
studied with MEG and EEG, given their excellent temporal
resolution.
Developmental neurophysiology
of the updating process
There are quite a few studies on P300 maturation that can
be interpreted as a developmental index of the WM con-
tent-updating process. Although most of the results have
been obtained using attentional paradigms, the WM state-
based models suggest that the updating of contents in the
WM is a critical aspect in understanding WM operations,
and this updating would have a close correlation with
attentional processes. Therefore, P300  maturation can
be considered an important component in the updating
process. Another type of paradigm in ERPs that could offer
insight on the development of WM sub-processes is the
DMTS and related experimental paradigms. In DMTS-type
tests, components related to the time when the stimulus is
coded, kept in memory (interval between S1 and S2), and
recovered (matching) can be studied. Particularly, aspects
related to the neural signals that make it possible to main-
tain the stored items in the WM, and the negativities asso-
ciated with the matching process, are reviewed here.
The P300 is one of the most complex waves, and it has
been related to different functional properties, including
the updating of WM content. This ERP corresponds to a
late positive component (LPC) that appears around 300 ms
after the presentation of infrequent stimuli (Squires et al.,
1976; Johnson and Donchin, 1982), and its amplitude is
inversely proportional to the probability of the stimulus’
occurrence. Donchin and Coles (1988a) proposed that
the posterior P300 or P3b would represent an operation
of updating the context where the WM operates (Polich,
2007). However, P3b presents alternative interpretations
(Mangun and Hillyard, 1991; Verleger et al., 2005; Polich,
2007; Gómez and Flores, 2011). Polich (2007) proposed
that the P3b component is related to the neuroinhibition
that is necessary to focus attention on the relevant task,
facilitating the action of memory systems without dis-
turbances. In general, a close relationship between the
P300 and WM updating is broadly supported. P3a, the
other sub-component of P300, is generated as the brain’s
response to stimuli that are novel compared to the more
frequent stimulation (Friedman et al., 2001). This compo-
nent would index an attentional reorientation generated
by an unexpected stimulus (Polich, 2007) or a change in
the processing rules (Barceló et al., 2002). Likewise, it has
been proposed that the disconfirmation of the subjective
expectancy about the characteristics of the target stimulus
is related to the generation of the P3a component (Gómez
et al., 2008). Frontal lobe lesions decrease the amplitude
of the P3a, but not the P3b recorded in parietal areas
(Lovstad et al., 2012), indicating a posterior localization of
P3b neural sources. The reduction in P3a after injury is not
only caused by damage in the lateral prefrontal cortex, but
also by lesions in the orbitofrontal cortex (Lovstad et al.,
2012). However, lesions in the temporo-parietal junction
reduce the amplitude of both components. In sum, the
generators of P3a and P3b are rather distributed, but P3a
has a high dependence of the frontal zones and the tem-
poro-parietal junction, whereas P3b does not depend on
frontal areas, but rather on posterior regions (Bledowski
et al., 2004).
One type of paradigm generating a P300 component
that can be linked to the process of WM updating is the
N-back, where the subject has to compare the current item
with previously presented items (N-1 back, N-2 back, etc.).
The study of the process of change in the WM contents
(Wild-Wall et al., 2011) suggests that the N-back task can
be categorized as a dual-task: (i) a WM task related to the
process of updating and (ii) a matching task between the
stored item and the new item (Watter et al., 2001).
However, there is no systematic approach to defining
the developmental trajectories of the P300 during devel-
opment and their relationship with WM (although in some
instances the P300 component has been used to assess
WM updating in children; Evans et al., 2011). Therefore, we
concentrate now on describing how the P300 component
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evolves with age in other types of paradigms, basically in
the ‘Oddball paradigm,’ where a more extensive descrip-
tion has been carried out. This is justified, in the context
of the present review, based on the hypothesis that P300
is related to the process invoked when there is a need to
revise the representations in the WM (Donchin and Coles
1988a,b).
Several studies have analyzed the amplitude and
latency of the endogenous components P3a and P3b
during child development in the auditory modality. Using
the three-stimulus Oddball paradigm (standard, deviant,
and novel stimuli), Määttä et  al. (2005) reported results
from children between 8 and 9  years old and adults
between 22 and 28  years old. These authors reported a
P3a of maximum amplitude in frontal areas in children,
whereas in adults, maximum P3a was found in the central
areas. In another study using the Oddball task, Fuchigami
et  al. (1995) found that the latency of both P3a and P3b
decreased with age, and that P3a matures earlier than
P3b. Oades et al. (1997) replicated the decrease in latency
with age for the P3b component. In general, with regard to
auditory P3b, the most frequently reported general trend
is a reduction in latency and an increase in amplitude
from childhood to adulthood (Segalowitz et al., 2010).
A few studies have analyzed P3  maturation in the
visual modality in children. With a three-stimulus Oddball
task, Stige et al. (2007) analyzed two age groups (6.8–15.8
and 20–88.8  years), and they found that P3a matures
earlier than P3b. They showed that the latency of P3a
increased and the amplitude decreased with age. The P3b
component showed a nonlinear reduction in amplitude
with age. By contrast, Courchesne (1978) found no visual
component P3a in children, but they reported the presence
of P3b. Our group reported the absence of the P3a compo-
nent in children and preadolescents in the visual modality
of two different types of visual experimental paradigms;
(i) odd-ball (Figure 1A) (Rojas-Benjumea et al., 2015) and
(ii) central-cue Posner paradigm (Figure 1B) (Flores et al.,
2009). One possible reason for the discrepancy between
the developmental trajectories of auditory and visual P3a
would be a possible contribution of posterior dipoles situ-
ated in the inferior bank of the Sylvian fissure for the audi-
tory modality, whereas in the visual modality, P3a sources
would be frontally situated. Given the earlier maturation of
posterior cortex areas compared to frontal areas, the pres-
ence of P3a in children and adolescents in the auditory
modality would be justified. With regard to the P3b com-
ponent, Thomas and Nelson (1996) and Van der Stelt et al.
(1998) found a decreased P3b latency and amplitude with
increasing age. Flores et al. (2009), in a central cue Posner
paradigm, showed a decrease in P3b with age (Figure 1B).
C.M. Gómez et al.: Working memory development      9
This decrease in amplitude and latency has also been
found by other authors (Thomas and Nelson, 1996; Van
der Stelt et al., 1998). Rojas-Benjumea et al. (2015), record-
ing a population from 6 to 26 years old, found a decrease
in latency and peak-to-peak amplitude of the P3b compo-
nent. The decrease in amplitude with age in a posterior
positivity, categorized as an LPC, has also been obtained
in DMTS paradigms during the encoding and recognition
phases (Figure 2B) (Barriga-Paulino et al., 2014, 2017).
In conclusion, and given the presence of P3b in chil-
dren of at least 6 years old, it is possible to conclude that
the cognitive function indexed by this component (the
updating of the WM content) is already formed at this age.
However, as most of the studies presented in the present
report indicate, P3b maturation continues during child-
hood and adolescence. The fact that the visual modality
does not present a clear P3a component in childhood and
early adolescence suggests that detection of novelty, a
processing step that precedes WM content updating, must
be assumed, at least partly, by different brain areas in
children and adults.
More detailed experiments based on structural models
of WM, taking into account the evolutionary perspective,
are needed to understand how the different phases of
WM updating (retrieval, transformation, and substitution)
evolve with age (Ecker et  al., 2010; Linares et  al., 2016).
The N-back task would be an excellent paradigm when
combined with EEG or MEG techniques to explore the
updating sub-components and to trace the developmental
trajectories of these sub-processes. The different number
of sub-processes involved in N-1 (substitution) and N-2
(substitution and retrieval) tasks would facilitate to iden-
tify the ERP indices of each sub-process. Other tasks
such as the mental counter task (changing the numerical
values of stored counters upon certain cues) would permit
us to explore the sub-process of transformation. However,
at this point there is no systematic approach of dissecting
these different updating sub-processes with a develop-
mental perspective.
DMTS paradigms for understanding the
developmental neurophysiology of the
encoding, maintenance, and recognition
process
The DMTS task makes it possible to separate the encod-
ing, maintenance, and recognition phases of WM, given
the considerable separation in time between the retained
item (S1) and the recognized item (S2). DMTS and DRT
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10      C.M. Gómez et al.: Working memory development

