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Deficits in cue detection underlie event-based prospective memory impairment in major depression: an eye tracking study Siyi Chen a,b,c , Renlai Zhou a,b,c,n , Hong Cui d , Xinyin Chen e a Beijing Key Lab of Applied Experimental Psychology, School of Psychology, Beijing Normal University, Beijing 100875, China b State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China c Research Center of Emotion Regulation, Beijing Normal University, Beijing 100875, China d Medical Psychology Division, General Hospital of People’s Liberation Army, Beijing 100853, China e Applied Psychology-Human Development Division, Graduate School of Education, University of Pennsylvania 3700, Walnut St., Philadelphia, USA article info Article history: Received 6 June 2012 Received in revised form 9 January 2013 Accepted 12 January 2013 Keywords: Event-based prospective memory Cue detection Major depressive disorder Eye tracking Behavioural measurement abstract This study examined the cue detection in the non-focal event-based prospective memory (PM) of individuals with and without a major depressive disorder using behavioural and eye tracking assessments. The participants were instructed to search on each trial for a different target stimulus that could be present or absent and to make prospective responses to the cue object. PM tasks included cue only and target plus cue, whereas ongoing tasks included target only and distracter only. The results showed that a) participants with depression performed more poorly than those without depression in PM; b) participants with depression showed more fixations and longer total and average fixation durations in both ongoing and PM conditions; c) participants with depression had lower scores on accuracy in target-plus-cue trials than in cue-only trials and had a higher gaze rate of targets on hits and misses in target-plus-cue trials than did those without depression. The results indicate that the state of depression may impair top-down cognitive control function, which in turn results in particular deficits in the engagement of monitoring for PM cues. & 2013 Published by Elsevier Ireland Ltd. 1. Introduction Depression is associated with mild-to-moderate impairment in several cognitive domains, including attention, memory and executive functioning (Beats et al., 1996; Elliott et al., 1996; Purcell et al., 1997; Veiel, 1997; Den Hartog et al., 2003; Hammar et al., 2003). Studies examining the impact of depression on memory functioning have focussed on retrospective memory (i.e., the ability to remember past events), whereas little is understood about the influence of depression on prospective memory (PM) (i.e., ‘remembering to remember’). PM refers to the formation, maintenance and execution of future intentions (Kvavilashvili and Ellis, 1996), involving the function of retro- spective memory, working memory and executive functions (Burgess and Shallice, 1997; Martin et al., 2003), but separable from these related constructs. There are two categories of PM: event-based (e.g., remembering to turn off the stove after cook- ing) and time-based (e.g., remembering to take medicine after 15 min) (Einstein and McDaniel, 1996). PM pervades our every- day lives, with an apparent clinical relevance. To our knowledge, the performance of patients with depres- sion on objective time-based and event-based PM tests has been assessed in three previous studies. Rude and his colleagues (1999) reported that major depression resulted in the impairment of tasks that required a high degree of controlled, self-initiated processing, such as time-based PM tasks. Lee et al. (2010) studied participants with bipolar disorder and discovered that increased age and disease severity contributed to deficits in time-based PM (Lee et al., 2010). The single evidence of impairment on measures of event-based PM provided by Altgassen et al. (2009) revealed that the non-depressed group outperformed the individuals with depression in the non-focal condition, but not in the focal condition. Focality describes the similarity of the cognitive pro- cesses needed for performing the ongoing task and detecting the prospective cue (McDaniel and Einstein, 2000). For example, if both the ongoing task and the prospective cues demand percep- tual processing, the cue is focal to the processes involved in the ongoing activity. However, if the ongoing task needs perceptual processing, but the prospective cues demand semantic proces- sing, the cue is non-focal to the ongoing processes. Relative to the focal condition that involves the same type of processing in retrieving the planned action on the task, a non-focal condition Contents lists available at ScienceDirect journal homepage: www.elsevier.com/locate/psychres Psychiatry Research 0165-1781/$ - see front matter & 2013 Published by Elsevier Ireland Ltd. http://dx.doi.org/10.1016/j.psychres.2013.01.015 n Corresponding author at: School of Psychology, Beijing Normal University, Beijing 100875, China. Tel.: þ86 10 58802021. E-mail address: [email protected] (R. Zhou). Psychiatry Research 209 (2013) 453–458

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Page 1: Deficits in cue detection underlie event-based prospective memory impairment in major depression: an eye tracking study

Psychiatry Research 209 (2013) 453–458

Contents lists available at ScienceDirect

Psychiatry Research

0165-17

http://d

n Corr

Beijing

E-m

journal homepage: www.elsevier.com/locate/psychres

Deficits in cue detection underlie event-based prospective memoryimpairment in major depression: an eye tracking study

