Howells et al. Behavioral and Brain Functions 2010, 6:39 http://www.behavioralandbrainfunctions.com/content/6/1/39 RESEARCH Open Access RPeeserarccheived mental effort correlates with changes in tonic arousal during attentional tasks FleurMHowells*1,2, DanJStein1 and VivienneARussell2 Abstract Background: It has been suggested that perceived mental effort reflects changes in arousal during tasks of attention. Such changes in arousal may be tonic or phasic, and may be mediated by the locus-coeruleus norepinephrine (LC-NE) system. We hypothesized that perceived mental effort during attentional tasks would correlate with tonic changes in cortical arousal, as assessed by relative electroencephalogram (EEG) band power and theta/beta ratio, and not with phasic changes in cortical arousal, assessed by P300 amplitude and latency. Methods: Forty-six healthy individuals completed tasks that engage the anterior and posterior attention networks (continuous performance task, go/no-go task, and cued target detection task). During completion of the three attentional tasks a continuous record of tonic and phasic arousal was taken. Cortical measures of arousal included frequency band power, theta/beta ratios over frontal and parietal cortices, and P300 amplitude and latency over parietal cortices. Peripheral measures of arousal included skin conductance responses, heart rate and heart rate variance. Participants reported their perceived mental effort during each of the three attentional tasks. Results: First, changes in arousal were seen from rest to completion of the three attentional tasks and between the attentional tasks. Changes seen between the attentional tasks being related to the task design and the attentional network activated. Second, perceived mental effort increased when demands of the task increased and correlated with left parietal beta band power during the three tasks of attention. Third, increased mental effort during the go/no-go task and the cued target detection task was inversely related to theta/beta ratios. Conclusion: These results indicate that perceived mental effort reflects tonic rather than phasic changes in arousal during tasks of attention. We suggest that perceived mental effort may reflect in part tonic activity of the LC-NE system in healthy individuals. Background activation) for successful completion of the task [2,3]. Arousal can be defined as a change in physiological and/ Therefore poor performance during a task may relate to or psychological responsiveness to internal or external inappropriate tonic levels of arousal and/or phasic pro- stimuli. Early studies attributed changes in peripheral cesses. measures of sympathetic nervous system activity, such as William James [5] defined attention as the "taking pos- skin conductance [1], to task-related changes in arousal session by the mind in clear and vivid form, of one out of [2,3]. According to the Yerkes and Dodson [4] theory, what seem several simultaneously possible objects or however, an individual who is underaroused or hyper- trains of thought". Posner and Petersen [6] proposed two aroused will perform a task poorly. This suggests that attentional networks that rely on interactions with tonic levels of arousal need to be maintained within an arousal systems. (1) The anterior attentional network has optimal range in order to achieve successful completion been suggested to involve the detection of sensory targets of a task. In addition, the individual would then recruit and is strongly reliant on the anterior cingulate cortex. (2) the necessary phasic neural processes (also referred to as The posterior attentional network has been suggested to involve sensory attention orienting and is reliant on the * Correspondence: [email protected] functioning of the posterior parietal cortex, superior col- 1 Department of Psychiatry and Mental Health, Faculty of Health Sciences, liculi and thalamic pulvinar nuclei [6]. Attention required University of Cape Town, Observatory, 7925, South Africa Full list of author information is available at the end of the article for successful completion of a task requires an optimal © 2010 Howells et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Howells et al. Behavioral and Brain Functions 2010, 6:39 Page 2 of 15 http://www.behavioralandbrainfunctions.com/content/6/1/39 level of arousal, which in turn requires activation of par- not clear. As an improved 'signal-to-noise ratio' may serve ticular attentional network. to reflect the tonic changes in LC-NE system activity, so This work leads to the question of whether an individ- changes in information processing and cortical updating ual would be able to report changes in arousal during per- may serve to reflect the phasic changes in LC-NE system formance of a cognitive task that required attention. activity. At the same time it is not possible to disengage Pribram and McGuinness [2] postulated that effort used the tonic and phasic activities of the LC-NE system. during a voluntary mental process (such as attention) is The aims of the present study were to determine: (1) related to the energy required to produce repeated whether changes in physiological levels of arousal changes in the "representational organization of informa- increased during the completion of