Neuropsychologia 84 (2016) 89104

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Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia

Longitudinal study of preterm and full-term infants: High-density EEG

analyses of cortical activity in response to visual motion
Seth B. Agyei n, F.R. (Ruud) van der Weel, Audrey L.H. van der Meer
Developmental Neuroscience Laboratory, Department of Psychology, Norwegian University of Science and Technology, NTNU, Norway

art ic l e i nf o

a b s t r a c t

Article history:
Received 25 July 2015
Received in revised form
14 January 2016
Accepted 3 February 2016
Available online 4 February 2016

Electroencephalogram (EEG) was used to investigate brain electrical activity of full-term and preterm
infants at 4 and 12 months of age as a functional response mechanism to structured optic ow and
random visual motion. EEG data were recorded with an array of 128-channel sensors. Visual evoked
potentials (VEPs) and temporal spectral evolution (TSE, time-dependent amplitude changes) were analysed. VEP results showed a signicant improvement in full-term infants' latencies with age for forwards
and reversed optic ow but not random visual motion. Full-term infants at 12 months signicantly
differentiated between the motion conditions, with the shortest latency observed for forwards optic ow
and the longest latency for random visual motion, while preterm infants did not improve their latencies
with age, nor were they able to differentiate between the motion conditions at 12 months. Differences in
induced activities were also observed where comparisons between TSEs of the motion conditions and a
static non-ow pattern showed desynchronised theta-band activity in both full-term and preterm infants, with synchronised alpha-beta band activity observed only in the full-term infants at 12 months.
Full-term infants at 12 months with a substantial amount of self-produced locomotor experience and
neural maturation coupled with faster oscillating cell assemblies, rely on the perception of structured
optic ow to move around efciently in the environment. The poorer responses in the preterm infants
could be related to impairment of the dorsal visual stream specialized in the processing of visual motion.
& 2016 Elsevier Ltd. All rights reserved.

Keywords:
EEG
Infants
Prematurity
Motion perception
Optic ow
Random motion
Visual motion
Visual perception
Locomotion
Self-motion
VEP
TSE
Time-frequency analysis
ERP

1. Introduction
Most daily activities including social interactions and cognitive
skills such as object categorisation, reading, and navigating
through the environment depend on perception and correct interpretation of visual information. Considering the relevance of
these abilities to everyday life, it is important to understand the
developmental processes underlying how infants learn to make
use of relevant visual information for perception.
During daily activities, it is important to recognise the landmarks in the environment and their egocentric positions in dening how relative an object's position is to an observer and vice
versa (Wall and Smith, 2008; Warren, 1976). The concept where
major images emanate from a central point in a structured form
within the angle of sight when there is a change of scenery either
by locomotion in any direction or as an object approaches an observer is referred to as radial optic ow (Gibson, 1979). The visual
motion perception that is achieved by this change is crucial for
adjusting posture (Vaina and Rushton, 2000), perceiving time-ton

Corresponding author.

http://dx.doi.org/10.1016/j.neuropsychologia.2016.02.001
0028-3932/& 2016 Elsevier Ltd. All rights reserved.

contact (Kayed and Van der Meer, 2009), avoiding obstacles

(Turano et al., 2005; Wilkie and Wann, 2003), and reaching a
target efciently by determining heading direction (Lappe et al.,
1999). The relation between optic ow perception and action has
often been studied in terms of motor activities (e.g., Bruggeman
et al., 2007). It has been shown that perception of optic ow plays
a major role in the control of walking speed and direction (Bruggeman and Warren, 2010; Lamontagne et al., 2007; Vilhelmsen
et al., 2015; Warren et al., 2001). The estimation of speed in order
to effectively reach a target is achieved by integrating inputs from
the visual system with locomotor variables (Saleem et al., 2013).
Improvement in visual perception by actual motor learning
through action-to-perception transfer has been reported in adults
(Beets et al., 2010). Young infants, on the other hand, are not as
efcient as adults in detecting optic ow (Gilmore et al., 2004,
2007; Van der Meer et al., 2008).
Rudimentary perception of optic ow patterns appears within
the rst weeks and months after birth (Gilmore et al., 2004), with
adults able to readily distinguish between expansion/contraction,
rotational, and translational (horizontal/vertical) forms of motion
(Gilmore et al., 2007). Behaviourally, infants younger than a month
of age exhibit defensive responses such as backward head tilting

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and frequent eye blinking in reaction to structured motion, with

even neonates as young as 3 days old observed to exhibit responses through backward head movements when exposed to
backwards ow stimuli (Jouen et al., 2000; Shirai and Yamaguchi,
2010). These defensive behavioural responses in very young infants, however, have been interpreted to be the result of multimodal integrative and cooperative processes in which visual,
vestibular, and proprioceptive senses are involved rather than a
direct consequence of motion perception (Jouen et al., 2000).
Further studies using electroencephalogram (EEG) have shown
that infants younger than 68 weeks do not discriminate between
motion directions and do not smoothly pursue small moving objects but such abilities improve rapidly around 614 weeks after
birth (Rosander et al., 2007). These motion patterns show unique
developmental trends with age in infants (Shirai and Yamaguchi,
2010). Here, perception of translational motion emerges at approximately two months of age whereas perception of radial
motion and its cortical responses develop rapidly afterwards from
just before 3 months until approximately 4 months of age (Shirai
and Yamaguchi, 2010). However, this fast perceptual development
starts decelerating after the rst few months but approaches adult
level around 4 years of age (Kaufmann, 1995).
Various brain studies in humans and other primates have investigated the cerebral networks specialized for perception of visuo-spatial information (for review, see Shirai and Yamaguchi
(2010)). In particular, perception of movement control including
self- and object-motion is processed via the dorsal visual stream
(see Creem and Proftt (2001)). Neurons within the medial temporal (MT/V5 ) complex are generally sensitive to radial motion
processing, with the dorsal medial superior temporal (dMST) area
involved specically in optic ow processing (Creem and Proftt,
2001; Duffy and Wurtz, 1991; Dukelow et al., 2001; Fukushima,
2008; Greenlee, 2000; Imura et al., 2008; Itoh et al., 2005;
Newsome and Pare, 1988; Riecansky, 2004; Smith et al., 2006;
Tohyama and Fukushima, 2005; Wall et al., 2008).
The human brain is an organised dynamic network of interconnected neurons and associated synapses that work together
such that dysfunctions within the network can have adverse effects on behavioural patterns. Magnetic resonance imaging (MRI)
studies show that being born preterm causes differential brain
development that leads to abnormalities in the microstructure of
tissues and in cerebral morphology (Counsell and Boardman,
2005; Counsell et al., 2006). Premature birth with its continuously
increasing incidence (Martin et al., 2003, 2013) has therefore been
given considerable attention over the years. Some of the dysfunctions of preterm birth have been related to cognitive and
behavioural impairments (Aarnoudse-Moens et al., 2009; Bhutta
et al., 2002; De Jong et al., 2012; Delobel-Ayoub et al., 2009;
Johnson, 2007; Salt and Redshaw, 2006) including decits in visual
perception and other neurodevelopmental disorders (see De Jong
et al. (2012)).
Some studies have reported decit in motion and form perception in premature children that was either a consequence of
being born preterm (MacKay et al., 2005; Taylor et al., 2009) or a
result of the accompanying periventricular leukomalacia (PVL)
(Downie et al., 2003; Jakobson et al., 2006). Using behavioural
experiments, further studies have shed more light on the decit in
motion and form perception where differences between global
motion (optic ow) perception and form perception have been
found (Guzzetta et al., 2009). They reported that preterm children
with and without brain damage appeared to perform worse than
full-term controls in global motion perception, with PVL preterm
infants performing worse on form perception than preterm infants
without PVL (Guzzetta et al., 2009). These observations suggested
impairment of the dorsal stream during visual processing in preterm children with and without brain damage. In four cohort

