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Heart rate variability and cognitive processing: the autonomic response to task 1"
demands. 2"
Antonio Luque-Casado1,2,3, José C. Perales1,2, David Cárdenas3 & Daniel Sanabria1,2 3"
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1. Brain, Mind, & Behaviour Research Center. University of Granada, Spain 5"
2. Department of Experimental Psychology. University of Granada, Spain 6"
3. Department of Physical Education and Sport. University of Granada, Spain 7"
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Submitted to: Biological Psychology 11"
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Corresponding author: Daniel Sanabria 13"
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E-mail address: daniel@ugr.es 15"
Phone: +34 958247875 16"
Fax: +34 958246239 17"
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Abstract 1"
This study investigated variations in heart rate variability (HRV) as a function of 2"
cognitive demands. Participants completed an execution condition including the 3"
psychomotor vigilance task, a working memory task and a duration discrimination task. 4"
The control condition consisted of oddball versions (participants had to detect the rare 5"
event) of the tasks from the execution condition, designed to control for the effect of the 6"
task parameters (stimulus duration and stimulus rate) on HRV. The NASA-TLX 7"
questionnaire was used as a subjective measure of cognitive workload across tasks and 8"
conditions. Three major findings emerged from this study. First, HRV varied as a 9"
function of task demands (with the lowest values in the working memory task). Second, 10"
and crucially, we found similar HRV values when comparing each of the tasks with its 11"
oddball control equivalent, and a significant decrement in HRV as a function of time-12"
on-task. Finally, the NASA-TLX results showed larger cognitive workload in the 13"
execution condition than in the oddball control condition, and scores variations as a 14"
function of task. Taken together, our results suggests that HRV is highly sensitive to 15"
overall demands of sustained attention over and above the influence of other cognitive 16"
processes suggested by previous literature. In addition, our study highlights a potential 17"
dissociation between objective and subjective measures of mental workload, with 18"
important implications in applied settings. 19"
Key words: Sustained attention, psychomotor vigilance task, perception, working 20"
memory, executive processing, NASA-TLX, mental workload. 21"
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Introduction 1"
A large body of research has shown a direct link between cognitive processing 2"
and the cardiovascular system through autonomic vagal control (Thayer & Lane, 2009). 3"
A simple way of measuring that relationship is to look at heart rate variability (HRV), a 4"
non-invasive measurement of the interactions between the autonomic nervous system 5"
and the cardiovascular system, based on the study of oscillations of the interval between 6"
heartbeats (Malik et al., 1996; Pumprla, Howorka, Groves, Chester, & Nolan, 2002). 7"
Thayer et al. have recently proposed the Neurovisceral Integration Model to 8"
account for the link between cognitive processing and the functioning of the 9"
autonomous nervous system (Thayer, Hansen, Saus-Rose, & Johnsen, 2009; Thayer & 10"
Lane, 2009). They pointed out that HRV is a particularly sensitive index of the changes 11"
in a flexible neural network that is dynamically organized in response to situational 12"
requirements. The authors highlighted the role of the prefrontal cortex in the modulation 13"
of subcortical cardio-acceleratory circuits via an inhibitory pathway that is associated 14"
with vagal function and that can be indexed by HRV. The link of the frontal cortex to 15"
autonomic motor circuits responsible for both the sympathoexcitatory and 16"
parasympathoinhibitory effects on the heart seems to be controlled both by direct and 17"
indirect pathways. In this sense, one of the potential mediators underlying variations in 18"
HRV as a function of cognitive demands is the baroreceptor system, i.e., the negative 19"
feedback loop adjusting heart activity to blood pressure fluctuations. In fact, the 20"
baroreflex function appears to be influenced by specific behavioural manipulations of 21"
cognitive demands and mental workload (e.g., Duschek, Werner, & Reyes del Paso, 22"
2013; Reyes del Paso, González, & Hernández, 2004). Consequently, variations in the 23"
baroreflex function may therefore also mediate modulations in HRV during the specific 24"
task conditions. In any case, HRV is thought of as an overall index of central-peripheral 25"
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neural feedback and central nervous system-autonomic nervous system integration 1"
(Thayer & Lane, 2000, 2009). 2"
A cursory look to the literature on the relationship between HRV cognition 3"
shows that researchers have used a wide range of tasks, tapping different cognitive 4"
processes, which make it difficult to establish a finer-grained relationship between HRV 5"
and cognitive processing. In more specific terms, a number of studies have singled out a 6"
subset of mental workload components -executive demands- as key to understand the 7"
HRV-cognitive processing link, with lower HRV as executive demands increase (Backs 8"