A B Valid
Time condition
Delay
(82.1%)

Invalid
700 ms condition
Delay
(17.9%)
700 ms
Cue Target Motor Cue
700 ms 300 300 response 300

700 ms
1370 1860
Age groups
Cz 6–9 Children Young adults
P3a FCz
10–13
14–17
18–21
22–26 P3a
Pz Cz P3a

Invalid
10 µV 10 µV Valid
+ +
P7
POz P3b
– –
15 µV 10 µV P3b
P3b
Pz

Oz
O2

S2 S2

0 400 800 0 500 0 500

Time (ms) Time (ms)

Figure 1: P3a and P3b during development.

(A) Above: an example of a trial on the Oddball task. Presentation of a sequence of cartoons where the bee was the frequent standard stimu-
lus and other cartoons were the infrequent novel target stimuli. The subjects had to respond to the novel stimuli. Below: difference waves
obtained by subtracting the ERPs in the standard condition from the ERPs in the target condition. Notice the presence of P3a from the 14- to
17-year-olds to the oldest group, and the presence of P3b in all age groups, although with a higher latency in the youngest group (adapted
from Rojas-Benjumea et al., 2015). (B) Above: the experimental paradigm comprised two conditions, valid and invalid (82.1% of valid trials).
In the valid condition, the cue indicated the spatial position where the visual target appears. In the invalid condition, the target appears on
the opposite side to the cued location. Below: grand average ERPs to the targets in the valid and invalid conditions for children and young
adults. Note the absence of the P3a component in children, whereas the P3b component was already present in children. Adults presented
both the P3a and P3b components (adapted from Flores et al., 2010).

are paradigms that were first designed and developed
to work with animals by means of lesions and invasive
recording techniques (Fuster, 2007), facilitating the possi-
ble interpretations of signals collected with non-invasive
techniques.
The encoding process
Encoding in DMTS paradigms is observed as the typical
succession of ERPs after S1 presentation (Figure 2A for
the experimental paradigm description). In the visual
modality, these components are similar to those obtained
in adults (Hillyard and Picton, 1987), and they are labeled
C1 (the striate component), frontal N1, posterior P1, pos-
terior N1 and P2, anterior N2, and parietal P3 (also called
the LPC for paradigms different from the oddball para-
digms and showing different latencies and/or topogra-
phies from the standard P3). The main difference between
children and adults in this encoding phase is a mono-
tonic decrease in the amplitude of all these components
(Barriga-Paulino, 2014, 2017). The difference in ampli-
tude of EEG and ERPs in children is probably not only
due to different electromagnetic passive properties of the

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 C.M. Gómez et al.: Working memory development      11

A Time Auditory
S2 feedback
2000 ms

Delay Answer
2000 ms

S1 Matching
1500 ms
Retention
1000 ms
Encoding
S2 Auditory
S1 Delay Answer feedback + S1

1000 ms 1500 ms 2000 ms 600 ms 2000 ms 1000 ms

Encoding Retention Matching Encoding

B Encoding Age groups

Cz 6–9
POz P1 Oz
P2 P1 10–13
12 LPC
0 LPC 14–17
8 20 18–21
22–26
4 C1
µV

–10 10 C1
N1
N2 0
0
–20
0 400 1200 0 400 1200 0 400 1200
S1 Time (ms) S1 S1

Retention
Cz Slow wave P8 POz P2 Slow wave
P1
0 Slow wave
10 5
µV

0 0
–6
–10
1200 2400 1200 2400 1200 2400
Time (ms)

C Encoding Retention
6–9 10–13 14–17 18–21 22–26
2 6 –9 10–13 14–17 18–21 22–26
40–60 ms
–2 10
C1 1100–1130 ms
25 –10
100–130 ms P1 offset
–25
N1 P1
20 10
130–160 ms 1160–1230 ms
–20 –10
N2 P2 offset
15
160–230 ms Slow wave
–15 15
P2 2100–2400 ms –15
25 Slow wave
290–400 ms
–25
LPC

Figure 2: Maturation of ERPs during the encoding and delay (retention) phases in a delayed match-to-sample task.
(A) Example of a trial from the delayed match-to-sample paradigm. (B) ERPs observed in the encoding and retention phases for the five age
groups. Time is expressed from S1 onset. The different ERP components are indicated. Note the polarity inversion of the slow wave in the
youngest group: positive in Cz and negative in P8. (C) Topographical maps of ERPs for the encoding and retention phases in the five age
groups (adapted from Barriga-Paulino et al., 2017).