studies in which several assessment techniques were used and the

correlations between the results and MRI indicators of brain abnormalities were analysed, it was also pointed out that the impairment of the visual dorsal stream is a possible cause for the
cluster of developmental problems seen in children born prematurely (Atkinson and Braddick, 2007). These ndings are further
supported by other studies where global motion, global form, and
biological motion (combination of cues for form and motion)
perception were compared in preterm children (e.g., Taylor et al.,
2009). Global motion perception decit was observed more densely than global form decit, and difculties in biological motion
perception were also present (cf., Atkinson et al., 2008b). Further
studies (e.g., Van Braeckel et al., 2010) that investigated the motor
skills of preterm children of 711 years report that they perform
less accurately or slower in movement pointing tasks, implying
less efcient elementary visuomotor processing and impaired
functioning of the dorsal visual stream. Other studies with the aim
to help detect early brain damage in premature infants have further formulated specic markers of visual cortical function in the
rst postnatal months for both normally and atypically developing
infants (Atkinson et al., 1992, 2008a,; Braddick et al., 1992, 2005).
Such studies showed that the severity of detected brain injury in
preterm infants was correlated with impaired orientation-reversal
visual event-related potentials and the cortical control of visual
attention through xation shifting. These studies also showed
preterm infants to display worse performances on given cortical
tests compared to full-term infants.
During visual perception tasks, EEG primarily records electrical
activities of pyramidal neurons with high temporal resolution (in
the millisecond scale) that permits the study of the neuronal basis
of motion perception and the functional specialisations of cortical
structures (Agyei et al., 2015; Dukelow et al., 2001; Sakkalis et al.,
2008; Tucker, 1993). Motion-sensitive visual evoked potential
(VEP) waveforms in EEG are thought to originate from V5/MT in
occipital and parietal visual areas (Kobayashi et al., 2004; Wall
et al., 2008), and are characterized by a negative N2 peak component that occurs around 270290 ms post stimulus in 1112month-old infants (Agyei et al., 2015) and around 130200 ms in
adults (Fielder et al., 1983; Heinrich et al., 2005). Previous studies
reported the N2 visual component in infants to be longer in latency and higher in amplitude compared to adults (Van der Meer
et al., 2008), with the longer N2 latencies improving with infants'
age (Agyei et al., 2015). Other studies of early visual N1, P1 and P2
components (e.g., Fielder et al., 1983; Hammarrenger et al., 2007)
have shown similar results where latencies were observed to decrease as children became older.
In addition to the use of VEPs in EEG studies, investigation of
neural activities in the time-frequency domain has allowed for the
study of cognitive and perceptual functions through observations
of the natural frequencies in EEG (Agyei et al., 2015; Basar et al.,
1999; Formaggio et al., 2010; Ganzetti and Mantini, 2013; Salari
et al., 2012). Analyses in the time-frequency domain permit the
extraction of event-related frequency changes in EEG that cannot
be observed in VEPs by using averaging techniques. These frequency changes are observed as event-related (de)synchronisation
(ERD/ERS) oscillatory activities that represent decreases/increases
in amplitude/power of specic frequency bands (Pfurtscheller and
Lopes da Silva, 1999), an indication of decrease/increase in synchrony of the underlying neuronal populations (Hoechstetter et al.,
2004; Pfurtscheller et al., 1994). Based on spectral proles within
specic frequency bands, different classes of oscillations have been
distinguished over the years: delta-band (14 Hz), theta-band (4
7 Hz), alpha-band (713 Hz), beta-band (1330 Hz), and gammaband (30150 Hz), with these rhythms shown to reect neurophysiological processes that manifest functionally different roles
(Buzsaki and Draguhn, 2004; Engel and Fries, 2010; Ganzetti and

S.B. Agyei et al. / Neuropsychologia 84 (2016) 89104

Mantini, 2013; Saby and Marshall, 2012). For example, while deltaband oscillations play a role in processes such as signal detection,
event-related oscillations in the theta-band have been reported to
play an important role in cognitive processes (Baar et al., 2000;
Freunberger et al., 2011; Gruber and Mller, 2006; Khader et al.,
2010; Klimesch et al., 1996). Event-related synchronisations in the
alpha-band may reect control of inhibition and cortical processing (Doppelmayr et al., 1998, 2005; Freunberger et al., 2011; Klimesch, 1999; Klimesch et al., 2007; Sauseng and Klimesch, 2008).
Further studies with visual stimuli (e.g., Wrbel, 2000) have linked
beta oscillatory responses to multisensory stimulation and the
shifting of neural systems to a state of attention that ultimately
allows for gamma synchronization and the utilisation of the resulting information for perception (Herrmann et al., 2004, 2010).
Particularly in infants, low-frequency oscillations especially in the
theta-alpha range undergo systematic development from early
childhood to adulthood (Stroganova and Orekhova, 2007; Stroganova et al., 1999). These low-frequency rhythms in infants have
been attributed to general signs of immaturity (Orekhova et al.,
2006; Stroganova and Orekhova, 2007). Recent infant studies have
implicated low-amplitude desynchronised theta-band activities
over visual areas when motion stimuli were compared with static
stimuli (Agyei et al., 2015; Van der Meer et al., 2008), with further
observation of high-amplitude activities especially in alpha-band
frequency observed in one-year-old infants (Agyei et al., 2015).
This transition of EEG spectral power/amplitudes from lower to
higher frequencies during development is considered a sign of
maturation in various psychophysiological studies (Hudspeth and
Pribram, 1992; Stroganova et al., 1999).
The present study explores the development of the visuocognitive systems, especially visual motion perception during early
infancy. The study presents information that contributes to the
understanding of the normal development of visual motion perception in infants and the developmental impairments associated
with motion perception in preterm birth. Using EEG longitudinal
data, the paper compares preterm and full-term infants at the ages
of 4 months and 12 months through a combination of VEP and
time-frequency analyses. VEPs were assumed to represent responses of cortical neurons to changes in afferent activity (Brecelj,
2003; Van der Meer et al., 2008), while event-related time-frequency responses represent interactions of local cortical neurons
that control the frequency components of an ongoing EEG
(Pfurtscheller and Lopes da Silva, 1999). It was expected that
perception of optic ow would rapidly improve with increasing
age especially in the full-term infants, with no such marked improvement in perception of random visual motion, and that lowfrequency decrease in amplitudes would generally be observed.

2. Methods
2.1. Participants
Twenty full-term and preterm normally developing infants
were recruited for the study through birth announcements, contact with parents and/or through the Neonatal Intensive Care Unit
at St. Olav's University Hospital in Trondheim. The full-term infants had mean gestational age of 39.9 weeks (SD 0.9, median 39.6, range38.441) and mean birth weight of 3693 g
(SD 628, median 3500, range30855120). The preterm infants (moderate to very preterm) were born at mean gestational
age of 31.4 weeks (SD 1.8, median 31.4, range28.433). Their
mean birth weight was 1622 g (SD 453, median 1530,
range10002670). The preterm infants did not have any major
neurological decits including severe brain damage, retinopathy of
prematurity (ROP) and other perinatal issues requiring serious

91

medical interventions that may lead to abnormal development.