& Seljos, 1994; Duschek, Muckenthaler, Werner, & del Paso, 2009; Hansen, Johnsen, 9"
& Thayer, 2003; Luft, Takase, & Darby, 2009; Mathewson et al., 2010; Mulder & 10"
Mulder, 1981). In this scenario, the above mentioned Neurovisceral Integration Model 11"
predicts an inverse relationship between executive task demands and levels of HRV, 12"
which seems to be confirmed by the studies cited above. However, the results of other 13"
studies appear to challenge this straightforward view of the relationship between HRV 14"
and cognitive processing. For instance, Fairclough & Houston (2004) failed to show 15"
differences between the congruent and incongruent conditions when participants had to 16"
name the colour of the ink in a Stroop task, a well-known executive task (e.g., Egner & 17"
Hirsch, 2005). On the contrary, they showed that HRV was sensitive to time-on-task, 18"
pointing to the role of overall attention demands on HRV. In this same line, Chang & 19"
Huang (2012) showed that HRV varied as a function of attentional demands in a visual 20"
search task, with lower HRV in a conjunction search task than in a feature search task 21"
and a control condition in which participants passively watched to the stimuli. 22"
Together with attention demands, perceptual difficulty seems to be another key 23"
factor modulating HRV. The results of two recent studies point in that direction. Chen, 24"
Tsai, Biltz, Stoffregen, and Wade (2015) reported lower HRV as a function of 25"
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perceptual difficulty, but not as a function of working memory load (linked to executive 1"
functioning; e.g., Duncan & Owen, 2000). Particularly relevant here is the study by 2"
Luque-Casado et al. (Luque-Casado, Zabala, Morales, Mateo-March, & Sanabria, 3"
2013), who compared HRV during performance of three tasks, tapping three different 4"
cognitive functions: the psychomotor vigilance task (PVT; a vigilance task), an 5"
endogenous temporal orienting task (a cognitive control task), and a duration 6"
discrimination task (a perceptual task). The results showed lower levels of HRV in the 7"
perceptual task than in the other two tasks, with no significant differences in the main 8"
indexes of HRV between the PVT and the temporal orienting task. In addition, they 9"
showed that HRV decreased with time-on-task, a result that did not seem to depend on 10"
the particular task running at that moment. 11"
Overall, the outcome of the above-mentioned studies seem to nuance Thayer et 12"
al.’s Neurovisceral Integration Model, and point to some aspects of cognitive demand 13"
(i.e. perceptual difficulty and sustained attention) and not others (working memory i.e. 14"
workload, interference) as key task features modulating HRV. However, as Luque-15"
Casado et al. acknowledged in their article, brain structures typically associated with 16"
executive processing seem to be also involved in difficult perceptual discrimination 17"
(Duncan & Owen, 2000). Thus, the question remains of whether a task purposely 18"
developed to involve high executive demands would induce a larger reduction in HRV 19"
than the perceptual task used by Luque-Casado et al. (2013). 20"
The present study is aimed at further investigating the role of particular 21"
processing demands involved in task effects on HRV. We partially replicated Luque-22"
Casado et al.’s (2013) manipulation, using the PVT and the duration discrimination 23"
task, but replaced the temporal orienting task by a N-back task. The N-back task tackles 24"
working memory capacity, a core component of executive functioning, by asking 25"
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participant to tag and update short-term stored information on a trial-by-trial basis 1"
(Kirchner, 1958; Owen, McMillan, Laird, & Bullmore, 2005). Importantly, along with 2"
these three tasks, we included three parallel oddball tasks, with the same stimuli 3"
parameters for each of the three, but in which participants just had to detect a rare event 4"
within a sequence of frequent stimuli. 5"
The inclusion of the oddball condition allowed us to control for an important 6"
aspect that has been neglected in the majority of previous studies investigating the 7"
relationship between HRV and cognitive processing: the potential influence of stimulus 8"
parameters of the task on the relationship between autonomic response and cognitive 9"
performance. That is, whether stimulus setting features (e.g., stimulus duration, inter-10"
stimulus interval) may explain (at least partially) the influence of task performance on 11"
autonomic reactivity over and above any specific cognitive process (e.g., executive 12"
processing, memory, etc.) specifically tapped by the task. In this sense, to the best of 13"
our knowledge, the only task feature that has been investigated in relation to this issue is 14"
the motor activity during the cognitive task (Bush, Alkon, Obradović, Stamperdahl, & 15"
Boyce, 2011; Stephen W. Porges et al., 2007). While Porges et al. showed that only 16"
gross motor activity (e.g., bike pedaling) could modulate the relationship between 17"
autonomic response and cognitive processing, Bush et al. found changes on autonomic 18"
reactivity to various cognitive tasks that were related to the particular motor activity 19"
during each procedure. Here, by asking participants to perform an oddball version of the 20"
