YNIMG-10542; No. of pages: 13; 4C: 5, 6, 7, 8, 9, 10, 11
NeuroImage xxx (2013) xxx–xxx
Contents lists available at SciVerse ScienceDirect
NeuroImage
journal homepage: www.elsevier.com/locate/ynimg
Review
Enhancing dual-task performance with verbal and spatial working memory training:
Continuous monitoring of cerebral hemodynamics with NIRS
Ryan McKendrick a,⁎, Hasan Ayaz b, Ryan Olmstead a, Raja Parasuraman a
a
b
Center of Excellence in Neuroergonomics, Technology, & Cognition (CENTEC), George Mason University, 4400 University Drive, Fairfax, VA 2230, USA
School of Biomedical Engineering, Science & Health Systems, Drexel University, 3141 Chestnut Street, Philadelphia, PA 19104, USA
a r t i c l e
i n f o
Article history:
Accepted 23 May 2013
Available online xxxx
Keywords:
Working memory training
Near infrared spectroscopy
Dorsolateral prefrontal cortex
Ventrolateral prefrontal cortex
Hemodynamics
a b s t r a c t
To better understand the mechanisms by which working memory training can augment human performance
we continuously monitored trainees with near infrared spectroscopy (NIRS) while they performed a dual
verbal–spatial working memory task. Linear mixed effects models were used to model the changes in
cerebral hemodynamic response as a result of time spent training working memory. Nonlinear increases in
left dorsolateral prefrontal cortex (DLPFC) and right ventrolateral prefrontal cortex (VLPFC) were observed
with increased exposure to working memory training. Adaptive and yoked training groups also showed
differential effects in rostral prefrontal cortex with increased exposure to working memory training. There
was also a significant negative relationship between verbal working memory performance and bilateral
VLPFC activation. These results are interpreted in terms of decreased proactive interference, increased neural
efficiency, reduced mental workload for stimulus processing, and increased working memory capacity with
training.
© 2013 Elsevier Inc. All rights reserved.
Contents
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . .
Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Participants . . . . . . . . . . . . . . . . . . . . . . . . .
Working memory tasks . . . . . . . . . . . . . . . . . . .
Training . . . . . . . . . . . . . . . . . . . . . . . . . .
Imaging . . . . . . . . . . . . . . . . . . . . . . . . . . .
NIRS data processing . . . . . . . . . . . . . . . . . . . .
Statistical model selection . . . . . . . . . . . . . . . . . .
Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Analysis, multiple comparison corrections, and contrasts . . . .
Behavioral performance . . . . . . . . . . . . . . . . . . .
Training day effects . . . . . . . . . . . . . . . . . . . . .
Training day by training condition interactions . . . . . . . .
Behavioral performance by hemodynamic response correlations
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Introduction
⁎ Corresponding author at: George Mason University, 4400 University Drive, MS 3F5,
Fairfax, VA 2230, USA.
E-mail address: rmckend2@gmu.edu (R. McKendrick).
The augmentation of human performance and its transfer to
improved functioning at work or in everyday settings via alteration of
underlying neurocognitive processes is a prime goal of neuroergonomics
1053-8119/$ – see front matter © 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.neuroimage.2013.05.103
Please cite this article as: McKendrick, R., et al., Enhancing dual-task performance with verbal and spatial working memory training: Continuous
monitoring of cerebral hemodynamics with NIRS, NeuroImage (2013), http://dx.doi.org/10.1016/j.neuroimage.2013.05.103
2
R. McKendrick et al. / NeuroImage xxx (2013) xxx–xxx
(Parasuraman, 2011; Parasuraman et al., 2012). Training to increase
working memory capacity (WMC) represents one potential method for
such neurocognitive enhancement. Working memory represents a
capacity limited process for the encoding, manipulation, and storage of
task relevant information for use by higher order cognitive processes
(Baddeley, 1986). Individuals with high WMC have been found to exhibit
superior focused visual attention (Engle, 2002), improved time critical
decision making (Endsley, 1995) and even enhanced supervisory
control of unmanned aerial vehicles (de Visser et al., 2010; McKendrick
et al., 2011). A growing body of research also suggests that WMC
can be improved in healthy adults, so that normal age-related or
degeneratively-linked declines in cognitive function may possibly be
minimized (see Buschkuehl et al., 2012; Klingberg, 2010; Chein and
Morrison, 2010 for reviews).
It is well established that repeated practice on simple span working
memory recall and working memory updating improves performance
on such tasks. After such training trainees are able to recall spans of
greater length and manipulate working memory information with less
forgetting. However, whether such improvement transfers to other
tasks, including higher functions required for everyday cognitive functioning, has proven more difficult to show. In other words, “far transfer”
of working memory training remains controversial. Early studies
showed robust transfer effects to other measures of general intelligence
such as Raven's progressive matrices (Klingberg et al., 2002). However
recent reviews (Hulme and Melby-Lervåg, 2012; Shipstead et al.,
2012) and a meta-analysis (Melby-Lervåg and Hulme, 2013) suggest
that the evidence for far transfer is minimal at best. Suboptimal transfer
effects may be a result of the use of simple span and updating working
memory tasks, rather than complex tasks, as well as the usage of
suboptimal training parameters. It has been suggested that the use of
complex span tasks, training on different variants of working memory,
increased practice span length, and more liberal criteria for adaptive
training advancement, are factors that need to be accounted for to afford
more efficient WMC improvement and far transfer (Gibson et al., 2012).