Siyi Chen a,b,c, Renlai Zhou a,b,c,n, Hong Cui d, Xinyin Chen e

a Beijing Key Lab of Applied Experimental Psychology, School of Psychology, Beijing Normal University, Beijing 100875, Chinab State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, Chinac Research Center of Emotion Regulation, Beijing Normal University, Beijing 100875, Chinad Medical Psychology Division, General Hospital of People’s Liberation Army, Beijing 100853, Chinae Applied Psychology-Human Development Division, Graduate School of Education, University of Pennsylvania 3700, Walnut St., Philadelphia, USA

a r t i c l e i n f o

Article history:

Received 6 June 2012

Received in revised form

9 January 2013

Accepted 12 January 2013

Keywords:

Event-based prospective memory

Cue detection

Major depressive disorder

Eye tracking

Behavioural measurement

81/$ - see front matter & 2013 Published by

x.doi.org/10.1016/j.psychres.2013.01.015

esponding author at: School of Psychology

100875, China. Tel.: þ86 10 58802021.

ail address: [email protected] (R. Zhou).

a b s t r a c t

This study examined the cue detection in the non-focal event-based prospective memory (PM) of

individuals with and without a major depressive disorder using behavioural and eye tracking

assessments. The participants were instructed to search on each trial for a different target stimulus

that could be present or absent and to make prospective responses to the cue object. PM tasks included

cue only and target plus cue, whereas ongoing tasks included target only and distracter only.

The results showed that a) participants with depression performed more poorly than those without

depression in PM; b) participants with depression showed more fixations and longer total and average

fixation durations in both ongoing and PM conditions; c) participants with depression had lower scores

on accuracy in target-plus-cue trials than in cue-only trials and had a higher gaze rate of targets on hits

and misses in target-plus-cue trials than did those without depression. The results indicate that the

state of depression may impair top-down cognitive control function, which in turn results in particular

deficits in the engagement of monitoring for PM cues.

& 2013 Published by Elsevier Ireland Ltd.

1. Introduction

Depression is associated with mild-to-moderate impairmentin several cognitive domains, including attention, memory andexecutive functioning (Beats et al., 1996; Elliott et al., 1996;Purcell et al., 1997; Veiel, 1997; Den Hartog et al., 2003;Hammar et al., 2003). Studies examining the impact of depressionon memory functioning have focussed on retrospective memory(i.e., the ability to remember past events), whereas little isunderstood about the influence of depression on prospectivememory (PM) (i.e., ‘remembering to remember’). PM refers tothe formation, maintenance and execution of future intentions(Kvavilashvili and Ellis, 1996), involving the function of retro-spective memory, working memory and executive functions(Burgess and Shallice, 1997; Martin et al., 2003), but separablefrom these related constructs. There are two categories of PM:event-based (e.g., remembering to turn off the stove after cook-ing) and time-based (e.g., remembering to take medicine after

Elsevier Ireland Ltd.

, Beijing Normal University,

15 min) (Einstein and McDaniel, 1996). PM pervades our every-day lives, with an apparent clinical relevance.

To our knowledge, the performance of patients with depres-sion on objective time-based and event-based PM tests has beenassessed in three previous studies. Rude and his colleagues (1999)reported that major depression resulted in the impairment oftasks that required a high degree of controlled, self-initiatedprocessing, such as time-based PM tasks. Lee et al. (2010) studiedparticipants with bipolar disorder and discovered that increasedage and disease severity contributed to deficits in time-based PM(Lee et al., 2010). The single evidence of impairment on measuresof event-based PM provided by Altgassen et al. (2009) revealedthat the non-depressed group outperformed the individuals withdepression in the non-focal condition, but not in the focalcondition. Focality describes the similarity of the cognitive pro-cesses needed for performing the ongoing task and detecting theprospective cue (McDaniel and Einstein, 2000). For example, ifboth the ongoing task and the prospective cues demand percep-tual processing, the cue is focal to the processes involved in theongoing activity. However, if the ongoing task needs perceptualprocessing, but the prospective cues demand semantic proces-sing, the cue is non-focal to the ongoing processes. Relative to thefocal condition that involves the same type of processing inretrieving the planned action on the task, a non-focal condition

Page 2: Deficits in cue detection underlie event-based prospective memory impairment in major depression: an eye tracking study

S. Chen et al. / Psychiatry Research 209 (2013) 453–458454

that involves different types of processing demands more effortand resources to engage in strategic processes to detect the cue andretrieve the associated intention (McDaniel and Einstein, 2000).