Infants were tested at 4 months and later at 12 months using a
longitudinal design. One preterm infant was excluded from the
study for presenting inadequate data for analysis at 12 months
since he became very uncomfortable early on in the testing. Hence,
one full-term infant was also excluded from further analysis. Thus,
longitudinal analyses were performed on 18 infants in total for
both testing sessions (full-term: 5 girls, 4 boys; preterm: 3 girls,
6 boys).
For the rst testing session, the mean age of the preterm infants was 4 months and 26 days (SD 6.9) with a range of 139158
days, and the mean age of the full-term infants was 4 months and
16 days (SD 21.3) with a range of 111164 days. Infants at the rst
testing session had no experience with self-locomotion. For the
second session, mean age was 12 months and 18 days (SD 18.6)
with range 356414 days for preterm infants, and 11 months and
20 days (SD 13.9) with range 333371 days for the full-term infants. Preterm ages were corrected for prematurity. All infants
could crawl and independently pull to stand or walk with help at
the time of the second testing session except three preterm infants
who had not started crawling or pulling to stand and were bottom-shufing instead (parental report and observation).
Electroencephalography is a physiological procedure that is
known to have no painful or harmful effects on participants. Parents gave their informed consent prior to the experiment and had
the right to withdraw from the testing at any time before or during
the experiment. The Norwegian Regional Ethics Committee and
the Norwegian Data Services for the Social Sciences approved the
study.
2.2. Experimental stimuli and paradigm
Stimuli were programmed using E-Prime (Psychological software tool) and mirror-reversed projected by an ASK M2 projector
onto a wide white screen (1.1 m  0.8 m) at a visual angle of 68
horizontal by 47 vertical. Image resolution was 593 pixels per
metre at a refresh rate of 60 Hz. The screen was placed at a distance of 80 cm from the infant (see Fig. 1). To discriminate between coherent and incoherent radial motion, three conditions, i.e.
forwards optic ow, reversed optic ow, and random visual motion, as well as a static non-ow condition, were used. Each condition consisted of 100 black dots (5 mm virtual radius) that were
randomly positioned on the screen. Each condition was presented
for 1.5 s, with stimulus contrast around 99.5% and mean luminance at 68 cd/m2. In the motion conditions, dot particles moved
at a constant rate of 30 mm per frame at 60 fps such that they
moved inwards and towards or outwards and away from a central
xation point, 1.69 mm in diameter, that subtended an angle of
0.16 at the centre of the screen. Dot particles appeared small
when far away from the eye in virtual space or large when closer
to the eye as they decreased or increased in size at a rate of 0.025
pixel per pixel with reference to the central xation point. Sizes of
dot particles that appeared on the screen ranged from 2 mm to
17 mm in radius.
In the forwards optic ow condition, dots moved coherently
towards the infant where movement was parallel to the z-axis
towards the eyes with zero velocity in the x- and y-axis. The reversed optic ow condition had similar properties as the forwards
optic ow condition except that the coherent movement of dots
was in the opposite direction and away from the infant. In the
random condition, dot particles moved incoherently in random
directions in virtual space but with similar properties as stated
above. For the static condition, however, dot particles had zero
velocity in all directions and remained in the same position on the
screen for the entire duration of a trial. The order of presentation
of the stimuli was random, with the static condition always

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S.B. Agyei et al. / Neuropsychologia 84 (2016) 89104

Fig. 1. Experimental set-up: actual appearance of the experimental room with a

12-month-old infant sitting in a baby car seat and the 128-sensors placed on his
head. The parent appears on the right side and the assistant on the other side of the
infant. Moving dots simulating optic ow and random motion appear on the large
screen in front of the infant. The eye tracker is on the desk in between the infant
and the screen.

appearing in between successive presentations of the motion

conditions in order to avoid motion adaptation.
Stimuli were presented as a uniform dot distribution to avoid
accretion of dots at the centre or edges of the screen. Particles that
moved outside the range of sight on the screen were automatically
resized and repositioned on the screen where all particles in each
motion condition had an equal probability of placement.
2.3. Data acquisition
EEG activity was recorded with a Geodesic Sensor Net (GSN)
200 (Tucker, 1993; Tucker et al., 1994). The net consisted of an
array of 128 Ag/AgCl sensors that were evenly distributed on the
infant's head. A high-input EGI amplier was connected to the
GSN 200 to ensure signals were amplied with maximum impedance set to the recommended value of 50 k for optimal signal-to-noise ratio (Budai et al., 1995; Ferree et al., 2001; Picton
et al., 2000). Amplied signals were recorded with Net Station
software on a Macintosh computer and sampled at 500 Hz. Tobii
X50 camera was used to track the gaze of the infants, with the
visual feed processed by ClearView software on an HP computer.
Two additional cameras positioned at different angles in front of
the infants were used to record digital videos to track the behaviour of infants during the experiment. Recorded data were subsequently stored for ofine analyses.
2.4. Procedure
Parents signed the consent form when they arrived with their
infant prior to the experiment. The infant was then allowed time
to get used to the laboratory surroundings by playing with toys
and generally exploring the new environment. In the process, an
assistant measured the infant's head circumference to allow for
the correct size selection of the GSN 200. To optimise electrical
conductivity of the net, it was immersed in a saline electrolyte
solution and partially dried before being mounted on the infant's
head while the infant was seated on the parent's lap. Distractors
such as colourful soap bubbles and small sounding toys were used
to attract the infant's attention from the net as it was being
mounted. Immediately after mounting the net, the infant was

moved into a dimly lit experimental room while other assistants

moved to the control room to manage the computers necessary for
data acquisition. A glass partition that was both soundproof and
transparent separated the control room from the experimental
room. The infant either sat on the parent's lap for the rst testing
session or in a baby car seat during the second testing session
while positioned in front of the screen, with the parent in close
proximity (Fig. 1). The impedance of the electrodes was then
checked with the net connected to the amplier, while electrode
contact was improved if necessary. An assistant was present in the
experimental room to help the infant focus on the screen and to
monitor the experiment, while the parent was present for the
entire duration of the experiment to avoid any stressful effect an
absent parent may have on the infant.
The experimental session immediately began after calibrating
the infant's eye movement in virtual space to the Tobii X50 camera. The session started with the optic ow experiment followed
by two other visual motion experiments. The optic ow experiment lasted between 5 and 7 min. From 80 to 120 trials were
presented per infant, where approximately half of those were
static non-ow trials. Data acquisition was carried out in one block
but when an infant showed signs of boredom or disinterest, the
session was paused in order for the assistant and/or parent to
revive the level of interest by playing with the infant for a short
period before resuming the presentations. An experimental session ended if an infant showed considerable level of disinterest,
fussiness, or tiredness.
2.5. Data analysis
EEG data were analysed with Brain Electrical Source Analysis
(BESA) research software version 6.0 and BESA statistics 1.0 (BESA
GmbH). In the initial pre-processing step, EEG recordings were
segmented with the Net Station software and exported as raw les
for further ofine analyses. Appropriate auxiliary les containing
trigger and sensor information were imported and attached.
Epochs around the triggers of stimuli were set with averaging
epoch at  200 to 800 ms at a baseline denition of 100 to 0 ms.
To remove slow drift in the data, high-pass lter was set at 1.6 Hz.
Low-pass lter was at 60 Hz while notch lter was set at 50 Hz to
remove lines interference from the recorded data. By visual inspection together with the visual feed from the eye-tracker, artefact-contaminated channels and epochs resulting from head or
body movements as well as instances where infants were not
looking at the screen were excluded from further analyses or the
data interpolated where necessary. In scanning for artefacts,
threshold values for gradient and low signal were set at 75 V and
0.1 V, respectively, while maximum amplitude was set at 200
230 V. Physiological artefacts from activities such as blinking and
eye movements (Lindsen and Bhattacharya, 2010; Pham et al.,
2011) were corrected from the data using manual and semi-automatic forms of artefact correction that were designed to separate
brain activities from artefacts using appropriate spatial lters
(Berg and Scherg, 1994; Fujioka et al., 2011; Ille et al., 2002; Shao
et al., 2009).
The mean numbers of accepted motion trials for full-term infants at 4 months and 12 months were 43 (SD 4.9, range3166)
and 42 (SD 4.8, range3172), respectively, while those for
preterm infants were 46 (SD 4.9, range2773) and 40 (SD 2.8,
range 3148) at 4 months and 12 months, respectively. Trial
numbers were more or less evenly distributed across the three
motion conditions. The static control condition had mean numbers
of accepted trials of 48 (SD 13.1), 48 (SD 18.1), 50 (SD 17.1),
and 40 (SD 6.6) for full-term infants at 4 months, full-term infants at 12 months, preterm infants at 4 months, and preterm
infants at 12 months, respectively.