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12      C.M. Gómez et al.: Working memory development
skull (Gómez et al., 2017), but also to differential synap-
tic density (Huttenlocher, 1990; Giedd et  al., 2009). The
psychophysiological meaning of these components goes
beyond the scope of the present review (for a review, Luck
et al., 2000). However, the presence of all the visual ERPs
during the DMTS encoding phase of WM suggests that
visual processing in WM tasks is not qualitatively different
from other cognitive processes in which visual analysis is
needed. For instance, an approach that would be useful
to indicate which visual ERPs are critical for the encoding
phase is the retrospective analysis of visual ERPs in which
a missing or incorrect response is obtained. This approach
has not yet been used during WM development. Another
possible approach would be the correlation of the number
of errors with the amplitude of the visual ERP components
during the development. This approach showed that the
c1, P1, N1, N2 and LPC components were correlated with
errors, and significant correlations were maintained after
controlling for age in the P1, N2, and LPC, indicating the
importance of early (P1) and late processing (N2 and LPC)
ERPs for a correct encoding process.
The negative slow wave during the retention
period
Several ERP studies, using S1-S2 paradigms, have revealed
a negative slow wave (NSW) during the retention period of
the stimulus on WM tasks (Ruchkin et al., 1990, 1992). The
amplitude and brain topography vary depending on the
mode and type of information to be memorized (Barceló
et  al., 1997). The NSW presents greater amplitude in the
left hemisphere during phonological memory operations
(Rugg, 1984a,b) and greater amplitude in the right hemi-
sphere during visual memory operations (Barrett et  al.,
1988). In fact, the latter is the main argument support-
ing the idea that NSW can be associated with mnemonic
processes, rather than unspecific processes, as suggested
by other authors (Luria et al., 2016). This component has
also been found to be sensitive to the difficulty of the task
(Ruchkin et al., 1992), and it appears to present a different
topographic distribution on spatial WM tasks and object
memorization (Ruchkin et al., 1997).
The memorization of visual material is generally asso-
ciated with a centro-posterior negativity (Patterson et al.,
1991; Ruchkin et  al., 1992). More specifically, memoriza-
tion of one object has been related to great negativity in
the fronto-medial area (electrodes F3, Fz, F4) during the
retention period (Mecklinger and Pfeifer, 1996). However, a
study carried out by Löw et al. (1999), using a visual DMTS
task, showed that after the presentation of S1, a slow wave
with a duration of 500 ms predominated in the right poste-
rior area. In addition, Ruchkin et al. (1997) reported a slow
posterior negative wave on a WM task. According to these
studies, the posterior activity observed on tasks involv-
ing visual stimuli and retention of information about the
object suggests that the coding and storage of the stimulus
characteristics activate posterior cortical networks. Based
on several investigations, Berti et al. (2000) suggest that
frontal activity might reflect motor control or preparation
processes, whereas slow negative potentials observed in
the parieto-occipital area would reflect activity related to
the storage of the stimulus. This NSW could be the mac-
roscopic counterpart of the sustained activity observed
in single cells recorded in the same types of paradigms
(Goldman-Rakic, 1995; Fuster, 2007).
Using a DMTS paradigm in a sample of subjects from 6
to 26 years old, we observed an NSW in the posterior region
during the retention period of the memory stimulus. The
NSW was already present in the youngest subjects. The
NSW was extended to more central areas in older sub-
jects (Figure 2B and C) (Barriga-Paulino et al., 2014, 2017).
In fact, a slow positive wave in the anterior region was
observed in younger children, becoming extinct with age
and resulting in negativity in adults.
Dipole analysis, using the brain electrical source
analysis program, showed that only two posterior located
dipoles are needed to explain almost all brain activity
during the retention period in children. However, the
adults needed two extra dipoles situated in more ante-
rior locations to explain the scalp topography during the
retention period. This result shows that children recruit
posterior brain resources to maintain the memory foot-
print in the WM (Jonkman et  al., 2003), and adults also
use anterior resources, indicating that children and adults
share the same neurophysiological mechanism during the
stimulus retention period (slow waves), but they use the
recruited brain areas with different intensities at different
ages. Neuroimaging studies have found the activation of
frontal areas in WM paradigms in children (Kwon et  al.,
2002; Tsujimoto et al., 2004; Klingberg, 2006). Based on
this, the possibility that this positive frontal side of the
NSW is not due to the positive side of posterior dipoles
should be acknowledged; and the positive frontal side
of the NSW in children may represent activity in frontal
areas. In fact, the regression with age of the neural
sources of the ERPs during a DMTS task (including the
retention period), as computed with LORETA (Pasqual-
Marqui, 2002), has shown that there is a displacement of
the intensity of neural sources from posterior to anterior
regions with age (Barriga-Paulino, 2015b). Along these
lines, not only a different level of activity in anterior and