Together, these findings suggest that depression may nega-tively impact time-based PM, but the deficit in event-based PM indepression needs more consideration. According to Altgassenet al. (2009), it is important to take into account the conditionsin which significant attentional capacity is (or is not) required tonotice the cue as relevant to an intention. Therefore, we con-ducted the present study focussing directly on the issue about cuedetection, and, more specifically, the links between depressionand event-based PM as well as the mechanisms that mightunderlie these links among major depressive disorder andmatched participants without depression in an eye tracking study.

In the laboratory-based measures of event-based PM tasks,cues are embedded in an ongoing activity and participants mustexecute dual-task processing, which requires detecting the cuewhile performing the ongoing task and shifting attention from theongoing to the PM task. For example, on a lexical decision task,participants are instructed to remember to perform a specificaction (e.g., ‘hit the Z key’) in response to the cue, such as theappearance of a special word (or items from the ‘animal’ category)on the computer screen. There is a dual-task trade-off betweenthe effort and the attention placed on the ongoing versusprospective tasks (Marsh and Hicks, 1998; Smith and Bayen,2004; Marsh et al., 2005). In the process, cue detection may bemediated by where the attention resources are focussed on at thetime in which a cue occurs in the environment (Marsh et al.,2003; West et al., 2005). If individuals cannot effectively dis-tribute attention resource respectively to perform the ongoingtask and monitor the cue, or if attention is withdrawn from theentire task set, the PM is likely to fail.

It is believed that neuropsychological malfunctions in depres-sion are based on pathological projections from the amygdala tothe anterior cingulate cortex (ACC) and the prefrontal cortex (PFC)(Elliott et al., 1997; Davidson et al., 2002), which are implicated inPM (Burgess et al., 2001). Since these areas of the brain are part ofwidely distributed networks of attention and executive function(Cabeza and Nyberg, 2000), the detected effects of depression onPM may be mediated by the top-down cognitive control function.Consistently, Ellis and Ashbrook’s (1988) resource allocationmodel indicates that a depressive mood leads to reduced overallcognitive capacity during the performance of cognitive tasks bydeflecting some amount of attentional resources to intrusive,task-irrelevant or depression-related thoughts (see also Ellis,1991; cf. Hartlage et al., 1993; Kliegel et al., 2005; Kliegel andJager, 2006).

To examine the cognitive control effect of depression on detectingthe cue, we used the non-focal condition in our experiment tosimulate the environment that demands the processes to strategicallymonitor the environment for the presence of the cue. We also used atarget-searching task as the ongoing task in which individualssearched for a different target stimulus (i.e., an image object), whichcould be present or absent, and made prospective responses toobjects from the specific category (i.e., fruit objects). We manipulatedthe interference to the cue by making the cue co-exist with the targetobject or appear without the target object. Thus, the stimuli included1) only targets, 2) only prospective cues, 3) target plus cues and 4)distracters (neither targets nor cues). The poorer performance ofparticipants with depression on target-plus-cue trials than cue-onlytrials compared with participants without depression would provideevidence suggesting that individuals with depression might havedeficits in shifting attention from ongoing trials to prospective trials.

We combined behavioural measures and eye tracking metho-dology to examine the attention processing of individuals withand without depression. Examining the visual processing of

prospective cues can determine the amount of attentionalresources that participants may devote to processing cue recogni-tion and to intention retrieval (West et al., 2007). PM processingof patients and the non-depressed group measured by eyetracking was compared on four indices: fixations, total fixationduration, average fixation duration and gaze rate. The number offixations was the total number of times a certain area was fixed,measuring whether stimuli fell on the fovea of the retina. Thetotal fixation duration was the total time of all fixations within agiven region, including both consecutive fixations within a region(gaze duration) and refixations on the region (fixations initiatedfrom outside the region). Total fixation duration provided anindex of the entire processing of stimuli on the fovea. The averagefixation duration was defined as the mean of all individualfixation durations on a particular area. Finally, the gaze rate wasthe ratio of gaze time divided by total time of stimuli presentation.

Concerning the profile and neural substrates of depression-associated cognitive deficits, we hypothesised that comparedwith their non-depressed counterparts individuals with depres-sion would require more attentional effort to complete the taskand engage in compensation processing, as indicated by greaternumbers of fixations and longer total and average fixation dura-tions. Moreover, the probability of gazing at the prospective cueor target on target-plus-cue trials would provide evidence indi-cating whether interference was inhibited and attention wascorrectly shifted from ongoing trials to prospective trials.