three voluntary atten- tion processing". Studies have shown that difficulty, com- tional tasks and what aspects of the tasks were associated plexity and stress-inducing tasks lead to increased with these changes, (2) whether perceived mental effort subjective perceptions of mental effort which have in turn reflected these changes in arousal during tasks of atten- been related to increased physiological arousal as mea- tion and what aspects of these tasks were associated with sured by increased skin conductance responses, heart these changes and (3) whether perceived mental effort rate, and heart rate variance [7-14]. Thus subjective per- reflected tonic or phasic changes in arousal as observed ception of mental effort may reflect changes in arousal in physiological recordings during the three tasks of during performance of attentional tasks. attention. Arousal systems of the central nervous system arise To address the aims of the present study several physio- from several nuclei in the reticular activating system of logical parameters were recorded during three voluntary the brain stem [15]. These systems are classified accord- attentional tasks. These parameters have previously been ing to their pathways and their specific neurotransmitters related to increased arousal and mental effort, and which include: (1) the locus coeruleus noradrenergic sys- included: relative theta, alpha, and beta band power of tem (LC-NE), (2) the magnocellular basal forebrain/ frontal and parietal electrodes, amplitude and latency of pedunculopontine cholinergic system, (3) the midbrain parietal P300s, number and duration of skin conductance substantia nigra/ventral tegmental area dopaminergic responses (SCRs), heart rate, and heart rate variance. Par- system, (4) the dorsal raphe serotonergic system, and (5) ticipants were asked to report their perceived mental the tuberomamillary hypothalamic histaminergic system effort during each of the three attentional tasks. In addi- [16]. tion salivary cortisol measures were taken before and The LC-NE system has been strongly related to arousal after the testing session to address the possible confounds and attentional regulation [17-21]. Activation of the LC of stress-related hypothalamic pituitary adrenal axis acti- has been shown to increase cortical arousal (as measured vation. by electroencephalographic (EEG) recordings) and We hypothesized that perceived mental effort during improve the 'signal' (information that needs to be attentional tasks would correlate with tonic changes in attended to) by decreasing the 'noise' (background non- cortical arousal, as assessed by beta band power and relevant information) which has been related to tonic theta/beta ratio in the EEG, and not with phasic changes activity of the LC-NE neurons [22-24]. In addition the in cortical arousal, assessed by P300 amplitude and LC-NE system responds phasically to salient stimuli. This latency. If perceived mental effort is related to tonic activity of the LC-NE system has been suggested to play changes in arousal then this may reflect tonic activities of an important role in the P300 component of an event- the LC-NE arousal system. related potential (ERP) [25]. The P300 is a positive deflec- tion of a stimulus-locked epoch in an EEG trace, such as Methods is seen in an array of cognitive tasks [26]. The occurrence Participants of the P300 has been suggested to reflect cortical updat- Forty-six healthy participants (28 females, 27.6 ± 5.3 ing [27], as is suggested by the 'orienting response' pro- years old) recruited from the postgraduate community of posed by Sokolov [28,29]. This work indicates that the University of Cape Town, South Africa, took part in individuals create a cortical representation of trials within the present study. Participation in the present study held a task. As the task endures and the individual completes no incentive and was voluntary. The study was approved more trials, the cortical representations of the trials are by the Health Science Faculty Human Ethics Committee updated [28,29]. The extent of cortical updating has been of the University of Cape Town, and the participants shown to depend on the individual's level of arousal [30- signed informed consent. The study was conducted in 32] and the value placed on the information being pro- accordance with the Declaration of Helsinki [34]. Partici- cessed [33]. The role of tonic and phasic firing of the LC- pants reported no psychiatric, psychological, substance NE system in the regulation of arousal during attention is use or dependence disorder, and did not have a current Howells et al. Behavioral and Brain Functions 2010, 6:39 Page 3 of 15 http://www.behavioralandbrainfunctions.com/content/6/1/39 general medical condition or history of brain trauma. In Vs. The 3rd condition of the go/no-go task was a go condi- addition participants had matriculated, with English as a tion with a longer inter-stimulus interval of 3 500 msec first language. unlike the inter-stimulus interval of 1 500 msec used in the 1st and 2nd condition. The 1st and 2nd conditions com- Experimental design prised 40 stimuli. In the 2nd condition 20 of 40 stimuli Participants were required to refrain from caffeine, ciga- were Vs which required response inhibition (50% target, rettes, alcohol, and non-prescription drugs for 18 hrs 50% non-target split). The 3rd condition comprised 20 before testing. Testing of participants occurred between stimuli. These three conditions were then repeated in 09h30 and 13h30. Saliva for the cortisol assay was col- reverse order forming a mirror image of the first three lected immediately before physiological recordings and conditions. immediately after (±1 hour apart). Physiological record- ings were collected by a MP150 Biopac acquisition sys- Cued target detection task tem (Biopac Systems Inc.) with amplifier modules set for The cued target detection task used in the present study EEG (electrodes of interest F3, F4, P3, P4), skin conduc- was an endogenous form of Posner's exogenous covert tance responses, and electrocardiogram. The testing ses- orienting task [35]. The cued target detection task sion comprised of five stages: (1) resting eyes open (2 required participants to maintain fixation on a central min) and three attentional tasks: (2) a continuous perfor- cue, a solid white circle in the centre of the computer mance task, (3) a go/no-go task, and (4) a cued target screen. On either side of the central fixation cue was an detection task. All of the above were programmed using outline of a rectangle that was grey in colour. The central E-prime 1.1. The physiological data and digital output fixation point and the grey rectangle outlines were pres- from E-prime were collected on-line by Acqknowledge ent throughout the cognitive task. The participant was 3.8.1 software (Biopac Systems Incorporated). At least 10 required to respond to the presentation of a square within min was permitted to ensure reliable signal conductance. either of the rectangles. For this task there were four con- The testing session was completed in a quiet unlit room ditions: (1) congruent cue and stimulus presentation; (2) to reduce distractors from the tasks at hand. The partici- incongruent cue and stimulus presentation; (3) double pants were tested only once and were naïve to the testing cue and stimulus presentation; and (4) no cue and stimu- session. Thereafter the participants completed a visual lus presentation. Cues were presented for 500 msec and analogue scale that expressed their perceived level of the stimulus was presented for 500 msec. The inter-stim- mental effort during performance of each of the atten- ulus interval was variable throughout the task, with dura- tional tasks. All data analyses were performed post-hoc to tions of 500, 1000, or 1500 msec. The cued target data acquisition. detection task had 64 stimuli that were congruent; 16 stimuli that were incongruent; 16 stimuli that had double Continuous performance task repeated letter version cueing; and 16 stimuli that had no cues. We only report The continuous performance task involved three consec- event-related potential data from the congruent stimuli in utive presentations of the letter 'S', the third 'S' was the the present paper. target stimulus. Sixty-four trials were presented. The stimuli were present for 500 msec, with an interval of 100 EEG relative band power analysis and P300 extraction msec. Non-target stimuli were presented for 500 msec in EEG data were collected with the use of EEG100C ampli- the centre of the computer screen with an interval of 100 fier modules which were attached to the MP150 acquisi- msec. The non-target stimuli were letters of the alphabet tion system (Biopac Systems Inc.), electrodes of interest which were not vowels. were F , F , P , and P . Linked ear lobe reference was 3 4 3 4 used. The EEG100C amplifier gain was set at 1000, mode Go/no-go task normal, low pass filter set at 100 Hz, and high pass filter The go/no-go task required sustained attention in addi- on at 0.1 Hz (application note 233, Biopac Systems Incor- tion to response inhibition and delayed response to stim- porated). The CAL1 input value was set at 10 with scale ulus presentation. The visual go/no-go task used in the value set at 10 and the CAL2 input value was set at -10 present study required the participant to respond to all with a scale value of -10. The sampling frequency of the consonants with the exception of the letter 'V'. No vowels software (Acqknowledge 3.8.1) was set at 500 Hz with were used. The 1st condition of the go/no-go task was a go units of recording set at μV. The EEG data was passed condition, in which all stimuli required responses by the through a Hamming window, FIR band pass filter, low participant as no Vs' were presented. The 2nd condition of frequency at 0.05 Hz and high frequency at 30 Hz, num- the go/no-go task was a no-go condition, in which partic- ber of coefficients was set at 4000, using Acqknowledge ipants needed to respond to the consonants that were 3.8.1. The filtered EEG data for the different stages of the non-Vs and inhibit their response on presentation of the testing session were Fourier transformed extracting theta Howells et al. Behavioral and Brain Functions 2010, 6:39 Page 4 of 15 http://www.behavioralandbrainfunctions.com/content/6/1/39 (θ, 4-7 Hz), alpha (α, 7-14 Hz), and beta (β, 15-30 Hz) fre- was set at 4000, using Acqknowledge 3.8.1. Tachograms quency bands. The extracted absolute power was con- for the different stages of the testing session were