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posterior areas in children and adults would occur, but
also and in order to explain the different polarity of frontal
NSW at different ages, a different organization of cortical
layer activation in frontal areas compared to posterior
areas may be acknowledged in childhood with respect to
adulthood, explaining the different polarity of sustained
slow waves at different ages (Bender et al., 2005). In fact,
other negativities, such as the CNV (Bender et al., 2005)
and the Bereitschaftspotential potential (Chiarenza et al.,
1983), found a posterior negativity and an anterior posi-
tivity during development, which becomes a negativity in
frontal sites as age progresses.
In the same study (Barriga-Paulino et al., 2014), a close
relationship was found between slow-wave amplitude
and behavioral performance on the three WM components
(central executive, phonological loop and visuo-spatial
sketchpad) measured with the WMTB-C during the devel-
opment, indicating that the functional role of the NSW
may not be exclusively associated with the DMTS test, but
rather with the construct of WM in a broader sense.
An ERP component that can be related to the NSW is
the so-called contralateral delay activity (CDA) (McCol-
lough et  al., 2007). Using a variation of the DMTS para-
digm (where subjects visualized stimuli in both visual
hemifields, but only the items in one of the hemifields
had to be remembered), a negativity in the contralateral
hemifield to the item to be memorized can be recorded
by subtracting the ipsilateral activity from the contralat-
eral electrodes. This negative wave presents a posterior
topography, with maximum amplitude at posterior sites
(Woodman and Vogel, 2008), and an increase in ampli-
tude with the number of stimuli stored, suggesting that it
is related to the process of maintaining the stored items
active in the WM during the delay period. Given the nega-
tive polarity and the posterior distribution of the CDA, it
can be considered to have a similar functional role to the
NSW during the retention period. Regarding the develop-
mental trajectory of the CDA, it has not yet been traced,
and the component is described in limited samples of
children and adolescents (Sander et al., 2011; Spronk et al.
2013).
Selection negativity during the stimulus
recognition phase
The matching or recognition phase of the DMTS task cor-
responds to the active search for correspondence between
the stored item maintained in memory and the presented
items during the recognition phase. The selection nega-
tivity (SN) consists of an endogenous potential related to
C.M. Gómez et al.: Working memory development      13
attention that arises in a stage of selective attention and
information processing (Hillyard and Anllo-Vento, 1998).
The stimuli selection based on non-spatial features (such
as shape or color) elicits the SN, which begins between 140
and 180 ms post-stimulus and persists for another 200 ms
or more (Hillyard and Anllo-Vento, 1998). SN is thought to
reflect the selection of relevant features at an early level of
information processing (Wijers et al., 1989). For the SN to
be elicited, the representation of the selected feature must
be in an active state to permit the matching process. SN
is best observed in difference waves, where the potentials
elicited by a stimulus with unattended features are sub-
tracted from the potentials elicited by the same stimulus
when these features are attended. Thus, the increase in
this posterior negativity for stimuli with attended fea-
tures versus unattended features has been associated
with the identification and categorization of the stimulus,
which involves comparison with representations stored in
memory (Eimer, 1994).
With regard to the development of the SN, the study
of selective attention to colors, carried out by Van der Stelt
et al. (1998) with subjects from 7 to 24 years old, showed
an SN distributed by the occipital, temporal, and parietal
regions in the latency range of 150–300 ms. This negativ-
ity was more visible in subjects from 19 to 24 and 16 to
18 years old, and less visible for subjects from 13 to 15 and
10 to 12 years old.
Another negative component related to the process
of selecting one stimulus surrounded by distractors is
the N2 posterior contralateral (N2pc) component. The
deployment of attention to an object in a hemifield pro-
vokes an inter-hemispheric imbalance of activity between
the contralateral and ipsilateral posterior visual areas.
This cortical imbalance is measured (between 200 and
300  ms post-stimulus onset) by subtracting the ERPs in
the ipsilateral hemisphere to the hemifield where the item
to be selected appears from the ERPs in the contralateral
hemisphere (Luck and Hillyard, 1994). The N2pc presents
a posterior scalp distribution with maximum amplitude
around electrodes PO7 for targets presented in the right
visual field (RVF), and PO8 for targets presented in the left
visual field (LVF). Neural generators of this component
have been obtained in the extrastriate visual cortex, with
parietal contributions (Hopf et al., 2000). The presence of
the N2pc component in the matching phase of the change
detection paradigms suggests that the process of noticing
the difference between the new input and the stored item
is very similar to the selection process indexed by the N2pc
component (Hyun et al., 2009). The obtained contralateral
SN and N2pc would be considered the macroscopic coun-
terparts of the results obtained by Chelazzi et  al. (1993,
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14      C.M. Gómez et al.: Working memory development