three main cognitive tasks we controlled for variations in HRV due to the particular 21"
stimulus features of the tasks (e.g., stimulus duration) regardless of the task demands, 22"
whilst largely reducing the motor activity. 23"
Here, as a cross-task and cross-condition manipulation check, subjective mental 24"
load was assessed with the National Aeronautics and Space Administration Task Load 25"
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Index (NASA-TLX) questionnaire (Hart & Staveland, 1988). The NASA-TLX 1"
sensitivity to mental workload has been demonstrated to be useful in a variety of 2"
cognitively demanding tasks such as aircraft piloting (Karavidas et al., 2010; Ma et al., 3"
2014), air traffic control (Brookings, Wilson, & Swain, 1996), surgery (Zheng et al., 4"
2012), or laboratory tasks context (Muth, Moss, Rosopa, Salley, & Walker, 2012). With 5"
the inclusion of the NASA-TLX we aimed at comparing objective (HRV) and 6"
subjective potential indices of mental load induced by the different task demands. This 7"
is not trivial since previous research has questioned the validity of subjective measures 8"
of mental load (see Annett, 2002, for discussion on this issue). 9"
On the basis of Luque-Casado et al.'s (2013) findings and the previous related 10"
research, we expected the N-back task to exert a stronger modulation over HRV than 11"
the PVT. The question of interest was to see whether the N-back task would also 12"
influence HRV to a greater extent than the duration discrimination task, a result that 13"
would add further support to the Neurovisceral Integration Model. Importantly, given 14"
that the three tasks in the oddball condition were essentially the same task (with 15"
variations only in stimuli parameters) with minimal response requirements, we did not 16"
expect significant differences in HRV across them. We predicted the NASA scores to 17"
parallel the HRV results, with larger perceived workload in the N-back task than in the 18"
other two tasks, and no differences across the three oddball tasks. 19"
Methods and design 20"
Participants 21"
Twenty-four males undergraduate students (age range: 18-28 years old; M= 21 22"
years old; SD= 2.6 years old) from the University of Granada (Spain) took part in the 23"
study in exchange of course credits. In order to take part in the experiment, participants 24"
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were required to maintain a regular sleep–wake cycle for at least one day before the 1"
study and to abstain from stimulating beverages or any intense physical activity for the 2"
day of the experiment. Once in the laboratory, none of them reported having had any 3"
stimulating beverage or exercise session, and they all reported a regular sleep the night 4"
before (6-10 hours; M= 7.5; SD= 0.9). None of the participants smoked, and all of them 5"
reported normal hearing and normal or corrected-to-normal vision. 6"
The experiment was approved by the local ethics committee and complied with the 7"
ethical standards laid down in the 1964 Declaration of Helsinki. Participants read and 8"
signed an informed consent statement before the beginning of the experimental session. 9"
They were also informed about their right to leave the experiment at any time. All data 10"
were analyzed and reported anonymously. 11"
Apparatus and materials 12"
Participants were fitted with a Polar H3 heart rate sensor and a Polar RS800 CX 13"
monitor (Polar Electro Öy, Kempele, Finland) to record their HRV during the 14"
experimental session. We used a digital thermo-hygrometer Inovalley 207H01 15"
(Inovalley,Saint-Ouen-l'Aumône, France) to measure the temperature and humidity 16"
percentage in the laboratory during the experimental session. 17"
We used a PC Intel Quad Core i7-3770, a 24’’ LED monitor (BenQ XL2411T) and 18"
the E-Prime software (Psychology Software Tools, Pittsburgh, PA, USA) to control the 19"
stimulus presentation and response collection. The centre of the PC screen was situated 20"
at 60 cm (approx.) from the head of the participant and at his eye level. The PC 21"
keyboard was used to collect responses. !22"
Procedure 23"
9
The experimental protocol comprised two conditions (henceforth, execution and 1"
oddball). In the execution condition participants performed three different tasks: the 2"
PVT, a duration discrimination task and the N-back task. In the oddball condition, 3"
participants performed parallel ‘oddball’ versions of the three tasks mentioned above 4"
(see Experimental tasks section for more details). The order of presentation of the 5"
execution and oddball conditions, and the tasks within each condition, were 6"
counterbalanced across participants. Immediately after each task, participants completed 7"
the NASA-TLX questionnaire (Hart & Staveland, 1988; Hart, 2006) for them to assess 8"
the subjective workload perceived for each task. 9"
At the beginning of each experimental condition, all the participants had a 10"
familiarization period. They received verbal and written instructions and, after that, they 11"
practiced each task for one minute. They also received the necessary instructions to 12"
complete the NASA-TLX questionnaire at the beginning of the first experimental 13"
condition. 14"
The timestamp of the start and end of each task was taken for further analysis of 15"
HRV. During the experiment, the participant was seated in front of the computer in a 16"