The success of working memory training and its potential for
transfer to higher order functioning has generated interest in understanding its underlying neural mechanisms. Various brain imaging
modalities, including both structural (Magnetic Resonance Imaging;
MRI) and functional (Functional Magnetic Resonance Imaging; fMRI,
Electroencephalogram; EEG) imaging, have been used to uncover
the underlying neural plasticity. The literature suggests that training
can alter the brain in multiple ways, such as increased gray matter
volume (Draganski et al., 2004, 2006; Hamzei et al., 2012; Taubert
et al., 2010), increased and decreased white matter fiber tract density
(Scholz et al., 2009; Taubert et al., 2010), increases and decreases in
the BOLD fMRI response (Dahlin et al., 2008; Jonides, 2004; Moore
et al., 2006; Olesen et al., 2004), and increased frontal-midline EEG
theta power (Dopplemayr et al., 2008; Gevins et al., 1997; Smith et al.,
1999). Short term working memory training is associated with
decreases in hemodynamic response in dorsolateral prefrontal cortex
(DLPFC) (Garavan et al., 2000; Jansma et al., 2001; Landau et al., 2004,
2007; Sayala et al., 2006; Schneiders et al., 2011), while prolonged training has been linked to an increase in hemodynamic response of DLPFC
(Dahlin et al., 2008; Jolles et al., 2010; Jonides, 2004; Olesen et al.,
2004; Westerberg and Klingberg, 2007). Working memory training
has also been linked to increases in white matter fiber tract density in
the anterior body of the corpus callosum which connects bilaterally
the DLPFC, thereby potentially improving information transfer between
the left and right DLPFC (Takeuchi et al., 2010). It is believed that
increases in DLPFC activity diminish inhibitory signals to intraparietal
sulcus (IPS) and mediate an increase in WMC (Edin et al., 2009).
Training related changes in DLPFC are also accompanied by evidence
for an increase in the ventrolateral prefrontal cortex (VLPFC) BOLD
response and neuronal recruitment during the maintenance of working
memory representations (Meyer et al., 2011; Moore et al., 2006; Qi
et al., 2011). These effects are consistent with other research in which
VLPFC activation has been implicated in the resolution of proactive
interference between working memory representations and concurrent
distracter representations (Badre and Wagner, 2007; Badre et al., 2005).
Therefore increased hemodynamic response in VLPFC and DLPFC is
expected as a result of working memory training.
Previous studies of working memory training have typically used a
pre- and post-training design, in which neurocognitive changes are
assessed before and after training. One reason for the use of such a
design is due to the high cost of multiple fMRI scans. However, neural
changes are likely to occur continuously throughout training, and it
would be of interest to see how such changes are linked to performance.
Accordingly, the present study focused on continuous changes in
cerebral hemodynamics, using a method that is well suited to repeated
imaging, near infrared spectroscopy (NIRS). NIRS uses specific wavelengths of light to measure changes in oxygenated and deoxygenated
hemoglobin and the NIRS signal is correlated with the fMRI BOLD as
both measure hemodynamic response, especially in brain regions
more proximal to the scalp such as the frontal cortex (Cui et al., 2011).
To accurately isolate changes in the hemodynamic response as a
result of working memory performance compared to changes due to
non-specific increases in mental effort, we compared two training conditions: A traditional adaptive condition whose working memory load
was adjusted based on the trainee's performance, and a yoked condition
whose working memory load was adjusted based on the performance of
trainees in the adaptive condition. Since task demands are not matched
to the capabilities of yoked-trainees we would expect them to expend
more mental effort in order to perform the task. Evidence for this
would be represented as an increase in hemodynamic response in PFC
for the yoked training condition. At the same time, task demands are
matched to the capabilities of adaptive-trainees, therefore we would
expect to see them exhibit a decrease or little change in hemodynamic
response in PFC due to minimal changes in required mental effort.
In addition, to improve the efficacy of the working memory training
design, we implemented the suggestions for optimal training proposed
by Gibson et al. (2012). Our task tested two components of working
memory; spatial working memory which requires the encoding and
retrieval of spatial locations, and verbal working memory which
requires the encoding and retrieval of semantic content. Memory for
the two working memory components was temporally combined in
order to tax the updating and executive control components associated
with working memory (Baddeley, 1986). In order to avoid ceiling
effects and challenge trainees, load for verbal and spatial working memory was set to a range beyond what is considered the average capacity
limit (spatial: 4 chunks, verbal: 7 chunks). We expected an increase in
verbal working memory performance over time, with moderate
changes in spatial working memory performance (McKendrick and
Parasuraman, 2012).
In summary, as an effect of working memory training, we anticipated
an increase in verbal working memory performance along with moderate
changes in spatial working memory performance as training progressed.