verted into relative band power (%). obtained through a specialized software application, Event-related potentials (ERPs) were extracted with using Acqknowledge 3.9. The data then underwent a fully Acqknowledge software (greater than +100 μV and less automated heart rate variance analysis (Biomedical Signal than -100 μV) as per digital inputs from E-prime for each Analysis Software, Department of Applied Physics, Uni- of the three attentional tasks. The ERPs were baseline versity of Kuopio, Finland). Default parameters set in the corrected for 100 msec before stimulus presentation and software for autoregressive analysis were applied to the visually inspected. The window for the P300 component tachograms: low frequency 0.04 to 0.15 Hz and high fre- for the continuous performance task was 200-500 msec quency 0.15 to 0.4 Hz components. The autoregressive after the stimulus, for the go/no-go task (go and no-go model order was set at 20. Heart rate, relative low fre- stimuli) it was 250 - 500 msec, and for the cued target quency, relative high frequency, and the low to high fre- detection task (congruent trials only) it was 400-700 quency ratio were obtained from the data. msec. The P300 amplitude was the point at which the Salivary cortisol assay height of the P300 was maximal. P300 latency was the time at which the P300 amplitude was maximal. Salivettes® (Sarstedt non-citric acid sterile cotton wool rolls) were used to collect saliva for the cortisol assay. Skin conductance responses Samples were stored at -80°C. Salimetrics LLC expanded Skin conductance responses were measured with the range high sensitivity salivary cortisol enzyme immuno- GSR100C amplifier module which was attached to the assay kits were used to determine cortisol concentrations. MP150 acquisition system (Biopac Systems Inc.). The The assay procedure was carried out as recommended by GSR100C module was set to measure phasic activity the insert of the assay kits, Salimetrics Catalog No. 1- (AC), with the gain set at 10 μS/V, the low pass filter was 3002/1-3012, 96-Well Kit (lower detection limit 0.003 μg/ set at 10 Hz and the high pass filter was set at 0.05 Hz, dL else 0.083 nmol/L). All samples were analyzed in with a sampling frequency of 500 Hz. Scaling parameters duplicate and the pH of all samples was within the range on the software CAL1 input were set at 0. The CAL2 of accuracy for the enzyme immune-assay. Optical den- input value was set at 1 with a scale factor set at 10. Units sity was measured at 450 nm. Values were converted in of skin conductance were recorded in μS. A TSD203 skin the manner suggested in Salimetrics Catalog No. 1-3002/ conductance transducer was attached to the GSR100C 1-3012, 96-Well Kit using standards supplied with the kit. amplifier module. The skin conductance data was passed through a Hamming window, FIR low pass filter of 1 Hz, Visual analogue scale of perceived mental effort and the number of coefficients was set at 2000, using The participants' perceived mental effort was assessed by Acqknowledge 3.8.1. The data were then analyzed for means of a visual analogue scale [37]. On a single A4 peaks exceeding a threshold value of 0.05 μS, the number landscape sheet there were three 10 cm vertical lines, one of responses and their durations were extracted during for each of the attentional tasks. At the top of the vertical each stage of the testing session and do not coincide with line 'very high mental effort' was typed and at the bottom measures of task responses (see [36]). of the vertical line 'very little mental effort' was typed. Participants were asked to mark on each of the three ver- Heat rate and heart rate variance tical lines the amount of perceived mental effort they felt Electrocardiograph data were collected with the use of that they had used for each of the attentional tasks. The three ECG100C amplifier modules which were attached score (%) was the distance (cm) from the bottom of the to the MP150 acquisition system (Biopac Systems Inc.). vertical line. The three ECG100C modules were connected to a TSD155C multi-lead ECG cable with built-in Wilson ter- Statistical analysis minal (five leads). The ECG100C amplifier module's gain The Statistica 8 software package was used for the statis- was set at 1000, mode normal, low pass filter set at 35 Hz, tical analyses. Non-parametric statistics were used to and high pass filter set at 0.5 Hz. The CAL1 input value analyze all data since the Shapiro-Wilks W test revealed was set at 10 with scale value set at 10. The CAL2 input that the data were not normally distributed. Wilcoxon value was set at -10 with scale value set at -10. The sam- matched pairs test was performed when comparing two pling frequency of the software (Acqknowledge 3.8.1) was dependent variables. Friedman ANOVA was performed set at 500 Hz with units of recording set at μvolts. The for comparison of several dependent variables. Spear- electrocardiogram data was passed through a Hamming man's Rank R was used to determine correlations window, FIR band pass filter, low frequency at 0.05 Hz between variables. Figures report mean ± SEM. Bonfer- and high frequency at 35 Hz, the number of coefficients roni correction was applied to all data exceeding two Howells et al. Behavioral and Brain Functions 