S.B. Agyei et al. / Neuropsychologia 84 (2016) 89104

VEP peak analysis was carried out using individual averages.

Individual averages were obtained for each infant by averaging
individual data over whole EEG continuous le and interpolating
to the standard 81-electrode conguration of the international 1010 standard electrode system by re-referencing to an articial reference calculated from the average potentials over the scalp. The
individual averages for infants in each of the testing sessions were
combined into grand averages for each session. Grand average
VEPs gave approximate time intervals that served as reference
intervals for selecting individual N2 components at different
electrode sites. Further, the N2 components of the VEP waveforms
were identied using 3D spherical spline whole-head voltage
maps of EEG scalp signal distributions that helped to visualise
maximum N2 activity in occipito-parietal areas for the most
dominant VEP waveform. Values for peak latencies and peak amplitudes of the individual averages were recorded. Peak latencies
were measured as the time from stimulus onset to the peak of
each scalp N2 component while peak amplitudes represented
maximum amplitudes of the N2 component relative to the prestimulus baseline. The values were then subjected to further VEP
analyses.
Time-frequency analysis was performed in brain space using
pre-dened multiple source dipoles that modelled activities in the
visual areas of the parietal and visual cortices. Measuring brain
oscillatory activities using surface electrodes may not be ideal
since scalp waveforms receive mixed contributions from underlying brain sources. This is due to the wide distribution of focal
brain activity as a result of the smearing effect of brain volume
conduction in EEG and the nature of dipole elds. Therefore, to
achieve optimal separation of focal brain activities, a source
montage was used. It was obtained using a multiple source model
(Scherg and Berg, 1991; Scherg et al., 2002) where source waveforms maximally separated activities from different brain regions.
The source montage consisted of 17 sources that modelled activities in the visual pathway as well as any residual activities in
other regions of the brain. Of these sources, the visual cortex lateral left (VClL), visual cortex radial right (VCrR) and the parietal
midline (PM) sources (see Fig. 2) that are believed to be active in
the visual processing of motion stimuli (Probst et al., 1993; Van der
Weel and Van der Meer, 2009; Zeki et al., 1991) were further
analysed. To analyse brain activities using these sources, a 4-shell
ellipsoidal head model (Berg and Scherg, 1994; Hoechstetter et al.,
2004; Scherg et al., 2002) with the source dipoles inserted, was
created for each infant where the artefact-corrected coordinate
les were appended. Bone thickness and conductivity were adjusted at 3.0 mm and 0.02 s, respectively, as recommended for
infants (Grieve et al., 2003; BESA information). Settings for epoch,
lters and average parameters were the same as in the VEP analyses. Time-frequency displays showing the change in amplitudes
over time (TSE, temporal spectral evolution) were generated from
single trials by averaging spectral density amplitudes over trials.
Each displayed graph was a plot of spectral amplitude density of
one montage channel over time and frequency normalised to the
baseline for each frequency. Signals from average evoked responses were removed from the single trial time series before
calculating TSEs in order to have only TSE displays of induced
oscillatory brain activities. Comparisons between the motion
conditions and static non-ow condition were computed. TSE
displays were set to frequency cut-off of 440 Hz at frequency and
time sampling of 1 Hz, 50 ms. Frequency cut-off was also adjusted
to further investigate oscillatory activities within the delta and
gamma frequency ranges.
The probability of signicance in amplitude values and frequency ranges between the TSEs of the motion conditions and the
static condition for all infants in each testing session was computed using the statistics software. An average of TSE statistics for

93

infants in each testing session was computed such that signicant

time-frequency ranges were used as a guide when nding patterns
of oscillatory activities in each infant's TSE displays. The multiple
comparisons problem was addressed using a combination of permutation testing and data clustering technique (see Bullmore et al.
(1999), Ernst (2004) and Maris and Oostenveld (2007)) where data
clusters that showed initial signicant effect between conditions
were rst dened. These clusters were assigned initial cluster
values comprising of the sum of all t-values of all data points for
each initial cluster. The initial cluster values were then passed
through permutation testing using paired t-test and assigned new
cluster values. The signicance of the initial clusters could then be
determined from the distribution of the calculated cluster values
assigned to each initial cluster after permutation. Number of permutations was 512 and frequency cut-offs were the same as stated
above with the signicance level for building clusters in time and/
or frequency (cluster alpha) set at 0.005.
Further, comparisons between the motion conditions and static
condition for each infant were performed in order to compute
probability maps to separately test for signicant differences in the
TSEs (change in amplitude from baseline to particular time-frequency sampling points) for each individual infant. This allowed
the observation of signicant oscillatory activity patterns across
the visual areas of interest for each infant in each testing session
that were not visible in the overall averaged TSEs. To correct for
multiple testing, Bonferroni procedure and permutation tests described by Simes (1986) and Auranen (2002) were applied to each
set of time samples belonging to one frequency bin. Frequency cutoffs and time-frequency sampling points were maintained as stated earlier.

3. Results
3.1. VEP responses
For each group and each testing session, four posterior electrodes that showed the highest N2 amplitude values in the forwards optic ow condition of the grand average VEPs (Fig. 3) were
chosen for further analysis (cf., Agyei et al., 2015; Van der Meer
et al., 2008). The four grand average electrodes for full-term infants at 4 months were PO4, PO3, POz, and O1, and those at 12
months were PO4, PO8, Oz, and O2. The corresponding electrodes
for preterm infants at 4 months were POz, PO4, Oz, and O2, while
the electrodes at 12 months were POz, PO3, Oz, and O1 (Fig. 3).
Latencies and amplitudes of the VEPs were analysed separately
using repeated-measures ANOVAs. Within-subjects factor was
motion condition (forwards optic ow, reversed optic ow, random motion) and age (4 months and 12 months), while betweensubjects factor was participant group (full-term, preterm). Latency
values from the electrode with the highest N2 amplitude in the
forwards optic ow condition were used in the ANOVA, with
Bonferroni correction used to adjust for multiple comparisons. The
chosen electrode varied across participants and testing sessions
but was always one of the four mentioned above and was the
same for the three motion conditions in each infant.
The mean N2 peak latency after stimulus onset for forwards
optic ow in full-term infants at 4 months was 426 ms (SD 70),
with corresponding values for reversed optic ow and random
motion at 440 ms (SD 72) and 450 ms (SD 80), respectively. At
12 months, mean latency values of full-term infants were reduced
to 277 ms (SD 49) for forwards optic ow, 338 ms (SD 39) for
reversed optic ow, and 405 ms (SD 66) for random visual motion. N2 mean peak latencies of preterm infants at 4 months for
forwards optic ow, reversed optic ow, and random motion were
325 ms (SD 63), 359 ms (SD 63), and 372 ms (SD 64),

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S.B. Agyei et al. / Neuropsychologia 84 (2016) 89104

Fig. 2. Head model with associated visual cortical areas VClL (left), PM (middle) and VClR (right). The signal magnitude reects the estimated source activity in the related
brain region if one brain region is active. The approximate Talairach coordinates of the sources were VClL (x  45, y  57, z 6.5), PM (x 0.0, y  72, z 37), and VClR
(x 45, y  57, z 6.5).