We also expected to observe an inverse relationship in PFC hemodynamic
response between the two training conditions as an effect of training.
Finally orthogonal to the hypothesized condition by training interaction, we expected an increase in hemodynamic response in both
DLPFC and VLPFC as an effect of working memory training.
Methods
Participants
Ten right handed adults were recruited for participation in working
memory training sessions over five days. All had normal or corrected to
normal vision and signed an informed consent form approved by the
George Mason Institutional Review Board before participating in the
study. Five participants were randomly assigned to each of two training
conditions.
Please cite this article as: McKendrick, R., et al., Enhancing dual-task performance with verbal and spatial working memory training: Continuous
monitoring of cerebral hemodynamics with NIRS, NeuroImage (2013), http://dx.doi.org/10.1016/j.neuroimage.2013.05.103
R. McKendrick et al. / NeuroImage xxx (2013) xxx–xxx
Working memory tasks
Participants received training and performed the working memory
task on a desktop PC running Matlab and Psychophysics Toolbox. The
experimental task consisted of two concurrently presented working
memory span tasks, verbal span and spatial span. Stimuli for the verbal
span task consisted of a string of gray numbers presented on a black
background. The length of the string varied across training sessions.
All participants began with verbal span load being randomly assigned
as seven, eight, or nine digit strings for a given trial, trainees saw
three examples of each load level within a training block. Each digit
within the string was also randomly selected and ranged from 1 to 9.
All the numbers in the string were presented simultaneously and
ordered left to right across the screen. The display duration of the string
was yoked to the length of the string. Each digit contributed .4 s to the
display duration of the string. Verbal span performance was defined as
the number of digits reported correctly and in the correct order. Inputting more digits than initially specified in the string to be remembered
was penalized. If a participant was presented with seven digits and
inputted 8 digits, the number of presented digits was divided by the
number of inputted digits, the quotient was then multiplied by the
number of digits correctly reported to arrive at the trainee's performance score for that trial.
The stimuli for the spatial task consisted of black circles presented
simultaneously over a gray background. The number of circles presented
varied across training conditions. All participants began with spatial
span load being randomly assigned as five, six, or seven circles for a
given trial, trainees saw three examples of each load level within a training block The spatial location for each circle was randomly chosen with
the only caveat being that the center of one circle had to be greater than
150 pixels from the center of any other circle displayed. All the circles
were presented simultaneously across the screen. The spatial task
stimuli were presented for 1 s. Spatial span performance was defined
as the number of circles reported correctly and in the correct location.
Inputting more circles than initially specified in the display to be
remembered was penalized. If a participant was presented with five
circles and inputted six circles, the number of presented circles was
divided by the number of inputted circles, the quotient was then multiplied by the number of circles correctly reported to arrive at the trainee's
performance score for that trial.
Each trial began with the presentation of the verbal stimuli
followed directly by the presentation of the spatial stimuli. The spatial
3
stimuli were followed by a random noise mask that was displayed for
4 s. Following the mask participants were instructed to respond to the
spatial stimuli by using a standard computer mouse and pressing the
left mouse button on the location where a circle had been presented.
Participants were instructed to reproduce the pattern of spatial stimuli
locations exactly, and to press the space bar once they had finished
responding. After responding to the spatial stimuli participants
responded to the verbal stimuli by pressing the number keys at the
top of a QWERTY keyboard. Participants were instructed to reproduce
the span exactly, and to press the space bar when they were finished
(Fig. 1).
Training
Participants trained for 2 h each day for five consecutive days,
resulting in 10 total hours of training. Daily training was separated
into two 1 h sessions with a 15 min break between training sessions.
Within a given training sessions participants performed 10 training
blocks and each training block consisted of nine trials of the dual
working memory task.
Participants were randomly assigned to two training conditions, an
adaptive and a yoked condition. In the adaptive condition the span
difficulty that participants were exposed to on subsequent days of
training was a product of their previous days' performance. If participants in the adaptive condition responded with 80% or greater performance in a component of the dual working memory task working
memory load of that component was increased by dropping the lowest span load and replacing it with a load level one greater than the
previous highest load. For example if an adaptive-trainee on the first
day of training correctly reported 85% of the digits presented in the
verbal span task averaged across load than their working memory
load was increased on the second day of training. Since this was the
first day of training the trainee was seeing loads of five, six, and
seven digits, on the second day of training the trainee would be
presented with loads of six, seven, and eight digits. Participants in
the yoked condition saw the same difficulty levels as those seen by
the adaptive condition but the difficulty changes were dictated not
by their performance but by the performance of the individual in the
adaptive condition to which they were yoked. Yoked pairings were
constrained by trainee gender, with males being yoked only to males
and females only to females.
Fig. 1. Dual verbal–spatial working memory task representation: (1) verbal span stimuli, duration: 2.8–4.0 s., (2) spatial span fixation, duration: 0.2 s., (3) spatial span stimuli,
duration: 1.0 s., (4) random noise mask, duration: 4.0 s., (5) response to spatial span, (6) response to verbal span, duration: trainee controlled.