2010, 6:39 Page 5 of 15 http://www.behavioralandbrainfunctions.com/content/6/1/39 comparisons (4 comparisons p < 0.0125, 3 comparisons p higher during the go/no-go task than the cued target < 0.01667). detection task. Wilcoxon matched pairs test for the right frontal electrode (F4) revealed that the theta/beta ratio Results was higher during the go/no-go task than the cued target Relative EEG band power and theta/beta ratio for each detection task (Figure 2). stage of the testing session Parietal P300 latency and amplitude for the three Friedman ANOVAs revealed differences in stages of the attentional tasks testing session (rest, continuous performance task, go/ Friedman ANOVAs revealed differences in the three no-go task, and cued target detection task) for relative attentional tasks for P300 latency and amplitude for left alpha and beta power for frontal electrodes (F3 relative α Chi Sqr = 17.09, p < 0.001, F3 relative β Chi Sqr = and right parietal electrodes and during the no-go condi- (3,46) (3,46) tion of the go/no-go task (P3 P300 latency Chi Sqr = 26.17, p < 0.0001 and F4 relative α Chi Sqr = 10.61, p (3,46) (3,46) 111.4, p < 0.0001, P4 P300 latency Chi Sqr = 114.5, p = 0.014, F4 relative β Chi Sqr = 19.48, p < 0.0002). Dif- (3,46) (3,46) < 0.0001, P3 P300 amplitude Chi Sqr = 66.15, p < ferences between the stages of the testing session were (3,46) also revealed for relative theta and beta power for left 0.0001 and P4 P300 amplitude Chi Sqr(3,46) = 66.15, p < parietal electrode (P3) and relative theta and alpha power 0.005). Wilcoxon matched pairs tests revealed the follow- for right parietal electrode (P4) (Figure 1). Wilcoxon ing: left parietal (P3) electrode P300 latency during the matched pairs tests revealed the following differences. continuous performance task was shorter than the go/no- Left frontal electrode (F3) relative alpha band power was go task and cued target detection task. The grand mean higher during the resting eyes open phase and the go/no- event-related potentials (ERPs) for parietal electrodes, P3 go tasks than during the continuous performance task and P4, are shown in (Figure 3). The P300 latency during and the cued target detection task. Left frontal electrode the go condition of the go/no-go task was shorter than (F3) relative beta band power during the cued target during the no-go condition and both were shorter than detection task was higher than during resting eyes open, P300 latency during the cued target detection task (Fig- the continuous performance task, and the go/no-go task ure 4a). Right parietal (P4) electrode P300 latency for the (Figure 1a). Right frontal electrode (F4) relative alpha continuous performance task was shorter than the go/no- band power was higher during the resting eyes open go task and the cued target detection task. The go/no-go phase compared to continuous performance task and the go condition had shorter latency than the go/no-go no-go cued target detection task. Relative alpha band power was condition and the cued target detection task while the go/ higher during the go/no-go task than during the cued tar- no-go no-go condition had shorter P300 latency than the get detection task. Right frontal electrode (F4) relative cued target detection task (Figure 4b). Left parietal (P3) beta band power was higher during the cued target detec- electrode P300 amplitude for the continuous perfor- tion task than during the continuous performance task mance task and the go/no-go go condition was lower than and the go/no-go task (Figure 1b). Left parietal electrode the go/no-go no-go condition and higher than the cued (P3) relative theta band power was lower during resting target detection task. The go/no-go no-go condition had eyes open than during the continuous performance task higher P300 amplitude than the cued target detection and the cued target detection task. Left parietal electrode task (Figure 4c). Right parietal (P4) electrode P300 ampli- (P3) relative beta band power was lower during the go/ tude for the continuous performance task and the go/no- no-go task than during resting eyes open, the continuous go go condition was lower than the go/no-go no-go con- performance task, and the cued target detection task dition and higher than the cued target detection task. The (Figure 1c). Right parietal electrode (P4) relative theta go/no-go no-go condition had higher P300 amplitude band power was lower during resting eyes open than dur- than the cued target detection task (Figure 4d). ing the continuous performance task and the cued target Response times for each of the three attentional tasks and detection task. Right parietal electrode (P4) relative alpha their conditions band power during resting eyes open and the go/no-go Friedman's ANOVA revealed significant differences in task were higher than during the cued target detection response times between tasks (Chi Sqr = 44.74, p < task (Figure 1d). (2,46) 0.0001). The Wilcoxon matched pairs test revealed Friedman ANOVA revealed differences between the shorter response times for the continuous performance three attentional tasks at frontal electrodes (F3 & F4) for task (386 ± 85 msec) compared to the go/no-go task (418 relative theta/beta ratios (F3 θ/β ratio Chi Sqr = (3,46) ± 21 msec) and cued target detection