dimly illuminated room and isolated from external noise. Comfortable temperature 17"
(21.3±0.8 ºC) and relative humidity (43.4±3.1 %) values were maintained throughout 18"
the experimental session. 19"
Experimental tasks 20"
a) Execution condition 21"
PVT: We used a modified version of the task created by Wilkinson & Houghton 22"
(1982). On each trial, the number 3 in white colour (2.67° x 1.62°) appeared on the 23"
centre of the screen in a black background. Later, in a random time interval (from 2000 24"
10
to 10000 ms), this number changed its orientation from vertical to horizontal (1.62º x 1"
2.67º). The participants were instructed to respond with their dominant hand as fast as 2"
they could when the change in orientation occurred. Feedback of the response time was 3"
displayed on the screen on each trial during 300 ms. The next trial began after 1800 ms. 4"
Response anticipations were considered as errors. Participants were allowed 1500 ms to 5"
respond. If a response was not made during this time, the message "You did not answer" 6"
appeared on the screen. The task comprised a single block of 12 minutes and the total 7"
number of trials was 111±3.4 on average. 8"
Duration discrimination task: The duration discrimination task was a 9"
psychophysical task in which participants had to make temporal judgments regarding 10"
which of two visual stimuli were presented for a longer period of time (Paul et al., 11"
2011). The task started with the presentation of a fixation point at the centre of the 12"
screen for a random duration between 500-1000 ms. The fixation point was the “+” 13"
symbol (0.38° x 0.38°) that remained on and steady for the whole trial. Then, two 14"
consecutive visual stimuli were presented (the sample and the comparison stimuli) with 15"
a random time interval of 500-1000 ms between them. The sample stimulus was a white 16"
number 3 and the comparison stimulus a red number 3 (2.67° x 1.62°, both stimuli). The 17"
duration of the sample stimuli was 350 ms. Duration of the comparison stimulus was 18"
manipulated using the method of constant stimuli, lasting for either 160, 260, 300, 340, 19"
380, 420, 460 or 560 ms. Participants had 3000 ms to respond before the start of the 20"
next trial. Once the participant responded, a random inter-trial time of 500-1000 ms of 21"
duration was presented. 22"
Participants were instructed to discriminate whether the duration of the comparison 23"
stimulus was shorter or longer than the duration of the sample stimulus. If the duration 24"
of the comparison stimulus was longer than the duration of the sample stimulus, the 25"
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participant should respond by pressing the up arrow. Otherwise, the participants should 1"
press the down arrow. The comparison stimuli of varying duration were randomly 2"
intermixed across trials. Each of the comparison stimuli was presented, on average, a 3"
12.5% of the total number of trials in the task. There was not feedback after each trial. 4"
The overall duration of the task was 12 minutes and the total number of trials was, on 5"
average, 177±9.3. In this case, accuracy was stressed over response speed. 6"
N-back task: One of four digits (1, 2, 3 or 4; 2.67° x 1.53°; 2.67° x 1.62°; 2.67° x 7"
1.62° and 2.67° x 1.81°, respectively) was presented for 500 ms, followed by a fixed 8"
delay of 2500 ms. Participants had to respond, at any time during the presentation of the 9"
stimulus or the delay period, whether the current stimulus displayed on the screen was 10"
the same as the stimulus presented two trials before. If the stimulus on the screen 11"
matched the stimulus presented two trials before, the participant had to press the letter 12"
“S” key on the PC Keyboard. Otherwise, the participants had to press the letter “N” key. 13"
A new stimulus was presented every 3000 ms (i.e., 500 ms of stimulus presentation and 14"
2500 ms of fixed delay). The digit appearing on each trial was randomly selected, which 15"
means that, on average, the current digit was the same as the one presented two trials 16"
earlier in 25% of the trials. There was not feedback after each trial. The overall duration 17"
of the task was 12 minutes and the total number of trials was 217±1.6 on average. 18"
Accuracy was stressed over response speed. 19"
b) Oddball condition: 20"
In this condition, instructions were essentially the same for the three tasks: to detect 21"
the presence of an infrequent stimulus presented amongst a series of frequent stimuli. 22"
Crucially, there were three versions of the oddball task, corresponding to each of the 23"
task procedures described for the execution condition. Hence, each oddball version 24"
shared all task parameters (i.e., the rate of stimulus appearance, physical characteristics 25"
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of the stimuli and duration of each interval) with its corresponding “execution” task, 1"
with the sole difference being the tasks demands. In effect, participants were instructed 2"
to respond only when the oddball stimuli (i.e., the stimulus in a green colour) appeared 3"
on the screen (5% of the trials) in all three versions of the oddball task. The oddball 4"
stimuli could be displayed instead of the number 3 in landscape orientation in the 5"
oddball version of the PVT, instead of the comparison stimuli in the oddball version of 6"
the duration discrimination task and instead of any of the numbers in the oddball 7"