Please cite this article as: McKendrick, R., et al., Enhancing dual-task performance with verbal and spatial working memory training: Continuous
monitoring of cerebral hemodynamics with NIRS, NeuroImage (2013), http://dx.doi.org/10.1016/j.neuroimage.2013.05.103
4
R. McKendrick et al. / NeuroImage xxx (2013) xxx–xxx
Table 2
Hemodynamic changes as a function of day and training condition.
Source
Imaging
We used a continuous wave fNIR Device model 1100 fNIR system
(fNIR Devices LLC, Photomac MD; www.fnirdevices.com) to image
cerebral hemodynamics of prefrontal cortex. At the beginning of each
training block, the participant was connected to the fNIR system and
their baselines were taken while participants visually fixated on a
central cross presented on the computer screen. Activation of each
participant's prefrontal cortex was monitored throughout the entire
time participants were trained on the dual working memory task. The
sensor had a temporal resolution of 500 ms per scan with 2.5 cm
source–detector separation allowing for approximately 1.25 cm penetration depth. The dual-wavelength light emitting diodes (LEDs) were
activated in turn one light source and wavelength at a time and the
four surrounding photodetectors around the active source were sampled. The positioning of light source and detectors on the sensor pad
yielded a total of 16 active optodes (Fig. 2). COBI Studio software (Drexel
University) was used for data acquisition and visualization (Ayaz et al.,
2011).
NIRS data processing
For each participant, raw fNIR data (16 optodes × 2 wavelengths)
were low-pass filtered with a finite impulse response, linear phase
filter with order 20 and cut-off frequency of 0.1 Hz to attenuate the
Table 1
Behavioral changes as a function of day and training condition.
Source
Main effects
dfnum
Verbal span performance
Day
4.00
Condition
1.00
Day × condition 4.00
Adaptive
Yoked
Spatial span performance
Day
4.00
Polynomial contrasts
dfden
F
Linear
Quadratic
981.00
8.00
981.00
60.18⁎⁎⁎
0.14
15.37⁎⁎⁎
14.26⁎⁎⁎
−4.20⁎⁎⁎
4.35⁎⁎⁎
13.82⁎⁎⁎
5.53⁎⁎⁎
−1.29
−5.15⁎⁎⁎
3.23⁎⁎
2.92⁎⁎
5.54⁎⁎⁎
−7.14⁎⁎⁎
985.00
22.77⁎⁎⁎
Cubic
−0.11
Polynomial contrasts = least squares t-ratios.
Denominator degrees of freedom calculated with Kenward–Rogers corrections.
Random effects specified as random intercept for each participant.
⁎⁎ p b .01.
⁎⁎⁎ p b .001.
Polynomial contrasts
dfnum
dfden
Optode 3 HbO2
Day
Condition
Day × condition
4.00
1.00
4.00
891.57
8.00
891.59
3.49⁎⁎
1.13
2.44
1.43
−0.65
3.30⁎⁎
Optode 3 total Hb
Day
Condition
Day × condition
4.00
1.00
4.00
891.51
8.00
891.53
3.66⁎⁎
1.09
2.77
2.44⁎
−1.27
2.24⁎
4.00
1.00
1.00
4.00
944.93
7.86
528.46
942.79
1.94
1.28
7.98⁎⁎
7.53⁎⁎⁎
2.47⁎
0.68
2.48⁎
−4.44⁎⁎⁎
−1.79
0.65
2.29⁎
0.30
1.02
−2.97⁎⁎
−0.10
1.51
Optode 4 HbR
Day
Condition
Digit performance
Day × condition
Adaptive
Yoked
Fig. 2. Registration of 16 optodes (measurement locations) across prefrontal cortex
(Ayaz et al., 2012).