task (473 ± 49 12.55, p < 0.01) and F4 θ/β ratio Chi Sqr = 8.23, p < (3,46) msec). In addition response times for the go/no-go task 0.05). Wilcoxon matched pairs test for left frontal elec- were shorter than the cued target detection task. During trode (F3) revealed that the relative theta/beta ratio was the go/no-go task, response inhibition errors were Howells et al. Behavioral and Brain Functions 2010, 6:39 Page 6 of 15 http://www.behavioralandbrainfunctions.com/content/6/1/39 Figure 1 Relative EEG band power during stages of the testing session. Relative EEG band power during various stages of the testing session: resting eyes open (REO), continuous performance task (CPT), go/no-go task (GNG), and cued target detection task (CTD). Relative band power report- ed: theta (θ, 4-7 Hz), alpha (α, 7-14 Hz), and beta (β, 15-30 Hz) for frontal (F3 & F4) and parietal (P3 & P4) electrodes. a) *Left frontal (F3) α band power was higher during REO and GNG than CPT and CTD. @β band power was higher during CTD than REO, CPT, and GNG. b) *Right frontal (F4) α band power was higher during REO than CPT and CTD. #α band power was higher during GNG than CTD. @β band power was higher during CTD than CPT and GNG. c) *Left parietal (P3) θ band power was lower during REO than CPT and CTD. #β band power was lower during GNG than REO, CPT, and CTD. d) *Right parietal (P4) θ band power was lower during REO than CPT and CTD. #α band power was higher during REO and GNG than during CTD (p < 0.0125, n = 46, mean ± SEM). recorded, with an average of 2.3 ± 0.25 errors made dur- eyes open than during the three attentional tasks. Fewer ing the task. skin conductance responses were made during the continuous performance task than during the go/no-go Skin conductance responses and durations task and the cued target detection task. A greater number Friedman ANOVA revealed differences in the number of of skin conductance responses were made during the go/ skin conductance responses (Chi Sqr = 92.93, p < (3,46) no-go task than during the cued target detection task 0.0001) and duration of response (Chi Sqr = 24.67, p (Figure 5a). (3,46) < 0.0001) during the different stages of the testing session Wilcoxon matched pairs test revealed that the duration (Figure 5). of skin conductance responses was shorter during resting Wilcoxon matched pairs test revealed that the number eyes open than during the three attentional tasks. Addi- of skin conductance responses was fewer during resting tionally the skin conductance responses were shorter Howells et al. Behavioral and Brain Functions 2010, 6:39 Page 7 of 15 http://www.behavioralandbrainfunctions.com/content/6/1/39 cued target detection task. Spearman rank order correla- tion showed strong relationships between perceived mental effort reported during each of the three atten- tional tasks (Figure 7b). Physiological correlates of perceived mental effort during the three attentional tasks Spearman's rank order correlation analysis was per- formed to determine relationships between perceived mental effort and physiological measures recorded dur- ing completion of the attentional tasks (Table. 1). Perceived mental effort correlated positively with left parietal beta (P3) band power during the three tasks of Figure 2 Relative theta/beta (θ/β) ratio for frontal (F3 & F4) and parietal (P3 & P4) electrodes for the stages of the testing session. attention. Right parietal beta band power during the go/ Relative theta/beta (θ/β) ratio for frontal (F3 & F4) and parietal (P3 & P4) no-go task also increased with increased perceived men- electrodes for the various stages of the testing session: resting eyes tal effort. Perceived mental effort correlated negatively open (REO), continuous performance task (CPT), go/no-go task (GNG), with relative theta/beta ratios during the go/no-go task, and cued target detection task (CTD). *θ/β ratio for F3 and F4 was for left frontal (F3) and parietal (P3 & P4) electrodes, dur- greater during GNG than during CTD (p < 0.0125, n = 46, mean ± SEM). ing the cued target detection task a similar correlation was found for the left frontal (F3) and left parietal (P3) during the continuous performance task compared to electrodes. Perceived mental effort correlated positively the go/no-go task and the cued target detection task with relative theta during the go/no-go task and cued tar- (Figure 5b). get detection task, for left frontal (F3) electrode, in addi- tion during the cued target detection task a similar Electrocardiogram heart rate and heart rate variance for correlation was found for the right frontal (F4) electrode. each stage of the testing session Perceived mental effort during the go/no-go task corre- Friedman ANOVA revealed differences in heart rate dur- lated negatively with heart rate variance high frequency ing the different stages of the testing session (Chi Sqr (3,46) band and positively with the heart rate variance low fre- = 49.89, p < 0.0001) and differences in high frequency quency band and high frequency band ratio. heart rate variance (Chi Sqr = 9.77, p < 0.05; Figure 6). (3,46) No relationships between perceived mental effort dur- Wilcoxon matched pairs test revealed heart rate was ing the three attentional tasks were found for response lower during resting eyes opened compared to all other times, errors of inhibition, skin conductance measures, or stages of the testing session. In addition, heart rate was for P300 latency and amplitude (Table. 