respectively, while corresponding values at 12 months were

392 ms (SD 55), 386 ms (SD 57), and 378 ms (SD 51),
respectively.
For latency, a signicant three-way interaction of condition,
age, and group was found, F(2, 32) 8.13, p o0.005, indicating that
only the full-term infants at 12 months of age decreased their latencies signicantly from random visual motion to reversed optic
ow to forwards optic ow with approximately 60 ms between
each condition (see Fig. 4A). However, the preterm infants did not
differentiate between the three visual motion conditions, neither
at 4 months nor at 12 months. The preterm infants did not decrease their latencies with age (Fig. 4A).
Further, a signicant two-way interaction of age and group was
found, F(1, 16) 27.75, p o0.005, suggesting that irrespective of
visual motion condition and only at 4 months of age, preterm
infants had signicantly shorter latencies than full-term infants
(Fig. 4A). The mean N2 latency of forwards optic ow in full-term
infants decreased by about 150 ms from 4 months to 12 months.
However, mean latency of random visual motion decreased around
45 ms for the same age interval in the full-term infants.
Mean N2 peak amplitudes for full-term infants at 4 months
were 7.1 mV (SD 3.6) for forwards optic ow, 5.4 mV (SD 4.4) for
reversed optic ow, and 4.2 mV (SD 2.4) for random motion,
while mean amplitude values at 12 months were 5.7 mV (SD 3.8),
2.7 mV (SD 1.7), and 0.9 mV (SD 2.1) for forwards optic ow, reversed optic ow, and random motion, respectively. Preterm infants at 4 months had mean peak amplitudes of 5.2 mV (SD 2.6)
for forwards optic ow, 1.4 mV (SD 2.2) for reversed optic ow,
and 2.2 mV (SD 1.9) for random motion, with corresponding values for preterm infants at 12 months being 4.3 mV (SD 3.2),
3.4 mV (SD 1.0), and 4.5 mV (SD 3.2) for forwards optic ow,

reversed optic ow, and random motion, respectively.

For amplitudes, a signicant two-way interaction between age
and group was found, F(1, 16) 11.23, p o0.005, implying that
preterm infants showed signicantly lower amplitudes than fullterm infants but only at 4 months (see Fig. 4B).

3.2. Individual analysis

Individual analysis was performed on the VEP latency values
for full-term and preterm infants at 12 months considering that
only full-term infants at 12 months showed signicant differences
between the motion conditions, with no such differences observed
in the preterm infants at 4 months and even at 12 months. The
individual analysis explored the possibility of nding a criterion
that distinguished the preterm infants that were extremely delayed in their VEP responses compared to the other full-term and
preterm infants during the end of the rst year of life. Field (2009)
dened an outlier as the value that was smaller or larger than the
mean 7SD*2.5 of a reference value. Using the VEP latency values
of the motion conditions in the full-term infants at 12 months as
the reference for comparison, the criterion showed three preterm
infants L, O, and P to have outlier latency values particularly for
both forwards and reversed optic ow conditions where their VEP
latencies were found to be longer than the mean SD*2.5 of the
average VEP latency in the full-term infants at 12 months (Table 1).
Two infants, J and R, also showed outlier latency values but only
for the forwards optic ow condition. None of these preterm infants with outlier values showed delayed motor responses, neither
were they bottom shufers at the time of the second testing.

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95

Fig. 3. Grand average motion VEPs in full-term infants at 4 months (A) and 12 months (B), and in preterm infants at 4 months (C) and 12 months (D). Amplitudes are on the
y-axis and latencies on the x-axis. The actual N2 peak latencies for forwards optic ow are indicated at PO4 in full-term infants and POz in preterm infants. Differences in N2
peak latencies for the three motion conditions were observed only in full-term infants at 12 months where latency increased from forwards optic ow to reversed optic ow
and random motion. No signicant differences between N2 peak latencies were observed between the three motion conditions in full-term infants at 4 months and preterm
infants at 4 and 12 months. N2 peak latencies were also shorter for preterm infants at 4 months than full-term infants at 4 months. (E) The head drawing (nose up) shows
scalp localisation of the 81 standard electrodes with the electrodes of interest indicated with lled black circles (from top to bottom and left to right): PO3, POz, PO4, PO8, O1,
Oz, O2. (For interpretation of the references to colour in this gure, the reader is referred to the web version of this article.)

Fig. 4. Group means (and SDs) of N2 peak latencies (A) and amplitudes (B) in full-term and preterm infants. *Signicant at p o 0.05, **Signicant at p o0.005, ***Signicant
at p o0.001.

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Table 1
VEP latencies (ms) of the visual motion conditions for full-term infants (AI) and preterm infants (JR) at 12 months of age. Preterm infants L, O, and P showed latency values
for both optic ow conditions that were larger than mean SD*2.5 of the average latency values of the corresponding optic ow conditions in the full-term infants.
GA gestational age in weeks days.
Full-term
infants

GA

Forwards optic
ow

Reversed optic
ow

Random visual
motion

Preterm
infants

GA

Forwards optic
ow

Reversed optic
ow

Random visual
motion

A
B
C
D
E
F
G
H
I
Mean
SD
Mean (SD*2.5)

39 5
40 6
39 6
39
41
41
39
38 4
39 2

354
236
284
280
298
220
322
234
310
282
45
394

368
290
350
350
290
344
344
268
338
327
35
414

456
360
380
422
420
296
438
340
368
387
52
516

J
K
L
M
N
O
P
Q
R

30
28 4
31 3
32 5
30 6
33
32 3
32 6
28 3

484
318
456
304
370
438
416
374
400

402
390
434
288
422
442
438
394
384

392
330
462
328
374
398
384
408
388

3.3. TSE responses

Fig. 5 shows the results of the permutation test displaying the
average for infants in each testing session when TSEs of the motion
conditions were compared with the static condition. The permutation test showed signicant negative clusters (suggesting signicantly smaller values in the motion conditions than static nonow condition) in at least one of the visual areas of interest in both
full-term and preterm infants. The visual areas showed signicant

negative clusters that appeared to be dominated by activity within

the theta-band range. Theta-band activity was most prevalent and
widespread in full-term infants at 4 months (Fig. 5A) compared to
full-term infants at 12 months (Fig. 5B) and preterm infants at
both 4 months and 12 months (Fig. 5C and D). This prevalent
theta-band activity occurred over relatively longer periods of time
when infants were younger (Fig. 5A and C) compared to shorter
periods of time when infants in each respective group were older
(Fig. 5B and D). Similar TSE results were obtained when TSEs of

Fig. 5. Average visualisation of signicant data clusters in the visual sources of interest when the motion conditions were compared with the static non-ow condition in
full-term infants at 4 months (A) and 12 months (B), and preterm infants at 4 months (C) and 12 months (D). Light blue colours represent negative clusters (i.e. motion
condition had smaller t-values than static non-ow) and positive clusters are marked with light red colours (i.e. motion condition had larger t-values than static non-ow).
Signicant negative cluster in the visual areas (VClL, PM, VClR) is marked with light blue voxel marks. Each visual area is dominated by activity in the theta-band but over
longer periods of time and more prevalent in the infants at 4 months than those at 12 months for both full-term and preterm infants, with the most prevalent theta-band
activity appearing in the 4-month-old full-term infants. In parentheses are the respective cluster means for motion conditions, cluster means for static non-ow, and the
probability level at which the specic cluster is signicant, in that order. Stimulus onset is indicated with a vertical line at 0 ms. Epoch is from  200 ms to 800 ms. (For
interpretation of the references to colour in this gure legend, the reader is referred to the web version of this article.)