version of the N-back task. The oddball stimuli were randomly intermixed across trials. 8"
Response anticipations or no response to oddball stimuli were considered as errors. 9"
Feedback was provided only after incorrect answers. In these cases, the word 10"
"incorrect" in a red color was displayed on the screen during 300 ms. The overall 11"
duration of each task was 12 minutes and the total number of trials, on average, was 12"
94±2.5 for the oddball version of the PVT, 112±1.1 for the oddball version of the 13"
duration discrimination task and 216±0 for the oddball version of the N-back task. 14"
Accuracy was stressed over response speed in all cases. 15"
HRV measures 16"
The elastic electrode transmitter belt (Polar H3 heart rate sensor) was placed on the 17"
chest of the participant at the level of the lower third of the sternum (just below the 18"
chest muscles) with conductive gel being applied as described by the manufacturer. This 19"
transmitter belt contains two electrodes to detect the voltage differential on the skin 20"
during every heart beat and sends the signal continuously and wirelessly using an 21"
electromagnetic field to the Polar RS800 CX receiver unit. The data were collected with 22"
a sampling rate of 1000 Hz, providing a temporal resolution of 1ms for each RR 23"
interval. This Polar equipment has been shown to be a valid and highly reliable way to 24"
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measure short-term HRV at rest (Nunan et al., 2009; Radespiel-Tröger, Rauh, Mahlke, 1"
Gottschalk, & Mück-Weymann, 2003). 2"
All data sets were transferred to a password-protected PC under ASCII format via 3"
Polar-specific software (Polar® ProTrainer 5 software version 5.35.161). Subsequently, 4"
each RR interval file was analysed by means of the Kubios HRV Analysis Software 2.0 5"
(Tarvainen, Niskanen, Lipponen, Ranta-aho, & Karjalainen, 2009; The Biomedical 6"
Signal and Medical Imaging Analysis Group, Department of Applied Physics, 7"
University of Kuopio, Finland). 8"
The recordings were preprocessed to exclude artifacts by eliminating RR intervals 9"
which differed more than 25% from the previous and the subsequent RR intervals 10"
(Malik, Cripps, Farrell, & Camm, 1989). Removed RR intervals were replaced by 11"
conventional spline interpolation so that the length of the data did not change (i.e., 12"
resulting in the same number of beats). We used the smoothness prior method with a 13"
Lambda value of 500 to remove disturbing low frequency baseline trend components 14"
(Tarvainen, Ranta-aho, & Karjalainen, 2002). 15"
NASA-TLX questionnaire 16"
The NASA-TLX provides an overall workload score (from 0 to 100 points) 17"
based on a weighted average of ratings on six dimensions: Mental Demands, Physical 18"
Demands, Temporal Demands, Own Performance, Effort, and Frustration. 19"
Participants were instructed to rate each dimension on a visual analog scale 20"
(from 0 to 100 points). After that, participants were presented with 15 paired 21"
comparisons of each dimension and asked to choose which of them had a greater impact 22"
on their performance. A specific weight to each dimension from 0 to 5 was applied from 23"
these comparisons. The rating of each dimension was then multiplied by its respective 24"
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weight and the total score (the sum of the scores of each dimension) was divided by 15 1"
(the total number of paired comparisons) to obtain the final workload score. 2"
Design and data reduction 3"
Behavioural: 4"
We performed descriptive analysis on the behavioural data with the sole purpose 5"
of checking the proper performance during the experimental session. With this aim, we 6"
obtained the overall mean reaction times (RTs), the Just noticeable difference (JND) 7"
and the overall accuracy percentage, for the PVT, duration discrimination task and N-8"
back task, respectively. For oddball tasks, the percentage of accuracy of response to 9"
oddball stimuli was calculated. Only the experimental blocks were included in the 10"
analysis in all tasks. 11"
For the PVT trials, with RTs below 100 ms (0.9%) and anticipations (i.e., 12"
responses prior to the target presentation; 1.7%) were discarded from the analysis 13"
(Basner & Dinges, 2011). JNDs were calculated for each participant by subtracting the 14"
stimulus onset asynchrony (SOA) at which the best fitting line crossed the 0.75 point 15"
from the SOA at which the same line crossed the 0.25 point and dividing by two. Thus 16"
JND = SOA (75%) − SOA (25%)/2 and SOA(75%) = (z-score(75%) − b/m) and 17"
SOA(25%) = (z-score(25%) − b/m) with b = intercept and m = slope. The result of the 18"
equation is JND = .675/m (Coren, Ward, & Enns, 1999). 19"
HRV and NASA-TLX: 20"
The analysis of the HRV focused on both the time and frequency domains. The 21"
root-mean-square difference of successive normal R-R intervals (rMSSD) and the 22"
proportion of NN50 (i.e., the number of pairs of successive NNs that differ by more 23"
15
than 50 ms) were used as indexes of vagal control within the time domain (Allen, 1"
Chambers, & Towers, 2007). The High Frequency (HF; 0.15 to 0.40 Hz) was used as 2"
the index of vagal tone in the frequency domain (Berntson et al., 1997; Reyes del Paso, 3"
Langewitz, Mulder, van Roon, & Duschek, 2013). The denotations and definitions for 4"