Main effects
Optode 4 Hbo2
Day
Condition
Digit performance
Day × condition
Adaptive
Yoked
4.00
1.00
1.00
4.00
946.04
7.92
781.69
944.12
F
Linear
1.53
0.23
9.66⁎⁎
4.60⁎⁎
Quadratic
Cubic
Optode 5 HbO2
Day
Condition
Day × condition
4.00
1.00
4.00
844.79
8.00
844.82
6.17⁎⁎⁎
0.26
0.71
2.69⁎⁎
−1.19
3.85⁎⁎⁎
Optode 5 total Hb
Day
Condition
Day × condition
4.00
1.00
4.00
845.83
8.00
845.87
3.33⁎
0.52
1.12
2.33⁎
−0.96
2.42⁎
4.00
1.00
4.00
877.50
8.00
877.50
0.33
0.25
5.28⁎⁎⁎
Optode 9 HbR
Day
Condition
Day × condition
Adaptive
Yoked
Optode 9 HbO2
Day
Condition
Day × condition
Adaptive
Yoked
Optode 9 total Hb
Day
Condition
Day × condition
Adaptive
Yoked
Optode 11 HbR
Day
Condition
Day × condition
Adaptive
Yoked
Optode 11 HbO2
Day
Condition
Day × condition
Adaptive
Yoked
1.74
−0.84
4.00
1.00
4.00
4.00
1.00
4.00
4.00
1.00
4.00
4.00
1.00
4.00
Optode 11 total Hb
Day
4.00
Condition
1.00
Day × condition
4.00
Adaptive
Yoked
878.31
8.00
878.33
876.32
8.00
876.34
890.81
7.98
891.13
889.60
8.00
889.72
889.59
8.00
889.71
3.58⁎⁎
0.18
3.97⁎⁎
1.93
0.34
6.18⁎⁎⁎
0.17
0.01
11.53⁎⁎⁎
−1.57
2.52⁎
1.50
−1.67
3.07⁎⁎
3.09⁎⁎
−0.85
0.08
−2.40⁎
0.92
3.37⁎⁎⁎
3.25⁎⁎
−1.04
1.30
−2.59⁎⁎
−0.14
3.27⁎⁎
1.95
−2.38⁎
3.81⁎⁎⁎
−2.55⁎
−1.97⁎
1.10
2.93⁎⁎
−2.65⁎⁎
1.33
−1.57
−0.44
0.91
3.75⁎⁎⁎
−3.18⁎⁎
3.52⁎⁎⁎
−2.38⁎
−1.61
1.21
0.96
0.16
8.67⁎⁎⁎
0.22
0.02
5.89⁎⁎⁎
2.35⁎
−1.69
Please cite this article as: McKendrick, R., et al., Enhancing dual-task performance with verbal and spatial working memory training: Continuous
monitoring of cerebral hemodynamics with NIRS, NeuroImage (2013), http://dx.doi.org/10.1016/j.neuroimage.2013.05.103
R. McKendrick et al. / NeuroImage xxx (2013) xxx–xxx
Table 2 (continued)
Source
Optode 12 HbR
Day
Condition
Day × condition
Adaptive
Yoked
Optode 12 HbO2
Day
Condition
Day × condition
Adaptive
Yoked
Main effects
dfnum
dfden
4.00
1.00
4.00
868.50
7.99
868.63
4.00
1.00
4.00
Optode 12 total Hb
Day
4.00
Condition
1.00
Day × condition
4.00
Adaptive
Yoked
869.81
8.00
869.90
868.94
8.00
869.04
Polynomial contrasts
F
Linear
Quadratic
Cubic
0.91
−1.45
3.61⁎⁎⁎
−2.43⁎
−1.23
2.93⁎⁎
2.31⁎
−2.67⁎⁎
0.83
−1.00
−0.57
1.96
2.07⁎
−2.86⁎⁎
2.56⁎
−1.86
−1.38
2.89⁎⁎
0.87
0.25
6.87⁎⁎⁎
0.22
0.01
5.34⁎⁎⁎
0.37
0.01
8.41⁎⁎⁎
Optode 14 total Hb
Day
4.00
Condition
1.00
Day × condition
4.00
855.20
8.00
855.60
3.77⁎⁎
0.12
3.05
3.08⁎⁎
−2.02⁎
0.90
Optode 16 HbR
Day
Condition
Day × condition
4.00
1.00
4.00
947.06
8.00
947.06
4.05⁎⁎
0.96
0.83
2.16⁎
−2.67⁎⁎
2.10⁎
Optode 16 HbO2
Day
Digit performance
4.00
1.00
955.13 10.39⁎⁎⁎
836.60 10.07⁎⁎
3.71⁎⁎⁎ −4.91⁎⁎⁎
2.62⁎⁎
11.98⁎⁎⁎
7.92⁎⁎
3.99⁎⁎⁎ −4.98⁎⁎⁎
3.32⁎⁎⁎
Optode 16 total Hb
Day
4.00
Digit performance 1.00
954.34
807.96
Polynomial contrasts = least squares t-ratios.
Denominator degrees of freedom calculated with Kenward–Rogers corrections.
Random effects specified as random intercept for each participant.
⁎ p b .05.
⁎⁎ p b .01.
⁎⁎⁎ p b .001.
5
high frequency noise, respiration and cardiac cycle effects (Ayaz et al.,
2010; Izzetoglu et al., 2005). Each participant's data was checked for
any potential saturation (when light intensity at the detector was
higher than the analog-to-digital converter limit) and motion artifact
contamination by means of a coefficient of variation based assessment
(Ayaz et al., 2010). It was of particular importance to control for motion
based artifacts in the present study, as the NIRS signal in VLPFC has been
shown to be sensitive to task concurrent motion (Schecklmann et al.,
2010). fNIR data for each training block were extracted using time
synchronization markers received through serial port during the experiment and hemodynamic changes for each of 16 optodes during each
trial block were calculated separately using the Modified Beer Lambert
Law (MBLL). The hemodynamic response at each optode was averaged
across time for each trial block to provide a mean hemodynamic
response at each optode for each block. The final output of each optode
was mean block deoxygenated hemoglobin (HbR), mean block oxygenated hemoglobin (HbO2), and the sum of the first to measures represented as mean block total hemoglobin (Total Hb).