2001), which showed an increase in neuronal activity in
the temporal cortex of monkeys coding for the selected
item presented on the contralateral side during the match-
ing phase. The N2pc related to object selection seems to
already be operational in the 9- to 12-year-old group,
presenting a slightly higher peak latency than in adults
(Couperus et  al., 2015). Meanwhile, during the encod-
ing and maintenance phases, there also seems to be an
N2pc component in children (by using cues and retrocues,
respectively) (Shimi et al., 2014, 2015). N2pc latency was
longer in children than in adults, and, interestingly, chil-
dren who presented N2pc more similar to adults also pre-
sented greater WM capacity. These latter results indicate
the importance of the selective mechanisms, indexed by
N2pc, in prioritizing the encoding of certain items in WM.
A DMTS experiment where the target to be remem-
bered appeared in the center of the screen, and after a
delay period, two different stimuli appeared in the left
and right visual hemifields (Figure 3A and B), recorded a
lower positive potential in the hemisphere contralateral
to the hemifield where the stimulus to be matched was
presented. A negative potential, with similar latency to
the SN, was obtained in the contralateral hemisphere
(Figure  3E–G) when the ERPs were subtracted (as indi-
cated in Figure 3A–D) (Barriga-Paulino et  al., 2015a).
This contralateral negativity (Figure 3E–G), analyzed in a
population between 6 and 26 years old, was obtained in
the difference waves of the ERPs (in electrode P7) induced
by the display where the target stimulus appeared in the
right visual hemifield minus the induced ERPs when the
target stimulus appeared in the left visual hemifield (and
vice versa for P8). It was characterized as an SN because
the protocol to obtain it was more similar to the one used
to obtain the N2pc. However, this SN may share some
common characteristics with the N2pc.
This contralateral negativity to the relevant stim-
ulus showed a tendency to decrease in latency and
increase in amplitude with age. In fact, the duration of
this component was longer in children than in the other
age groups (Figure  3E–G). These effects represented