2. Methods

2.1. Participants

Participants with depression (N¼19; right-handed) were recruited from the

Medical Psychology Division of a General Hospital. All the participants with

depression were categorised according to Diagnostic and Statistical Manual of

Mental Disorders, fourth edition (DSM-IV; American Psychiatric Association, 1994;

First et al., 2002) criteria for unipolar major depression. No participant was taking

antidepressant medication at the time of participating in this study. They came to

seek treatment when they did not have any antidepressant medication. After

communicating with the doctor, they participated in this study, and then they

began the antidepressant medication. These participants were tested on 17-item

Hamilton Depression Rating Scale (Ham-D 17; Hamilton, 1967) and 21-item Beck

Depression Inventory-II (BDI-II; Beck et al., 1996) to ensure that they were over

the cut-off score on the severity of depression. All the participants scored at least

17 on Ham-D 17 and 20 on BDI-II. Participants in the non-depressed group

(N¼19; right-handed) were recruited from a university in the same city. Exclusion

criteria were based on clinical laboratory tests such as the mini-mental state

examination (MMSE; Folstein et al., 1975), comprehensive demographic and

clinical information including family history, psychiatric and medical history

and medication history. All participants scored 27 or higher on the MMSE.

Individuals were excluded from the groups if they had diagnoses of lifetime or

current bipolar I or II disorder, primary diagnosis of another Axis I or II disorder,

schizophrenia, delusional disorder and organic brain disorder. Other exclusion

criteria included substance abuse or dependence in the last 6 months, imminent

suicide risk, current use of medications and pregnancy. Written informed consent

was obtained from the participants before the study began.

2.2. Materials and equipment

The stimuli were 128 black-and-white line drawings of common objects, taken

from Snodgrass and Vanderwart (1980). Before the experiment, the participants

were asked to name the objects to avoid confusion during the experiment. The 128

objects were combined into 128 search displays, each containing four semantically

unrelated objects on a white background. These displays appeared after the target

word (black) presented at the centre of the screen. The display was divided into

four areas, equivalent to the four quadrants in which an object could occur. Each

object subtended approximately 21 of visual angle both horizontally and vertically

and there were approximately 4.51 of visual angle between the centres of any two

adjacent objects. The cues were the fruit objects (e.g., apple). The experiment

included 64 trials with targets (target-present) and 64 without (target-absent).

Within the 64 target-present trials, there were 60 target-only trials and 4 target-

plus-cue trials. For these trials, the target appeared 16 times and the cue appeared

one time at each of the four positions. Within the 64 target-absent trials, there

Page 3: Deficits in cue detection underlie event-based prospective memory impairment in major depression: an eye tracking study

Table 1Demographic and clinical characteristics of the sample (N¼38).

Non-

depressed

Depressed

N¼19 N¼19

Gender (N, %)

Female (N¼18) 9 (47.37) 9 (47.37)

Male (N¼20) 10 (52.63) 10 (52.63)

Age (years) (Mean7S.D.) 27.9574.58 28.2674.65

Education (years) (Mean7S.D.) 20.1672.71 16.8973.09

BDI-II score (Mean7S.D.) a 1.7971.13 38.7975.72

Ham-D score (Mean7S.D.) b N/A 20.6873.51

Total duration of major depression (years)

(Mean7S.D.)

N/A 5.0572.69

Number of previous episodes (Mean7S.D.) N/A 2.5371.35

a BDI-II¼Beck Depression Inventory, Second Edition.b Ham-D¼Hamilton Depression Rating Scale score.

S. Chen et al. / Psychiatry Research 209 (2013) 453–458 455

were 4 cue-only trials, with the cue appearing one time at each of the four

positions. The remaining 60 trials were the distracter-only trials, in which the four

objects were neither a target nor a cue. The cues were embedded in the ongoing

trials in a pseudorandom sequence, with the 12th, 44th, 76th and 108th trials

being target-plus-cue and the 28th, 60th, 92nd and 124th trials cue-only.

The participants’ eye movements were tracked with the SMI iView X-RED Eye

Tracking System at a sampling rate of 250 Hz. Responses were collected using a

digital response pad connected to a dedicated input–output (I/O) card. The stimuli

were displayed at a resolution of 1024�768 on a 17-inch cathode ray tube (CRT)

monitor. The refresh rate was 60 Hz. The eye tracker, display monitor and

response panel were interfaced with standard personal computers. The experi-

ment was conducted using E-Prime software (version 1.1). The subjects’ eyes were

positioned 85 cm from the CRT. Eye movements were monitored from the right

eye, but viewing was binocular. The experiment was conducted individually in a

private suite of a university laboratory. The room was dark except for the displays

and a dim indirect light source.