Statistical model selection
We used linear mixed effects models to estimate effects of training
on cerebral hemodynamics and behavioral performance. Linear mixed
effects models offer advantages over repeated measures ANOVA when
modeling hemodynamic change over time. They do not require an
equal number of observations per participant. Linear mixed effects
models allow for the estimation of parameters unique to individual
participants. Furthermore linear mixed effects models allow for time
to be modeled as a continuous variable, therefore temporal change
can also be modeled nonlinearly (Baayen et al., 2008; Krueger and
Tian, 2004; Laird and Ware, 1982). Models only containing fixed effects
were fitted first. Behavioral performance and hemodynamic responses
were specified as dependent variables. The Akaike information criterion
corrected for sample size (AICc) was used to select the most parsimonious model (Akaike, 1973) of fixed effects; if there was less than a difference of two in AICc (Burnham and Anderson, 2002) between the
two most parsimonious models, the simpler model containing fewer
parameters was selected. After the most parsimonious fixed effects
were determined, random effects were selected once again using AICc
Fig. 3. Average number of correct digits reported for the verbal span task for a training block as a factor of training group (A—adaptive, B—yoked), day, and trainee. Line of fit is
representative of mixed model estimate for significant polynomial factors.
Please cite this article as: McKendrick, R., et al., Enhancing dual-task performance with verbal and spatial working memory training: Continuous
monitoring of cerebral hemodynamics with NIRS, NeuroImage (2013), http://dx.doi.org/10.1016/j.neuroimage.2013.05.103
6
R. McKendrick et al. / NeuroImage xxx (2013) xxx–xxx
Fig. 4. Average number of correct locations reported for a training block as a factor of day, and trainee. Line of fit is representative of mixed model estimate for significant polynomial
factors.
to assess model fit. If there was competition between the top two
models the model with fewer parameters was selected for further
analysis.
Table 1, and the results of the hemodynamic analyses are presented in
Table 2.
Behavioral performance
Results
Analysis, multiple comparison corrections, and contrasts
To test for changes in behavioral performance and hemodynamics,
final models were analyzed as linear mixed effects models with restricted
maximum likelihood (REML) using lme4 in R (Bates and Sarkar, 2007).
F tests were approximated with Kenward–Roger corrections for denominator degrees of freedom (Kenward and Roger, 1997). Benjamini–
Hockberg corrections with q specified at .05 were applied to effects for
a given hemodynamic response across optodes to control for false discovery error rate (Benjamini and Hochberg, 1995; Verhoeven et al.,
2005). Orthogonal polynomial contrasts were applied to significant
effects to further model behavioral and hemodynamic changes over
time. The results of the behavioral analyses are summarized in
Performance on the verbal span task increased over training day,
being best modeled as a cubic function. Differences between training
groups were modeled by a significant negative quadratic component
for the yoked training condition, representing a slowing of skill development on the third and fourth days of training relative to the adaptive
condition (Fig. 3). Performance on the spatial span task was best
modeled as a negative quadratic function for both training conditions
(Fig. 4).
Training day effects
Both training conditions showed an increase in hemodynamic
response in optodes 3, 5, 14 and 16, being best modeled as a cubic function (Fig. 5–8). During the first two days of training all four optodes
Fig. 5. Optode-3 average HbO2 levels for a training block as a factor of day, and trainee. Line of fit is representative of mixed model estimate for significant polynomial factors.
Please cite this article as: McKendrick, R., et al., Enhancing dual-task performance with verbal and spatial working memory training: Continuous
monitoring of cerebral hemodynamics with NIRS, NeuroImage (2013), http://dx.doi.org/10.1016/j.neuroimage.2013.05.103
R. McKendrick et al. / NeuroImage xxx (2013) xxx–xxx
7
Fig. 6. Optode-5 average HbO2 levels for a training block as a factor of day, and trainee. Line of fit is representative of mixed model estimate for significant polynomial factors.
showed a linear increase in hemodynamic response. Optodes 3, 14, and
16 showed an increase continuing to day three, and specifically optode
14 showed an increase in response up until the fourth day of training.
Optode 5 showed a decrease in response on days three and four and
optodes 3 and 16 showed a similar response but only for day four. Response in optodes 3, 5, 14, and 16 increased again on the final day of
training.
Training day by training condition interactions
Significant day by training condition interactions were found in
optodes 4, 9, 11, and 12 (Fig. 9–12). The hemodynamic response of
the adaptive condition had either positive linear and or quadratic
components: the response tended to decrease over the first three
days of training and then increase on the fourth and fifth days. In
contrast, the hemodynamic response of the yoked condition in optodes
4, 9, 11, and 12 was best modeled with negative linear and or quadratic
components: the response of this group tended to increase after the first
day of training until the third day, after which the response declined on
the fourth day.
Behavioral performance by hemodynamic response correlations
Behavioral response variables were included in models for optodes
with a significant effect of training day when they could parsimoniously
explain further variance in the hemodynamic response. A relationship
was found in optodes 4 and 16 between the hemodynamic response
and behavioral performance on the verbal span task (Fig. 13–14). In
both cases increases in performance on the verbal span task were
accompanied by decreases in the hemodynamic response at optodes 4
and 16.