A B
Time Auditory Time Auditory
S2 feedback feedback
2000 ms 2000 ms
Delay Answer Delay E F
2000 ms 2000 ms 6 7 8 9 years old
Matching Matching 6 7 years old
S1 S1
1500 ms 1500 ms 10 11 12 13 years old 8 9 years old
Retention Retention 14 15 16 17 years old 10 11 12 13 years old
1000 ms 1000 ms 18 19 20 21 years old
Encoding Encoding
22 23 24 25 26 years old

C D 5 5
P7 P7
ERPs in electrode P7 Difference wave (B-A)
SN + SN
+
0 0
µV
µV

+ + SN – –
µV

µV

– S2 – S2
S2 S2
–5 –5
0 Time (ms) 0 Time (ms) 0 1000 (ms) 0 1000 (ms)

G
6–9 years old 10–13 years old 14–17 years old 18–21 years old 22–26 years old

CSD

0.02 µV/cm2

Figure 3: Maturation of the selection negativity (SN) during the recognition (matching) phase.
(A, B) Example of trials from the delayed match-to-sample paradigm used in the experiment. (C) Schematic representation of the ERPs obtained
in P7 when the relevant stimulus appeared on the left and on the right of the screen. (D) The SN obtained from the difference waves (left-pre-
sented target minus right-presented target). (E) Difference waveforms of ERPs obtained from RVF stimulation minus LVF stimulation for the five
age groups in electrode P7 during the recognition of the target stimulus. (F) Same as for (E), but for the three youngest age groups. Note that the
SN extends over a longer time in the youngest age groups. (G) Current source density maps for SN of the five groups in the 150–250 ms tempo-
ral window after the S2 onset. Note the current sink over the P7 electrode in the five age groups. The anterior sinks are not discussed because
they may have presented contamination from eye dipoles (adapted from Barriga-Paulino et al., 2015a).