S.B. Agyei et al. / Neuropsychologia 84 (2016) 89104

97

Fig. 6. TSE plots (A, B) and the corresponding TSE probability maps (C, D) across brain regions of interest (VClL, PM, VClR) when the motion conditions were compared with
the static non-ow condition in a typical full-term infant at 4 months (A, C) and 12 months (B, D). For the TSE plots, increased spectral amplitude (induced synchronised
activity) is shown as red coloured contours while decreased spectral amplitude (induced desynchronised activity) is shown as blue coloured contours. Induced theta-band
desynchronised activities were observed in all the visual areas of interest in the full-term infants at both ages. Induced alpha-beta band synchronised activities can be
observed in two or more visual areas but only at 12 months (B). For the TSE probability maps, signicant increase and decrease of TSEs (p o 0.05) in the motion conditions
compared to the static non-ow are shown with red and blue voxel marks, respectively. TSEs of the motion conditions showed signicant decrease in amplitudes in induced
theta-band activity than static non-ow. Further, induced amplitude increases particularly in the alpha-beta range can be observed in the older infants (D). Epoch is from
 200 ms to 800 ms and baseline at  100 to 0 ms. Stimulus onset is indicated with a vertical red line at 0 ms. (For interpretation of the references to colour in this gure
legend, the reader is referred to the web version of this article.)

each of the motion conditions were separately compared with the

TSEs of the static condition, with no signicant differences observed when TSEs were compared between pairs of the three
motion conditions.
TSEs of the motion conditions showed lower amplitude values
in theta-band range than the static control condition in the visual
areas of interest for full-term and preterm infants at both
4 months and 12 months. These activities within the theta-band
range appeared as desynchronised oscillatory activities in the TSEs
of the full-term (Fig. 6) and preterm (Fig. 7) infants at 4 months
and 12 months when the motion conditions were compared with
the static non-ow condition. Additionally, the decrease in lowfrequency amplitudes were observed to be desynchronised with
activities induced by the motion conditions in both full-term and
preterm infants such that suppression of theta-band activity as a
result of the presentation of the motion conditions was observed
in the visual areas from about 500 ms to end of stimulus. However,

the observed theta-band desynchronisation in the TSEs of the

motion conditions was rather seen as synchronised theta-band
activities in the same time range in the TSEs of the static non-ow
condition for both full-term and preterm infants at 4 months and
12 months.
Further statistical analysis of each infant when comparing the
TSEs of the motion conditions with the TSEs of the static condition
showed signicant high-amplitude oscillatory activities in at least
two of the visual areas of interest but only in the full-term infants
at 12 months (see Fig. 6B, D). TSEs of the motion conditions when
compared to the static condition showed high amplitudes within
the alpha-beta frequency band which occurred at different latencies from start to around 450 ms post-stimulus, and around
600 ms to end of stimulus. These high amplitude increases were
synchronised with induced expression of alpha-beta frequencies
at peak latencies around 250 ms after stimulus onset. The alphabeta frequency band activities appeared as synchronisations in the

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Fig. 7. TSE plots (A, B) and the corresponding TSE probability maps (C, D) across brain regions (VClL, PM, VClR) when the motion conditions were compared with the static
non-ow in a typical preterm infant at 4 months (A, C) and 12 months (B, D). In the TSE plots, induced synchronised and desynchronised activities are shown in red and blue
contours, respectively. Only induced theta-band desynchronised activities are predominantly observed in all the visual areas in the preterm infants at both 4 months and 12
months. In the TSE probability maps, signicant decrease of TSE spectral amplitudes (p o 0.05) in the motion conditions compared to static non-ow is shown in blue voxel
marks. TSEs of the motion conditions showed signicant decreased amplitudes in induced theta-band activity with respect to the static non-ow condition. Stimulus onset is
indicated with a vertical red line at 0 ms. Epoch is from  200 ms to 800 ms and baseline at  100 to 0 ms. (For interpretation of the references to colour in this gure legend,
the reader is referred to the web version of this article.)

TSEs of the motion conditions compared with the static condition

in the full-term infants. No signicant differences in induced activities were found when TSEs were compared between the motion conditions in each infant. Further, the observed induced alpha-beta synchronised activities in the TSEs of the motion conditions in the full-term infants occurred within the same frequency range as the alpha-beta desynchronised activities observed
in the static non-ow condition. Unlike in the older full-term infants, however, no such high-frequency activities were generally
observed in the preterm infants at 12 months (see Fig. 7). Nonetheless, a few preterm infants at 12 months (3 out of 9) showed
signicant high-frequency synchronised activities particularly in
the beta-frequency band albeit not as prominent as the synchronised activities observed in the older full-term infants. In addition,
the three preterm infants who showed outlier latency values for
the optic ow conditions did not have any high-frequency oscillatory activities in their TSEs at 12 months. In the TSEs of each
individual infant and in the TSEs of each infant group, no

signicant induced activities were observed in any other frequency bands, including the delta and gamma band frequencies
when frequency cut-off was analysed below 4 Hz and above 40 Hz.

4. Discussion
The present longitudinal study investigated the perception of
visual motion information during early infancy, and the differences in visual motion perception between normally developing
full-term and preterm infants. High-density EEG was used to observe cortical electrical activity as a perceptual response to structured radial optic ow (forwards and reversed) and to random
visual motion. Motion specic N2 components of the VEP waveforms for 4- and 12-month-old full-term and preterm infants were
compared for latencies and amplitudes, with induced EEG activities further analysed.
A signicant improvement in latencies from forwards optic

S.B. Agyei et al. / Neuropsychologia 84 (2016) 89104

ow to reversed optic ow and random motion was observed only

in full-term infants at 12 months, with no marked improvement in
latencies between the motion conditions when full-term infants
were younger. The older full-term infants showed shortest latency
for forwards optic ow and longest latency for random visual
motion. The result corroborates earlier ndings from the study
that longitudinally compared full-term infants at 34 months and
1112 months using similar experimental paradigm (Agyei et al.,
2015). One contributing factor to this observed improvement in
visual motion perception could be neural maturation that allowed
for more efcient processing of the visual motion information at
12 months. It has been shown that bre volume of white matter
aggrandises due to ongoing axonal myelination during the early
maturational stages until adulthood (Jito et al., 2008; Paus et al.,
2001). Myelin sheath over the axons serves to increase the speed
of propagation of electrical impulses. Increased myelination as
infants aged from 4 to 12 months may have contributed to the
faster propagation of motion information and the shorter latencies
observed at 12 months. Thus, full-term infants appeared to show
better responses when perceiving structured radial optic ow information (shown by the shorter latencies), and they seemed affected by the lack of structure in random visual motion as evidenced by the longest latencies in the random condition. Full-term
infants' N2 latencies in response to random visual motion did not
become saliently shorter with age. It is possible that the lack of
structured information in a random visual scene hinders visual
motion perception in infants in the early stages of independent
self-motion. Further, other neurological studies have reported that
the numbers of dendrites and synaptic connections in the primary
visual cortex increase during the rst months of life and that they
reach a peak level between the ages of 8 months and 2 years
(Klaver et al., 2011; Loenneker et al., 2011). It has also been observed that the rate of metabolic activity in occipital, parietal, and
temporal cortices increases strongly after 3 months, while in visual
association cortex and frontal cortex, the rate of increase occurs
after 68 months of age (Klaver et al., 2011; Loenneker et al., 2011).
These increases in the number of dendrites and synaptic connections, as well as the rate of metabolic activity could mean that
functional specialisations of the neurons become optimal around
the second half of the rst year of life. Thus, latency differentiations between the three motion conditions that occurred only in
full-term infants at 12 months but not when they were 4 months
old could be associated with improved functional specialisations of
neurons in the dorsal visual stream of the older infants.
The shorter latencies observed in the older full-term infants
when presented with the structured optic ow conditions could
also be attributed to infants' frequent use of structured information for effective navigation (Bruggeman and Warren, 2010;
Bruggeman et al., 2007; Lamontagne et al., 2007; Lee and Aronson,
1974; Slobounov et al., 2006). Infants start to passively explore the
environment soon after birth either in a stroller or when being
carried by their caregivers until they begin crawling or walking
(see e.g., Raudies et al., 2012). With crawling and/or walking, infants are able to actively explore the surroundings through their
own movement. Considering that passive experience of motion
has been shown to reveal a minimum level of improvement in
sensitivity to optic ow between 3 and 6 months (Gilmore et al.,
2004), the passive experience acquired by the younger full-term
infants could have partially accounted for their inability to distinguish between the three motion conditions. This inability of the
younger infants to distinguish between the motion conditions is
further supported by studies in 4-month-old infants that showed
that infants at this age are poor at discriminating between different directions simulated by optic ow patterns (Gilmore and Rettke, 2003). Further, behavioural studies on postural control show
a strong coupling between visual motion perception and postural