Discussion
We continuously monitored cerebral hemodynamic changes in
the prefrontal cortex in two groups of participants—an adaptive and
a yoked control training condition—while they were trained on a
dual verbal–spatial working memory task. As expected, verbal span
and spatial span increased with training: increases in verbal span later
in training were accompanied by decreases in spatial span as individuals
focused more on improving their verbal span. We believe that this
Fig. 7. Optode-14 average total Hb levels for a training block as a factor of day, and trainee. Line of fit is representative of mixed model estimate for significant polynomial factors.
Please cite this article as: McKendrick, R., et al., Enhancing dual-task performance with verbal and spatial working memory training: Continuous
monitoring of cerebral hemodynamics with NIRS, NeuroImage (2013), http://dx.doi.org/10.1016/j.neuroimage.2013.05.103
8
R. McKendrick et al. / NeuroImage xxx (2013) xxx–xxx
Fig. 8. Optode-16 average HbO2 levels for a training block as a factor of day, and trainee. Line of fit is representative of mixed model estimate for significant polynomial factors.
pattern is due to skill acquisition being easier in the verbal task relative
to the spatial task (McKendrick and Parasuraman, 2012). Differences in
the behavioral performance of the training conditions did not become
apparent until the final two days of training where the yoked control
group appeared to reach a performance limit and could no longer
keep pace with the adaptive group.
Behavioral differences between training conditions informed the
interpretation of the cerebral hemodynamic differences. As predicted,
we observed an increase in hemodynamic response for the yoked
control condition. This was specifically observed in the right rostral
prefrontal cortex during the first three days of training. In the same
region, in the adaptive condition there was a decrease in hemodynamic
response over the same time period. Following the third day the
response in the yoked condition decreased and the response in the
adaptive condition increased (Fig. 15). The rostral prefrontal cortex is
believed to be involved in the monitoring and processing of sensory
stimuli during multitasking (Burgess et al., 2005). The NIRS signal has
reduced sensitivity in this region due to increased scalp to cortex
distance (Haeussinger et al., 2011; Heinzel et al., 2013). While we did
find a robust interaction within rostral prefrontal cortex as predicted,
there is a possibility that other effects in this region were obscured by
reduced signal sensitivity.
Overall the interactions within rostral prefrontal cortex suggest
that in order to keep pace with the performance of the adaptive group
the yoked group had to apply considerably more effort in maintaining
and processing dual task representations. Furthermore, towards the
end of training the adaptive group had to increase the effort applied
to processing dual task representations to improve their performance.
At the same time the yoked group may have become fatigued due to
the high level of effort required on the first three days of training.
Fig. 9. Optode-4 average HbO2 levels for a training block as a factor of training group, day, and trainee. Line of fit is representative of mixed model estimate for significant polynomial
factors.
Please cite this article as: McKendrick, R., et al., Enhancing dual-task performance with verbal and spatial working memory training: Continuous
monitoring of cerebral hemodynamics with NIRS, NeuroImage (2013), http://dx.doi.org/10.1016/j.neuroimage.2013.05.103
R. McKendrick et al. / NeuroImage xxx (2013) xxx–xxx
9
Fig. 10. Optode-9 average HbO2 levels for a training block as a factor of training group, day, and trainee. Line of fit is representative of mixed model estimate for significant
polynomial factors.
Irrespective of condition differences, we observed changes in the
hemodynamic response of left DLPFC and right VLPFC as a result of
training (Fig. 16). As predicted, the hemodynamic response increased
with time spent on training working memory. However, the changes
not only were linear but also contained significant linear, quadratic
and cubic components. Importantly, non-linear changes over time
would not have been observed if a pre-/post-training design commonly
used in fMRI studies had been used. Hemodynamic increases in right
VLPFC suggest a reduction in proactive interference improving the
maintenance of working memory representations (Badre and Wagner,
2007; Moore et al., 2006; Qi et al., 2011). This effect could be a result of
the dual-task nature of our training methodology. However right PFC
activation as a result of inhibition of irrelevant stimuli during working
memory has been previously observed via NIRS (Schreppel et al.,
2008). It is possible that increased training reduced the proactive
interference between concurrent verbal and spatial working memory
representations, making their simultaneous maintenance easier and
facilitating greater representation capacity. The increased hemodynamic
response in left DLPFC may have been representative of the top down
influence of the IPS, increasing its activity thereby increasing working
Fig. 11. Optode-11 average total Hb levels for a training block as a factor of training group, day, and trainee. Line of fit is representative of mixed model estimate for significant
polynomial factors.
Please cite this article as: McKendrick, R., et al., Enhancing dual-task performance with verbal and spatial working memory training: Continuous
monitoring of cerebral hemodynamics with NIRS, NeuroImage (2013), http://dx.doi.org/10.1016/j.neuroimage.2013.05.103
10
R. McKendrick et al. / NeuroImage xxx (2013) xxx–xxx
Fig. 12. Optode-12 average total Hb levels for a training block as a factor of training group, day, and trainee. Line of fit is representative of mixed model estimate for significant
polynomial factors.
memory capacity (Edin et al., 2009). We also note the lack of difference
between training groups in their hemodynamic response in these
regions, suggesting that these changes are not representative of changes
in mental effort.