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neurophysiological evidence about the greater effec-
tiveness of the visual selection processes in the transi-
tion from childhood to adolescence (Van der Stelt et  al.,
1998). The results suggest that children, adolescents, and
young adults use the same mechanism and brain areas
(contralateral parietal negativity, categorized as an SN)
to identify and select the recognized stimulus; however,
children spend more time on this process, possibly due to
the typical immaturity of neural structures.
Relationship of ERPs and behavioral
­maturation in DMTS tasks
In addition to the NSW and the SN, a series of ERPs appear
in the encoding, retention (delay), and recognition (match-
ing) phases (Figure 2B and C), including the posterior C1,
P1, and LPC, and the anterior frontal N1 and N2. During
the delay period, and in addition to the NSW, offset P1 and
P2 components were recorded, indicating the processing
of the offset of the encoded stimuli. Children presented
higher amplitudes than adults in most of these compo-
nents (including the posterior NSW) (Barriga-Paulino
et  al., 2017), and although the decrease in amplitude of
these components could be due to passive electromag-
netic properties generated by the increase in skull elec-
trical resistivity with age (Hoekema et  al., 2003), it was
recently demonstrated that passive electromagnetic skull
bone properties cannot completely explain the reduction
in amplitude of the EEG signals with age (Gómez et  al.,
2017).
The ERP components that appear during the differ-
ent phases of the DMTS task are related to the visual
processing of the stimuli in different stages, and they are
correlated with accuracy, indicating that the maturation
of these components co-varies with performance on the
different WM operations (Barriga-Paulino et  al., 2017).
When principal component analysis is applied to the
matrix of the amplitudes of the different ERPs appearing
during the DMTS task, the scores on the first principal
component extracted from the ERPs during develop-
ment were indexing both the age-related increase in
performance accuracy and the individual variability in
accuracy performance, suggesting that there is an indi-
vidual maturational factor of ERPs that is related to WM
performance. The presence of a first principal component
explaining both age and individual variability has also
been obtained from behavioral results on WM tasks
(Barriga-Paulino et  al., 2016). Therefore, the principal
component obtained from ERP (explaining age and
individual variability) results is probably related to the
C.M. Gómez et al.: Working memory development      15
component extracted from behavioral results, which
would suggest a possible causal relationship between
ERPs and behavioral maturation in DMTS.
Brain oscillations associated with
WM development
Oscillations evoked and induced by sensory
stimuli during WM tasks
Brain oscillations are rhythmic EEG signals generated
by the activity of connected neurons. Oscillations can
be studied in resting state or linked to the processing of
stimuli or motor responses. The role of the theta band in
WM has been clearly demonstrated; Raghavachari et  al.
(2001) showed an increase in theta band activity during
a Sternberg task. Gamma and theta phase coupling has
been proposed as a mechanism for keeping the items in
memory during the retention period of the DMTS task
(Sauseng et  al., 2010), whereas alpha amplitude has
been related to the suppression of distracting informa-
tion (Sauseng et  al., 2009). The synchronization of the
theta phase during the retention period has also been
described. An increase in theta amplitude during the prep-
aration period of a warning task (where the subjects have
to remember the type of trial (no-go, prosaccades, and
antisaccades) in order to produce a correct response) has
also been reported (Cordones et al., 2013). The number of
oscillations during the matching phase increases with the
number of items retained in the WM, which suggests that,
if more attempts are made to recover information, more
phase-locked theta cycles are needed (Tesche and Karhu,
2000). It is not yet clear how specific the theta oscilla-
tions are to WM operations, or whether theta corresponds
to a type of activity required from a myriad of cognitive
processes. The role of low beta band coherence between
parietal and prefrontal cortex during DMTS tasks has been
observed in intracranial recordings, showing a type of
object content-specific relationship (Salazar et al., 2012).
The latter approach stresses how important higher cogni-
tive functions, as WM, would depend on the inter-areal
cortical dynamics of different frequency bands (Bressler
and Richter, 2015).
Using a Sternberg task, Harmony (2013) showed a
delta band increase in adults after presentation of the
stimuli to be retained. However, children did not show
this increase. This difference suggests that delta would be
related to an increase in resistance to distractors in adults.
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16      C.M. Gómez et al.: Working memory development
On the other hand, children showed a higher theta rhythm
increase than adults. This occurred in the most difficult
condition, and it would be due to the higher cognitive
effort made to keep the presented items in memory. In
adults, an increase in synchronization in the alpha range
(during the encoding phase on WM auditory tasks) and
a corresponding desynchronization during recognition
have been observed. Similar results have been obtained
in children, not only in alpha but also in the theta band
(Krause et al., 2008). It is difficult to establish the particu-
lar contribution of the frequency bands to the different
sub-processes in WM operations, partly due to the variety
of paradigms used.
The P300 component has been related to the process
of WM updating (Donchin and Coles, 1988), and to an
increase in delta and theta oscillations (Basar-Eroglu
et al., 1992; Kolev and Yordanova, 1997; Yordanova et al.,
2000). The role of the theta rhythm in WM can also be
supported by the fact that the P300 component is related
to the delta and theta frequency range as an increase in
power and phase locking to the stimulus in these two
frequency bands (Digiacomo et  al., 2008). The relation-
ship between delta oscillations and the development
of P300  has been demonstrated by the simultaneous
decrease in the latency of peak delta oscillations and the
P300 latency with age, suggesting that both are part of
the same phenomenon (Kolev et  al., 1994). Yordanova
and Kolev (1998), using the oddball auditory task (typi-
cally used to generate the P300 component), and analyz-
ing single trials, showed that theta oscillations amplitude
decayed with age, not only during the baseline period (as
would be expected in studies on spontaneous EEG), but
also in post-stimulus-induced theta. The brain oscilla-
tions in the delta range at baseline (spatially filtered by
phase-locking to the stimulus), added to the increase
in power induced by the stimulus, was expressed in a
model by Barriga-Paulino et  al. (2013) to explain the
developmental trend of P300 amplitude. Little is known
about how the maturation of inter-trial synchrony and
event-related spectral power, induced in P300 eliciting
tasks, are related to the process of WM updating and its
maturation.
There is no doubt that theta, low beta, and delta
rhythms are emerging as a landmark for WM operations,