the HRV parameters in this paper follow the guidelines given in Task force of the 5"
European society of cardiology and the North American society of pacing and 6"
electrophysiology (Malik et al., 1996). 7"
In order to investigate the time course of HRV during task performance, 3 intervals 8"
of 4’ each were considered for the analysis of the HRV. The ln-transformed HRV data 9"
were analyzed through repeated measures analysis of variance (ANOVA) with the 10"
within-participants factors of condition (execution and oddball), task (PVT, duration 11"
discrimination task and N-back task) and time-on-task (1, 2, 3). The NASA-TLX data 12"
were analysed through repeated measures ANOVA with the within-participants factors 13"
of condition (execution and oddball) and task (PVT, duration discrimination task and N-14"
back task). The effect sizes were reported by partial eta-squared (ηpartial2). Sphericity 15"
was tested by means of the Mauchley Sphericity test and the Green-House Geisser 16"
correction was applied when violation of this assumption occurred (corrected values are 17"
reported). 18"
Results 19"
Behavioural results: 20"
The descriptive analyses conducted on behavioural data showed a normal and 21"
typical execution for all tasks. On the one hand, the overall mean RT for the PVT was 22"
210.27 ± 26.89 ms, the JND for the duration discrimination task was 77.19 ± 10.90 ms 23"
and the overall accuracy percentage for the N-back task was 91.27 ± 6.07. On the other 24"
16
hand, the percentage of accuracy of response to oddball stimuli was 98.61± 6.80 and 1"
98.44 ± 7.65 for the version oddball of the PVT and N-back task, respectively. The 2"
percentage of accuracy for the oddball version of the duration discrimination task could 3"
not be calculated due to faulty response recording. However, there was no problem in 4"
carrying out the task by the participants. 5"
HRV:!6"
The ANOVAs showed that the main effect of condition (execution vs oddball) was 7"
not significant for any of the parameters, all Fs<1 (see Table 1). On the contrary, the 8"
main effect of task reached statistical significance in all indexes, rMSSD, 9"
F(2,46)=10.52, p<.001, ηpartial2=.31 (see Figure1), pNN50, F(2,46)=5.98, p<.01, 10"
ηpartial2=.20, HF, F(2,46)=9.21, p<.001, ηpartial2=28. All indexes showed the lowest 11"
values in the N-back task, all ps≤.01. The difference between the PVT and the duration 12"
discrimination task did not reach statistical significance in any of the parameters (all 13"
ps>.05). HRV values in the duration discrimination task and the NBack tasks were 14"
significantly different for the rMSSD, p<.01, and HF, p<.01, but not for pNN50, 15"
p=.053. The main effect of time-on-task was significant for rMSSD, F(2,46)=6.51, 16"
p<.01, ηpartial2= .22 (see Figure 2), and HF, F(2,46)=6.12, p<.01, ηpartial2=.21, and did 17"
not reach statistical significant for pNN50, F(2,46)=2.42, p=.10. There were differences 18"
between block 1 and block 2 (rMSSD, p<.001, and HF, p<.001) and between block 1 19"
and block 3 (rMSSD, p=.01 and HF, p=.04). The difference between block 2 and block 20"
3 was not significant for any of the indexes, all ps>.42. 21"
Crucially, the interaction between task and condition did not reach statistical 22"
significance for any of the parameters, F(2,46)=2.71, p=.08, F(2,46)=1.66, p=.20, F<1, 23"
for rMSSD, pNN50 and HF, respectively. The interactions between task and time-on-24"
17
task, and between task, time-on-task and condition were not significant for any of the 1"
HRV indexes [all Fs<1, except for Task x Time-on-task for HF, F(2,46)=1.63, p=.18]. 2"
Table 1. Mean (± standard deviation) for the HRV parameters as a function of 3"
condition, task and time-on-task. 4"
HRV parameters
Task
rMSSD (ms)
pNN50 (%)
HF (ms2)
Block1
Block2
Block3
Block1
Block2
Block3
Block1
Block2
Block3
Execution condition
PVT
82.4
(28.3)
76.9
(27.1)
79.2
(29.7)
46.2
(15.2)
43.9
(16.6)
43.0
(17.6)
2218.9
(1380.3)
1913.8
(967.0)
2130.6
(1536.8)
DDT
79.6
(32.2)
73.3
(31.0)
70.7
(27.0)
43.5
(18.7)
39.7
(18.1)
39.4
(15.4)
2762.4
(2651.3)
2135.8
(1646.0)
2062.9
(1568.9)
NBT
69.4
(29.0)
66.5
(26.3)
67.1
(23.2)
38.8
(18.5)
36.7
(17.5)
37.2
(17.0)
1965.1
(1661.1)
1626.2
(1170.4)
1749.0
(1221.5)
Oddball condition
PVT
77.2
(26.4)
73.1
(24.3)
74.0
(24.5)
41.7
(15.3)
40.4
(15.7)
41.1
(14.2)
2175.8
(1497.6)
1893.2
(1305.1)
1935.1
(1102.5)
DDT
78.1
(33.1)
76.2
(33.5)
73.2
(28.9)
41.0
(16.1)
40.7
(16.7)
38.5
(15.3)
2565.9
(2558.3)
2387.4
(2093.2)
2086.6
(1843.2)
NBT
73.1
69.2
72.5
40.0
38.6
39.5
2034.9
1797.7
1900.5
18
(27.9)
(25.7)
(27.3)
(16.6)
(14.7)
(15.6)
(1635.2)
(1678.2)
(1645.1)
PVT: psychomotor vigilance task; DDT: duration discrimination task; NBT: n-back 1"
task; O-PVT; O-DDT and O-NBT: the oddball version of each task respectively. 2"
Figure 1. HRV (rMSSD index) as a function of the task. The root-mean-square 3"
difference of successive normal R-R intervals (rMSSD) in miliseconds (ms) for each of 4"
the cognitive tasks (PVT = psychomotor vigilance task; DDT= duration discrimination 5"
task; NBT= n-back task). Bars represent standard errors of the mean. 6"
7"
Figure 2. HRV (rMSSD index) as a function of the time-on-task. The root-mean-8"
square difference of successive normal R-R intervals (rMSSD) in miliseconds (ms) for 9"
each of the blocks of the three cognitive tasks (Block1= between 0 and 4 minutes of 10"
each task; Block 2= between 4 and 8 minutes of each task; Block3= between 8 and 12 11"