99

control (Anderson et al., 2001; Higgins et al., 1996; Lejeune et al.,

2006). Such studies found that infants who had crawling experience were more sensitive to optic ow stimuli for postural control.
Infants that perceived optic ow in the anteroposterior direction
in a moving room were also able to substantially improve their
postural responses particularly after they learned to sit and crawl
(Bertenthal et al., 1997). Thus, the experience from self-produced
locomotion affords infants the ability to make better use of the
information embedded in optic ow (Anderson et al., 2001; Higgins et al., 1996; Lejeune et al., 2006). Self-produced locomotion
experience may therefore be more relevant for normal development of visual perception than passive experience. Niell and
Stryker (2010) showed that neural responses in the visual cortex
are modulated by visual input from locomotion but strongly driven responses of neurons in the visual cortex arise from motorrelated input to the cortex from self-generated actions (Keller
et al., 2012; Szuts et al., 2011). Further, functional perception of
structured radial ow develops with acquired independent locomotion (Van der Meer et al., 2008), with only self-generated actions leading to a strong link between perception and action in the
developing brain (James and Swain, 2011; Schwarzer et al., 2013).
In the present study, parental records showed full-term infants to
have approximately 3 months of crawling experience, with ve
infants able to walk for at least 2 weeks by the second testing
session. It is plausible that, in addition to maturation, the active
self-locomotion experience acquired by the older full-term infants
may have led to faster recruitment and activation of neural networks responsible for motion recognition compared to the
younger infants who may have only experienced locomotion
passively.
Results also indicated that preterm infants did not show latency differences in the motion conditions from 4 months to 12
months. Even though most of the preterm infants had similar
months of crawling experience as full-term infants at the time of
the second testing, they did not differentiate between the three
motion conditions at 12 months unlike the full-term infants. It has
been shown that preterm infants at corrected age of 23 months
are delayed several weeks compared to full-term infants when
differentiating between changes of direction (Birtles et al., 2007;
Braddick et al., 2005). Most neuroimaging studies agree on the
idea that there is white matter abnormality characterised by the
appearance of diffuse and excessive high signal intensity (DEHSI)
throughout the cerebral cortex in preterm infants at corrected ages
(Atkinson et al., 2008a; Counsell and Boardman, 2005; Counsell
et al., 2003, 2006; Maalouf et al., 1999; Salt and Redshaw, 2006;
Skiold et al., 2010). Other follow-up studies (e.g., Hart et al., 2011;
Skiold et al., 2012) show no association between DEHSI and possible brain damage while others assert that DEHSI should be
considered a form of white matter injury rather than white matter
immaturity (e.g., Domizio et al., 2005). Nonetheless, it is probable
that white matter abnormality that underlies the impairment of
the dorsal visual stream could have adversely affected the effective
propagation of axonal electrical impulses during transmission of
motion information in the preterm infants. This could have partly
accounted for the unimproved latencies in the preterm infants
with age.
Further, studies with docosahexaenoic acid (DHA), the long
polyunsaturated fatty acid that is transferred to the foetus in the
third trimester of pregnancy, show that DHA is an important
component involved in synaptogenesis, brain tissue synthesis,
cellular differentiation, and neurotransmitter metabolism (Neuringer et al., 1986; Sabel et al., 2009; Stein, 2001). Other studies
report impaired functioning of the dorsal pathway due to insufcient supply of DHA (Auestad et al., 2001; Carlson and
Werkman, 1996; O'Connor et al., 2001; Werkman and Carlson,
1996). Since the developmental period of the dorsal stream is

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believed to be concentrated around the third trimester of pregnancy (Hammarrenger et al., 2007; Klaver et al., 2011) and the cells
of the dorsal pathway need high levels of polyunsaturated fatty
acids for the optimal functioning of physiological processes (Sabel
et al., 2009; Stein, 2001), it is possible that the unimproved latencies observed in the preterm infants who were all born at gestational age of 33 weeks or less may have been related to their
being deprived of sufcient essential fatty acids such as DHA.
However, it is also possible that the unimproved latencies and the
inability to differentiate between the motion conditions in the
preterm infants at 12 months could have been a normal delay
related to premature birth that may be recovered at a later age. A
follow-up study to monitor the developmental progress of the
preterm group could help ascertain the validity of this notion.
Interestingly, preterm infants at 4 months showed signicantly
shorter latencies regardless of visual motion condition compared
to the full-term infants at 4 months. The fact that preterm infants
were tested corrected for prematurity could have contributed to
this faster perceptual response, considering that the 4-month-old
preterm infants had up to 3 months longer exposure and experience to real-world visual ow than the 4-month-old full-term
infants. The individual analysis of the preterm infants further
pointed to three infants that showed extremely longer latencies in
response to the structured optic ow conditions compared to the
other infants. Since these three preterm infants were born at later
gestational ages relative to the other preterm infants and were
neither bottom shufers nor showed any signs of delayed motor
development prior to testing, it is rather likely that their longer
latencies represent normal developmental delays that may be recovered with age. The suggested longitudinal follow-up on the
preterm infants could help uphold the criterion used in the individual analysis as an early screening tool to detect impairments
of visual motion perception in premature infants.
Comparison of the amplitudes of the N2 components revealed
lower activation values in preterm infants at 4 months than in fullterms at 4 months. Given that amplitudes of brain electrical waveforms represent the synchronous activity of excited neurons, it
is considered that higher amplitudes may reect more synchronous signals elicited by activated neurons in large cortical areas
(Pfurtscheller and Lopes da Silva, 1999; Pfurtscheller et al., 1994).
When compared to the full-term infants at 4 months, the lower
amplitudes in preterm infants at 4 months could reect a relatively lower number of synchronously active neurons that were
activated in response to the presented motion stimuli. This number of synchronously active neurons may have been better adapted
to respond to motion stimuli in the younger preterm infants
compared to the younger full-term infants, considering the preterm infants' earlier exposure to optic ow information. However,
the activation values recorded for all the infant groups were generally high when compared to adults (cf., Van der Meer et al.,
2008). These large activation values that may reect activation of
large cortical areas could imply less specialized and adapted neural
networks involved in the perception of visual motion in the infants
in general (see Huttenlocher and Dabholkar (1997)). The larger
activation values in the infants could also have been a result of
infants' relatively thinner skulls that allowed for less impedance
when measuring cortical electrical activity (Grieve et al., 2003).
Skull thickness and bone density in the infants were adjusted
using recommended values during the TSE analysis where the
time-dependent changes in amplitudes were explored.
Investigating the differences in induced activities showed that
both full-term and preterm infants had signicantly low amplitude
values in the theta-band range over the visual areas of interest
when the motion conditions were compared with the static nonow control condition. More prevalent theta-band activities occurred in the younger infants compared to the older infants in