including in the developmental period. This is probably
due to the role of slow oscillation in nesting higher fre-
quency oscillations, and providing them with an adequate
spatio-temporal framework (Buzsáki, 2006). However, a
complete description of how the maturation of power and
synchrony at different frequencies is related to WM devel-
opment does not yet exist.
The relationship of WM with spontaneous
brain oscillations during development
The spontaneous EEG is a continuous activity produced
by synaptic potentials not linked to the occurrence of any
specific event, but associated with the general cognitive
enhancement with age. Harmony et  al. (1992) demon-
strated that theta rhythm maturation is needed to improve
cognitive performance with age. The amplitude of this
cerebral rhythm, which is prevalent in young children,
decreases progressively (Carretié, 2001; Segalowitz et al.,
2010). Through the study of correlations between the
power spectral density of spontaneous EEG and the scores
on the three WM components, based on the Baddeley and
Hitch model (1974): central executive, phonological loop
and visual-spatial sketchpad, Rodríguez-Martínez et  al.
(2013) observed a close association between the matura-
tion of theta and low beta rhythms and WM maturation
in subjects from 6 to 26  years old. This study revealed
that the subjects who showed better performance on the
neuropsychological test presented smaller theta rhythm
amplitudes in the spontaneous EEG. The same phenom-
enon was observed (although with a lower correlation) in
the low beta rhythm. Moreover, Rodríguez-Martínez et al.
(2014) showed that there is co-maturation between the
theta and beta rhythms in fronto-parietal areas, suggest-
ing that the maturation of these two rhythms in fronto-
parietal areas may be important for the maturation of WM.
What neurophysiology suggests
about WM maturation from
childhood to adolescence and
young adulthood
Neuroimaging studies are suitable for providing insights
about how neuroanatomical and functional brain matura-
tion are related to WM maturation. The neurophysiology
of WM provides information about the evolution of WM
operations (mechanisms) during the different develop-
mental stages. In this regard, and taking into account the
previously mentioned studies about WM, it seems that
subjects from early childhood to young adulthood share
the same mechanisms as adults, although there are func-
tional differences.
Based on the DMTS studies, the NSW and the SN
were similar from 6 to 26 years old (Barriga-Paulino et al.,
2015a, 2017). Regarding the NSW, the main differences
between children and adults were: (i) higher amplitude
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in children, possibly due to greater cortical thickness.
This decrease in amplitude with age is general for all the
components in the DMTS task and for P3b in the visual
oddball task; (ii) the possibility of explaining the NSW in
children with only two posterior dipoles (whereas adults
need a couple of anterior dipoles); and (iii) the positive
slow wave registered in frontal sites in children, instead
of the widespread NSW recorded in adults. The presence
of an NSW in children clearly suggests a similar mecha-
nism for WM during the retention period in children and
adults. However, different dipole modeling and polarity
changes indicate that brain activation is not the same
in childhood and adulthood. Neuroimaging studies,
reviewed above, and LORETA analysis of NSW (Barriga-
Paulino, 2015b), suggest the progressive involvement of
the frontal cortex in WM tasks as age increases. However,
at the same time, the different polarity in the frontal
cortex suggests a different organization of the neural acti-
vation in cortical layers. A simplified schema of how EEG
is generated in cortical layers (Bear et  al., 2001) would
suggest that the positive SW in frontal areas in children
would be dominated by near to the soma excitatory post-
synaptic potentials, whereas in adults the frontal NSW
would be dominated by superficial excitatory postsynap-
tic potentials and/or near to the soma inhibitory postsyn-
aptic potentials.
In the same direction, the work of our group (Flores
et  al., 2009, 2010) has shown that, although children
perform attentional tasks with slightly lower efficacy
to adults, they present important differences in ERPs,
which indicates that they use different brain resources to
perform the same tasks. Specifically, the presence of the
orientation frontal sub-component of the CNV in children
is not evident, nor is the frontal motor negative compo-
nent that appears in the late CNV. Likewise, the formation
of a visual P3a in the processing of target stimuli in the
presence of invalid cues (Flores et  al., 2010) and novel
stimuli (Rojas-Benjumea et  al. 2015) was not evident in
children. All these results suggest a protracted matura-
tion of the frontal cortex, which explains the lower perfor-
mance on attentional and WM tasks. However, in children
and adults, the sensory component of CNV (induced by
sensory cues) and the P3b modulation (generated by
invalidly signaled target stimuli and novel stimuli) were
clearly formed. Therefore, as is likely to occur in attention,
part of the WM function is transferred to frontal areas as
age advances. Thus, it is possible to speculate about the
possibility that the considerable increase in clinical psy-
chopathology that appears in post-adolescence (Paus
et  al., 2008) could partly be explained by maladaptive
functional reorganizations (including WM and attention
C.M. Gómez et al.: Working memory development      17
functions) that would occur during the pre-adolescent
and adolescent periods.
In addition, the main difference in the SN corresponds
to a longer duration of this component in children than in
adults (Barriga-Paulino, 2015a), which may correspond to
a slower pace for the extraction of information from the
matching stimulus in children. This maturational delay
would be due to physiological maturational processes that
are taking place in young children. The maturation of the
posterior cortex, where the neural sources of the SN are
located, is asynchronous in different posterior areas. As
Giedd et al. (2009) indicated, a maturational gradient from
low to higher-order association cortices inside lobules is
superposed with the more general anterior-­posterior matu-
ration gradient. This within-lobule gradient would justify
the higher SN duration in children than in adults if SN has
its neural sources in these late maturation associative areas.
Conclusions
From the review of the neuroimaging studies, it can be
concluded that children and adults use similar brain areas
(mainly fronto-parietal) to process stimuli in WM. In the
same way, electrophysiological studies show that both age
groups use similar brain mechanisms (including NSW, SN
and P3b), but they suggest that in WM processing, in chil-
dren the posterior areas are more important than the ante-
rior ones, and in adulthood the anterior areas would have
greater participation. It is necessary to study more in depth
how brain oscillations participate in WM maturation.
Acknowledgments: This work has been possible thanks to
grants from the Ministry of Science and Innovation PSI2013-
47506-R and PSI2016-80059-R (FEDER funds from the EU),
and from the Consejería de Innovación, Ciencia y Empresa
of the Junta de Andalucía. We thank to prof. ­Santiago Peleg-
rina for the careful review of this manuscript.
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