minutes of each task). Bars represent standard errors of the mean. 12"
19
1"
NASA-TLX scores: 2"
The repeated-measures ANOVA with the within-participants factors of condition 3"
(execution and oddball) and task (PVT, duration discrimination task and N-back task) 4"
revealed a significant main effect of condition, F(1,23)=76.36, p<.01, ηpartial2=.77, with 5"
greater scores in the execution condition than in the oddball condition (see Table 2). 6"
The main effect of task was also significant, F(2,46)=9.91, p<.01, ηpartial2=.30. 7"
Importantly, these main effects were better qualified by the significant interaction 8"
between condition and task, F(2,46)=6.29, p<.01, ηpartial2=.21 (see Figure 3). In the 9"
execution condition, there were significant differences between the PVT and N-back 10"
task, p<.01, between the PVT and duration discrimination task, p=.04, and between the 11"
N-back and the duration discrimination task, p=.03. In all cases, the PVT and N-back 12"
task elicited the lowest and the highest scores respectively. Instead, comparisons 13"
between tasks for the oddball condition did not reveal significant differences (all 14"
ps>.21). 15"
16"
Figure 3. NASA-TLX scores as a function of task for the execution and oddball 17"
condition. Mean of the NASA-TLX overall scores for the execution and oddball 18"
20
condition in each of the cognitive tasks (PVT = psychomotor vigilance task; DDT= 1"
duration discrimination task; NBT= n-back task). Bars represent standard errors of the 2"
mean. 3"
4"
5"
Table 2. Mean (± standard deviation) for the NASA-TLX overall scores as a function of 6"
condition and task. 7"
NASA-TLX overall scores
Execution Condition
PVT
DDT
NBT
51.0 (23.8)
60.5 (16.0)
68.1 (14.4)
Oddball Condition
O-PVT
O-DDT
O-NBT
28.2 (18.6)
31.0 (21.8)
29.6 (20.3)
21
PVT: psychomotor vigilance task; DDT: duration discrimination task; NBT: n-back 1"
task; O-PVT; O-DDT and O-NBT: the oddball version of each task respectively. 2"
Discussion 3"
HRV is sensitive to cognitive processing with significant variations as a function 4"
of changes in task demands. Previous accounts have pointed to executive demands of 5"
the task at the key parameter to explain those variations in HRV in the variety of tasks 6"
that have been tested in the laboratory (Thayer & Lane, 2009). On the contrary, other 7"
recent studies suggest that rather than broadly ranging executive demand, other, more 8"
molecular factors such as perceptual difficulty influence HRV. Here, we investigated 9"
this issue by comparing HRV values during performance of a vigilance task, a working 10"
memory task, and a duration discrimination task. Crucially, we also added a condition 11"
to control for the effect of the particular stimulus parameters of each task, minimizing 12"
the motor activity by using an oddball procedure. The NASA-TLX was used as a 13"
subjective measure of cognitive workload. 14"
HRV indeed varied as a function of task demands, with lower values in the N-15"
Back task than in the other two tasks, and no differences between the PVT and the 16"
duration discrimination task. At this point, these results would confirm the hypothesis 17"
stated by Luque-Casado et al. (2013) in their conclusions, whereby a task with greater 18"
executive demands than the temporal orienting task used in their study would induce 19"
lower HRV than the perceptual task. 20"
However, the oddball control condition revealed intriguing results. The 21"
interaction between condition and task was not significant, apparently meaning that the 22"
reliable task effect was not (only) due to the particular demands of the tasks, since 23"
participants performed exactly the same task in the three version of the oddball 24"
22
procedure. It would however suggest that the particular stimulus features of the N-Back 1"
task, in comparison to the PVT and the duration discrimination task, were responsible 2"
for HRV decrements. The three tasks (in both the execution and oddball control 3"
conditions) were only differentiated in terms of stimuli duration, interval between 4"
stimuli, and, above all, presentation rate. The N-Back task, both in the execution and the 5"
oddball procedure, had twice the number of trials (in 12’) as compared to the duration 6"
discrimination task and even more compared to the PVT, while the difference in the 7"
number of trials was much less between the PVT and the duration discrimination task 8"
(with no significant differences in HRV either). This larger number of trials in the N-9"
Back task resulted in a larger number of motor responses, even in the oddball task. 10"
However, based on the scarce previous research (Bush et al., 2011; Porges et al., 2007) 11"
and given that the number of targets was very low in the oddball condition, one would 12"
argue that the motor demands of the task cannot explain the reliable task effect shown 13"
here. Note that if motor activity were responsible of the changes in HRV, significant 14"
differences would have emerged between the execution condition and the oddball 15"
condition for every task. On the contrary, it is more plausible that the higher 16"
presentation rate resulted, both in the execution and oddball conditions, in a significant 17"
increase in the demands of sustained attention (Lanzetta, Dember, Warm, & Berch, 18"
1987; Parasuraman & Giambra, 1991; Sarter, Givens, & Bruno, 2001) with respect to 19"
the other two tasks, which in turn resulted in lower HRV. Crucially, two results from 20"