1). higher during the go/no-go task than during the cued tar- get detection task (Figure 6a). Wilcoxon matched pairs Discussion test revealed high frequency heart rate variance was The main findings were as follows: First, changes in higher during resting eyes open than during the go/no-go arousal were seen from rest to completion of the three task (Figure 6b). No differences were found in low fre- attentional tasks and between the attentional tasks. quency heart rate variance parameters (Figure 6c) or the Changes seen between the attentional tasks being related low frequency/high frequency ratio (Figure 6d). to the task design and the attentional network activated. Second, perceived mental effort increased when demands Salivary cortisol before and after the testing session of the task increased and correlated with left parietal beta The Wilcoxon matched pairs test revealed no significant band power during the three tasks of attention. Third, difference between salivary cortisol levels before (0.16 ± increased mental effort during the go/no-go task and the 0.1 μg/dL) and after testing (0.17 ± 0.13 μg/dL). In addi- cued target detection task was inversely related to theta/ tion no significant effects were found for gender, or use of beta ratios. contraceptive pill. First, several changes in arousal were seen from rest to Perceived mental effort during the three attentional tasks completion of the three attentional tasks. Cortical relative Friedman ANOVA revealed differences in perceived alpha band power was higher during rest and during the mental effort during performance of the three attentional go/no-go task than during the continuous performance tasks (Chi Sqr = 30.83, p < 0.0001) (Figure 7a). Wil- task and cued target detection task. The continuous per- (2,46) coxon matched pairs test revealed that greater mental formance task and cued target detection task required the effort was required when completing the go/no-go task individual to keep information in mind (cues) preceding than during the continuous performance task and the the presentation of the target stimulus. Decreased alpha Howells et al. Behavioral and Brain Functions 2010, 6:39 Page 8 of 15 http://www.behavioralandbrainfunctions.com/content/6/1/39 Figure 3 Grand mean event-related potentials (ERPs) for parietal electrodes (P3 and P4) during the three attentional tasks. Grand mean event-related potentials (ERPs) for parietal electrodes (P3 and P4) during the three attentional tasks: continuous performance task (CPT), go/no-go task (go and no-go conditions; GNG), and cued target detection task (CTD). band power is thought to be a measure of increased power decreases with increased mental load [11,39] and attentional performance [38], and so may be related to increases with anticipatory waiting during attentional cues being presented in the continuous performance task tasks [40] or during increased focused attention and/or and cued target detection task. Given that alpha band increased arousal [41,42], the present findings suggest Howells et al. Behavioral and Brain Functions 2010, 6:39 Page 9 of 15 http://www.behavioralandbrainfunctions.com/content/6/1/39 Figure 4 Latency and amplitude of the event-related potentials (ERPs) of parietal electrodes (P3 & P4) during the three attentional tasks. Latency and amplitude of the event-related potentials (ERPs) of parietal electrodes (P3 & P4) during the three attentional tasks: continuous perfor- mance task (CPT), go/no-go task (go and no-go conditions; GNG), and cued target detection task (CTD). a) For left parietal P300 latency the *CPT was shorter than GNG and CTD, #GNG go condition P300 latency was shorter than GNG no-go condition and CTD @GNG no-go condition P300 latency was shorter than CTD b) For right parietal P300 latency the *CPT was shorter than GNG and CTD, #GNG go condition P300 latency was shorter than GNG no-go condition and CTD. @GNG no-go condition P300 latency was shorter than CTD. c) For left parietal P300 amplitude the *CPT and GNG go con- dition were smaller than GNG no-go condition and greater than CTD. The #GNG no-go condition P300 amplitude was greater than CTD. d) The right parietal P300 amplitude *CPT and GNG go condition was smaller than GNG no-go condition and was greater than CTD. The #GNG no-go condition P300 amplitude was greater than CTD. that during the continuous performance task and the the go/no-go task which required increased activation of cued target detection task there was increased mental the anterior attentional network. In addition covert load due to cueing systems of the tasks. While the endogenous shifting of attention that is necessary during increased alpha band power during the go/no-go task the cued target detection has been correlated with frontal may reflect the lack of cueing and anticipation of the eye field 18-34 Hz oscillations [45], consistent with the other two tasks. present findings. Relative beta band power during the cued target detec- During the go/no-go task theta/beta ratios were higher tion task was higher over frontal cortical electrodes than over the frontal areas than during