each group. Theta-band activities were observed as desynchronised oscillatory activities in the TSE plots. Studies have observed
low-frequency activities of large amplitudes in infant EEG as a
general sign of immaturity (Agyei et al., 2015; Carmeli et al., 2005;
Pfurtscheller et al., 1994; Stroganova and Orekhova, 2007; Thierry,
2005). These studies are corroborated by the ndings in the present paper where induced activities within the theta-band range
were observed when the TSEs of the motion conditions were
compared with the static dot pattern. Given that optimal synaptic
plasticity occurs in the infant brain (Casey et al., 2000; Stroganova
and Orekhova, 2007), with the implication of theta-band activities
during the successful encoding of memory information (Freunberger et al., 2011; Khader et al., 2010; Klimesch et al., 1996), it is
possible that the observation of theta-band activities in the infants
could reect the formation of cortical synapses involved in the
processing of the motion information. Further, slowly oscillating
cell assemblies are usually composed of more neurons in comparison to faster oscillating assemblies, with amplitude of oscillation found to be proportional to the number of synchronously
ring neurons (Elul, 1971; Pfurtscheller and Klimesch, 1992;
Pfurtscheller and Lopes da Silva, 1999; Pfurtscheller et al., 1994;
Singer, 1993). The more prevalent and widespread theta-band
activities in the younger infants could suggest the recruitment of
larger neuronal networks during processing of the visual motion
conditions (Pfurtscheller and Lopes da Silva, 1999), a general indication of the involvement of less specialised cortical networks
involved in motion information processing in infancy.
The theta-band activity was more prevalent and widespread in
full-term infants at 4 months compared to preterm infants at
4 months. The less specialised and larger cortical neuronal networks in the full-term infants at 4 months could further help explain the observation of slower perceptual responses (shown by
the longer N2 latencies as stated above) in the full-term infants at
4 months compared to the preterm infants at 4 months whose
responses to visual motion were relatively faster. Considering that
theta-band oscillatory activities were found in all infants both at
4 and 12 months in response to the radial motion stimuli, it is
possible that oscillatory activities within the theta-band frequency
may be a general property of the immature neuronal networks
that are responsible for the processing of motion information in
the rst year of life.
High-amplitude values in the alpha-beta frequency band were
further observed in the full-term infants but only at 12 months.
The alpha-beta frequency was seen as synchronised activities in
the TSE plots over the visual areas of interest. Alpha and beta
rhythms may be important for cross-network functional connectivity (Ganzetti and Mantini, 2013) and may serve to consolidate and link actions across wide areas of the brain (De Pasquale et al., 2010, 2012). Synchronised oscillatory activity that rapidly changes within specic brain circuits may characterize longrange neuronal communication (De Pasquale et al., 2012) that may
enable the progressive maintenance and modulation of different
aspects of task representations within brain circuits (Deco and
Corbetta, 2011; Engel et al., 2001; Gilbert and Sigman, 2007;
Vanni, 1999). The faster oscillating alpha-beta synchronised frequency band activities in the older full-term infants give credence
to the emergence of more specialised functional neuronal networks within the visual areas of the older full-term infants when
processing motion information. These synchronised activities at
higher frequencies may also suggest the involvement of activated
subsets of cortical areas and the use of higher cortical structures
during the global perception of radial motion. Thus, there appeared to have been a progression from the slowly oscillating
theta-band frequency that was particularly prevalent when infants
were younger to the faster alpha-beta frequency band during
processing of radial motion in the older full-term infants. This

S.B. Agyei et al. / Neuropsychologia 84 (2016) 89104

progression may become more apparent as infants develop into

adults since adult studies have implicated increased gamma-band
power in the visual cortex during motion processing (Hoogenboom et al., 2006; Krishnan et al., 2005). The faster gamma-band
frequency is shown to be a more effective way of establishing
rapid coupling between cell assemblies where information processing is more specic and locally conned (Fries, 2005; Fries
et al., 2008; Singer, 1993).
However, unlike the TSEs of the full-term infants at 12 months,
the TSEs of the older preterm infants were observed to show no
synchronised oscillatory activities in the alpha-beta range when
the TSEs of the motion conditions were compared with the static
control pattern. TSEs of the preterm infants at 12 months were still
dominated by activities within the theta-band frequency albeit not
as prevalent as when they were younger. The absence of highfrequency oscillatory activities in the preterm infants at 12 months
may indicate that their cortical growth may have been slower than
the full-term infants as they may not have sufciently developed
specialized neural networks for rapid processing of visual motion
information compared to the full-term infants at 12 months. Since
the dorsal visual stream develops and matures relatively earlier
(Hammarrenger et al., 2007), being born preterm may have disrupted the association bres and synaptic development in the
dorsal stream that help to ne-tune cortical growth during late
foetal and early extrauterine life (Huppi et al., 1998; Kapellou et al.,
2006; Mewes et al., 2006). This disruption in the development of
the dorsal visual stream as a result of the infants being born preterm may have impeded efcient cortical growth and contributed
to the absence of higher frequency oscillatory activities when they
were older. Other studies (e.g., Agyei et al., 2016; Kapellou et al.,
2006) have also suggested slower cortical growth in preterm infants compared to full-terms.
While induced theta-band desynchronisation was observed in
the TSEs of the motion conditions in the infants, induced thetaband synchronisation was rather observed in the TSEs of the static
condition. Neuronal assemblies may have therefore red in synchrony under the perception of the static dot pattern but this
synchronised activity was suppressed when infants perceived the
motion conditions. With task complexity contributing to enhancement of theta desynchronisations (Pfurtscheller et al., 1994),
it is possible that differences in task complexities of the presented
stimuli, from the relatively simple static dot pattern to the more
complex radial motion conditions, may have contributed to these
observed oscillatory differences when perceiving the motion
conditions and the static dot pattern.
In the present longitudinal study, developmental improvements in brain activities as observed in VEPs and TSEs of full-term
and preterm infants when processing radial motion information
were presented. Full-term infants were shown to functionally
discriminate between different patterns of radial motion conditions with age, while preterm infants showed no such developmental differences. In addition, both full-term and preterm infants
showed desynchronised theta-band oscillatory activities when
processing the motion conditions, with only the full-term infants
at 12 months further showing synchronisations in alpha-beta
frequency bands in response to the motion conditions. These improvements in the functional neuronal networks of full-term infants in perceiving visual motion were attributed to neurodevelopmental changes coupled with active locomotor experience. The
poorer responses in the preterm infants were associated with
abnormalities related to visual dorsal stream vulnerabilities. Follow-up studies on the preterm infants, together with more longitudinal research in full-term infants will be carried out in future
to help acquire a better understanding of the developmental
progress of visual motion perception in preterm and full-term
infants. Considering that the present paper studied moderate to

101

very preterm infants, the present ndings should not be generalised to all groups of preterm infants, especially those born below
28 weeks of gestation. Further future research could examine
different groups of premature infants, including those classied as
extremely preterm in order to have a comprehensive understanding of the effects and severity of prematurity on the development of visual motion perception.

Acknowledgements
This project was partly made possible by the Norwegian ExtraFoundation for Health and Rehabilitation. The authors are
grateful to Broen van Besien and Eirik Paulsen for programming
the visual stimuli, and to the parents and their infants for taking
part in the study. They are also grateful to Belde Mutaf for her
contribution during her Master's thesis, and to Magnus Holth and
Kenneth Vilhelmsen for their help with testing, as well as the
neonatologist at St. Olav's University Hospital, Ragnhild Sten, for
her help with the recruitment of the preterm infants.

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