our study appear to support the hypothesis of the HRV sensitivity to sustained attention 21"
demands: the non-significant main effect of condition and the significant main effect of 22"
time-on-task. 23"
The non-significant main effect of condition was driven by similar HRV values 24"
when comparing each of the tasks in the execution condition with their oddball 25"
23
equivalent. An oddball task like the one used here requires participants to maintain a 1"
high level of vigilance in order to detect the infrequent targets (Eason & Dudley, 1970; 2"
Fruhstorfer & Bergström, 1969) and it has been used as a paradigm to assess sustained 3"
attention (Czisch et al., 2012; Weber, Van Der Molen, & Molenaar, 1994). In addition, 4"
the robust time-on-task effect shown in our experiment is consistent with previous 5"
accounts suggesting the sensitivity of HRV to vigilance decrements or mental fatigue 6"
(e.g., Middleton, Sharma, Agouzoul, Sahakian, & Robbins, 1999; Porges & Raskin, 7"
1969). For example, Luque-Casado et al. (2013), using a similar procedure to that of our 8"
execution condition, showed a gradual decrement in participants’ HRV as a function of 9"
the time on task. Fairclough & Houston (2004) also showed that the 0.1 Hz component 10"
of HRV was sensitive to time on task although it did not seem sensitive to a 11"
manipulation of workload within the same task. Additionally, Chua et al. (2012) have 12"
recently shown that HRV provides information about a person’s vigilance state, and that 13"
this measure could potentially be used to predict when an individual is at increased risk 14"
of attentional failure. 15"
Taken together, our results therefore point to sustained attention demands of the 16"
tasks in general and of the NBack task in particular, as the major factor influencing 17"
HRV in our study, over and above any other of task-related cognitive components (e.g., 18"
working memory, cognitive control, perceptual processing) or task parameters. 19"
Sustained attention has been considered one of the executive functions linked to 20"
the prefrontal cortex (Alvarez & Emory, 2006; Stuss, Shallice, Alexander, & Picton, 21"
1995). In that sense, our results do not plainly contradict, but nuance the Neurovisceral 22"
Integration Model. Moreover, it would explain the outcome of previous research that 23"
failed to show differences between experimental conditions varying in terms of 24"
cognitive control demands (e.g., Fairclough & Houston, 2004; Hansen et al., 2003; 25"
24
Luque-Casado et al., 2013), and those reports showing that overall attentional load is 1"
crucial in order to explain HRV variations (e.g., Chang & Huang, 2012)."Importantly, 2"
on the basis of our results, it would be interesting for future research to incorporate 3"
experimental designs including specific manipulations of the sustained attention load"4"
(e.g., by manipulating the likelihood of the target appearance) for a more thorough 5"
investigation of the specific effect of the sustained attention demands on HRV."In fact, 6"
this could be considered as a potential limitation of our study since the level of 7"
sustained attention load was not systematically manipulated in addition to task-related 8"
cognitive components or task parameters. 9"
The results of the NASA-TLX replicated previous studies (e.g., Karavidas et al., 10"
2010; Ma et al., 2014; Muth et al., 2012), showing larger cognitive workload in the 11"
execution condition than in the oddball condition, and scores variations as a function of 12"
task, with larger values for the N-Back task, followed by the duration discrimination 13"
task and the PVT. Interestingly enough, NASA scores appear clearly differentiated from 14"
HRV measures, suggesting a dissociation between objective and subjective cognitive 15"
workload, and contributing to the discussion regarding the validity of subjective 16"
measures of cognitive workload (Annett, 2002). The present results show that two 17"
conditions that contribute differently to subjective load (which would suggest that one 18"
of them is much less loading, and, supposedly, less interfering or potentially dangerous 19"
than the other one), can actually be equally loading in psychophysiological terms. In 20"
other words, some aspects of mental workload can remain hidden to subjective insight. 21"
In sum, the outcome of the present study suggests that HRV is highly sensitive 22"
to sustained attention over and above the influence of other cognitive processes, a 23"
finding that needs to be considered by any research looking at the link between 24"
autonomic control and cognitive processing. In addition, our study highlights a potential 25"
25
dissociation between objective and subjective measures of mental workload, which has 1"
important implications in applied settings. 2"
3"
26
Acknowledgments 1"
This research was supported by a predoctoral grant FPU-AP2010-3630 2"
(Ministerio de Educación, Cultura y Deporte, Spain) to Antonio Luque-Casado, a 3"
research grant DEP21013-48211-R (Ministerio de Economía y Competitividad, Spain) 4"
to David Cárdenas, and research grants SEJ-6414 (Proyecto de Excelencia, Junta de 5"
Andalucía, Spain) and PSI2013-46385-P (Ministerio de Economía y Competitividad, 6"
Spain) to Daniel Sanabria. We thank Guillermo Sánchez-Delgado for his assistance 7"
during the data collection. 8"
9"
27
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