Changes in prefrontal hemodynamic response as an effect of training
were accompanied by negative correlations between the verbal span
performance and the hemodynamic response in bilateral VLPFC. Negative relationships between performance and hemodynamic response
in frontal brain regions are generally interpreted as an increase in processing efficiency (Kelly and Garavan, 2005; Neubauer and Fink, 2009;
Poldrack, 2000). This increase in efficiency during multitasking can
potentially manifest as an increase in automatic processing in task
specific pathways, the creation of independent streams of processing
for each task, or an increase in processing speed due to improved
response selection. The strongest support has been found for an improvement in processing efficiency via an increase in processing speed
due to improved response selection (Dux et al., 2009). Therefore we
take the negative relationship between verbal performance and hemodynamic response to suggest an increase in the speed of retrieval for
verbal working memory representations.
Conclusion
NIRS provides an efficient and effective way to continuously monitor
hemodynamic changes over extended periods of time, as required in
training studies. In addition, portable NIRS systems are being developed
Fig. 13. Optode-4 average HbO2 levels for a training block as a factor of average number of correct digits reported on the verbal span task. Line of fit is representative of linear mixed
model estimate.
Please cite this article as: McKendrick, R., et al., Enhancing dual-task performance with verbal and spatial working memory training: Continuous
monitoring of cerebral hemodynamics with NIRS, NeuroImage (2013), http://dx.doi.org/10.1016/j.neuroimage.2013.05.103
R. McKendrick et al. / NeuroImage xxx (2013) xxx–xxx
11
Fig. 14. Optode-16 average HbO2 levels for a training block as a factor of average number of correct digits reported on the verbal span task. Line of fit is representative of linear
mixed model estimate.
Fig. 15. Mean total Hb (B-spline interpolated) as a factor of day and training group.
as part of mobile brain imaging (MoBI) initiatives (Makeig et al., 2009).
Consistent with the goals of neuroergonomics (Parasuraman, 2011;
Parasuraman et al., 2012), NIRS technologies could be used to measure
the effects of training in complex real world tasks where the use of fMRI
would be challenging or impossible. Furthermore, the inclusion of linear
mixed effects models to NIRS measurement affords a robust and powerful means of cataloging hemodynamics over time.
Working memory training is a potentially efficacious method of
neurocognitive enhancement. The present study examined the effects
of such training and its underlying neural correlates using an optimal
training methodology, a complex working memory task, and a continuous monitoring of cerebral hemodynamics over the course of training.
The results suggests that adaptive working memory training improves
working memory performance by one of at least four mechanisms:
(1) a reduction in proactive interference during representation maintenance due to increased recruitment of VLPFC; (2) an increase in
working memory capacity via top down disinhibition of IPS by DLPFC;
(3) an increased efficiency of retrieval due to increased processing
speed during response selection; and (4) not over taxing mental
resources during the monitoring and processing of relevant stimuli.
Fig. 16. Mean HbO2 (B-spline interpolated) as a factor of day.
Please cite this article as: McKendrick, R., et al., Enhancing dual-task performance with verbal and spatial working memory training: Continuous
monitoring of cerebral hemodynamics with NIRS, NeuroImage (2013), http://dx.doi.org/10.1016/j.neuroimage.2013.05.103
12
R. McKendrick et al. / NeuroImage xxx (2013) xxx–xxx
Additional work is needed before firm conclusions can be reached
on the efficacy of working memory training as a method of
neuroenhancement. Future work should examine larger samples of
participants and greater periods of training. It would also be important
to investigate hemodynamic response on a trial by trial basis within
both prefrontal and parietal cortices so that training effects on proactive
interference, disinhibition, and response selection can be more directly
assessed. Finally, consistent with the neuroergonomic approach,
evidence of transfer to complex and ecologically relevant tasks would
need to be obtained in order to establish the usefulness of working
memory training.
Acknowledgments
This research was supported by Air Force Office of Scientific
Research grant FA9550-10-1-0385, and the Center of Excellence in
Neuroergonomics, Technology, and Cognition (CENTEC). We thank
Emily Marszalkowski, Rabia Murtza, and Molly Owens for their assistance
in data acquisition. We also thank Harry Haladjian for supplying the code
that became the spatial working memory component of our training task
and Patrick McKnight for comments on the data analysis. The views,
opinions, and/or findings contained in this article are those of the authors
and should not be interpreted as representing the official views or
policies, either expressed or implied, of the funding agencies.
Disclosure statement
fNIRDevices, LLC manufactures the optical brain imaging instrument and licensed IP and know-how from Drexel University. H.Ayaz
was involved in the technology development and thus offered a
minor share in the new start up firm fNIRDevices, LLC.
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Please cite this article as: McKendrick, R., et al., Enhancing dual-task performance with verbal and spatial working memory training: Continuous
monitoring of cerebral hemodynamics with NIRS, NeuroImage (2013), http://dx.doi.org/10.1016/j.neuroimage.2013.05.103