the continuous perfor- during the continuous performance task and go/no-go mance task and cued target detection task. This finding is task. Increased beta band power over the frontal cortex of interest as individuals with ADHD are known for their has been associated with deficits in sustained attentional poor attentional performance, which is accentuated in performance [43,44]. However this increase may simply tasks that require response inhibition such as the go/no- suggest that during the cued target detection task there go task. It has been suggested that individuals with was disengagement of the anterior attentional network, ADHD are incapable of increasing their arousal levels and given that the reflexive cued target detection task would this is reflected in high theta/beta ratios [46]. The present require increased activation of the posterior attentional study suggests that healthy individuals increased their network [6,19]. This hypothesis is supported by the fact theta/beta ratio when increased arousal was required, that frontal beta band power was further reduced during during the go/no-go task. This finding supports Barry Howells et al. Behavioral and Brain Functions 2010, 6:39 Page 10 of 15 http://www.behavioralandbrainfunctions.com/content/6/1/39 Figure 5 Skin conductance responses and their duration during stages of the testing session. a) Skin conductance responses recorded during resting eyes open (REO), continuous performance task (CPT), go/no-go task (GNG), and cued target detection task (CTD). *The number of skin con- ductance responses during REO were fewer than at all other stages. #CPT responses were fewer than responses made during the GNG and greater than responses made during the CTD. @GNG responses were greater than during the CTD. b) Duration of skin conductance responses. *The duration of responses during REO was shorter than at all other stages. #CPT duration of response was shorter than the duration of responses during the GNG and CTD (p < 0.0125, n = 46, mean ± SEM). and colleagues' suggestion that the theta/beta ratio is not latency and amplitude of the P300. (1) Habituation to task a good physiological measure of the suggested hypo- and repetition of task, as shown in an oddball task that arousal seen in individuals with ADHD [47,48]. In addi- led to decrements in P300 amplitude sequentially for tion activation of working memory during the continuous each of the ten times the task was repeated [50]. (2) Task performance task and the cued target detection task due difficulty as shown in a series of mathematical tasks that to cueing stimuli may account for increased theta band gradually increased their level of difficultly, the P300 power relative to beta band power over the frontal cortex amplitudes formed a U-shaped trend from 'extremely [49]. easy' to 'extremely difficult' [51]. P300 amplitudes and latencies were extracted from The present findings support these studies. To com- parietal electrode sites as these have been suggested to be plete the continuous performance task the individual was maximal over the parietal cortices during attentional required to respond to the presentation of a third consec- tasks [30] and may serve to reflect in part the phasic utive 'S', the reduced latency and reduced amplitude may activities of the LC-NE system [25]. Bilaterally P300 relate to the reduced cortical updating required as the latencies were shorter for the continuous performance individual was primed by the first and the second 'S'. To task when compared to the go/no-go task (go and no-go complete the cued target detection task the individual conditions) and the cued target detection task. In addi- received a cue in their peripheral visual field and tion left parietal P300 amplitudes were lower during the responded to the target stimulus that was also in their continuous performance task compared to the go/no-go peripheral visual field. The increased latency and reduced (go and no-go conditions) task and the cued target detec- amplitude may reflect the exogenous orienting required tion task. It has been suggested that the P300 is a repre- that then effected the cortical updating of the peripheral sentation of the neural processing required for cortical images. To complete the go/no-go task the individual updating [27]. The 'orienting response' suggests that an received no cueing system, the increased latency and individual creates a cortical representation of trials within increased amplitude relative to the continuous perfor- a task, as the task endures and the individual completes mance task may reflect an increase in cortical updating more trials, the cortical representations of the trials are due to the 'no-cueing' design of the task. In addition dur- continuously updated [28,29]. The extent of this cortical ing the no-go trials the P300 amplitude and latency were updating or 'orienting response' is dependent on the indi- greater than during the go trials of the go/no-go task. The vidual's state of arousal and may be affected by changes of no-go trials required individuals to inhibit their response tonic arousal levels and phasic arousal activity [30-32]. In that would require increased cortical updating to prevent addition several factors have been shown to affect the error responses.