2.3. Procedure

Before the task began, the participants were instructed that they would be

doing a visual search task and that we were interested in whether they could

realize a delayed intention. At the beginning of each experimental task, the

participants performed a calibration routine to coordinate eye position and screen

location. The participants fixated, in turn, on nine locations that were distributed

in a random order across the top, middle, bottom and at the left, centre and right

sides of the display. After calibration, the participants read the instruction and

then did a 12-trial practice (including one trial for prospective response) before

starting the formal tests. The participants were asked to judge whether the target

was present. Specifically, they were instructed to use their left middle finger to

press button ‘1’ on the response pad to indicate that the target was present or

press button ‘2’ with their left index finger if the target was not present. At the

same time, the patients were asked to use their right index finger to press button

‘3’ (representing the prospective response) when they saw fruit objects (the cues)

in the display rather than make a target present/absent response. Each trial began

by presenting the centred fixation for 500 ms. Then a word display specifying the

target appeared and remained visible for 500 ms before being replaced with the

search display. The search display remained visible until the participants pressed a

button to register a response (Fig. 1.). The participants’ eyes were tracked and their

response times were recorded from the onset of the search display until the

response.

2.4. Data Analysis

Repeated-measure multivariate analyses of covariance (MANCOVAs) and

correlation analyses were conducted for each dependent variable with the 0.05

level of significance (two-tailed). The effect size was measured by partial eta

squared (Zp2), with small, medium and large effects defined as 0.01, 0.06 and 0.14,

respectively (Cohen, 1988).

3. Results

Table 1 shows demographic and clinical characteristics of thetwo groups. Of the 38 participants, the age range was from 20 to37 years (mean¼ 28.11, S.D.¼4.56) and the education years werefrom 12 to 23 (mean¼18.53, S.D.¼ 3.31). There was no significant

Fig.1. The sequence of events on a trial: Participants start by fixating on the

centered symbol. Then, the display of a word specifying the target appears for

500 ms, followed by the display of the objects that remains visible until a response

is registered.

group difference in age and gender (P40.10). A group differencewas observed for years of education, t (36)¼3.46, P¼0.01. Thus,all further analyses comparing the depressed versus thenon-depressed group take years of education into account as acovariate.

3.1. Accuracy and reaction time data

The response accuracy and reaction time (RT; derived fromcorrect responses) under different stimuli conditions arepresented in Table 2. The difference in response accuracy andRT was quantified in a 4 (stimulus: target-only, cue-only, target-plus-cue and distracter-only)�2 (group: depressed and non-depressed) interaction. Participants with depression performedworse than the non-depressed group, F (1, 35)¼14.11, P¼0.001,Zp

2¼0.29. The accuracy of the depressed group was lower than

that of the non-depressed group in cue-only trials (P¼0.017) andtarget-plus-cue trials (Po0.00001). There were non-significantgroup differences in the target-only and distracter-only trials(Fo1). For the depressed group, accuracy of target-plus-cue trialswas lower than cue-only trials (P¼0.048); for the non-depressedgroup, there was no significant difference between accuracy oftarget-plus-cue and cue-only trials (P¼1.000). The depressedgroup had longer RTs than the non-depressed group, F (1,35)¼7.23, P¼0.011, Zp

2¼0.17. The RTs of the depressed group

were longer than those of the non-depressed group in cue-onlytrials (P¼0.011) and target-plus-cue trials (P¼0.021).There wereno significant group differences in target-only and distracter-onlytrials (P40.05). No differences were found between RTs of target-plus-cue and cue-only trials in the two groups (P40.1). In orderto explore the effects of fatigue and other time-related factors, weexamined the accuracy and RT data during the first and secondhalf times of the performance. The results indicated no significantdifferences.

3.2. Eye movement data for different stimuli conditions

For the eye movement data analyses, the regions of all objectsin four quadrants were defined as areas of interest (AOIs,8 cm�8 cm each), with position 1 located in the upper left,position 2 in the upper right, position 3 in the lower left andposition 4 in the lower right. The comparison of eye movementdata under different stimuli conditions in the depressed and thecontrol groups was conducted in hit trials.

Repeated-measure MANCOVAs on fixations, average fixationduration and total fixation duration were conducted (see Table 3).Participants in the depressed group displayed a larger number of

Page 4: Deficits in cue detection underlie event-based prospective memory impairment in major depression: an eye tracking study

Table 2Accuracy and reaction time (ms) for target only, cue only, target plus cue, and distracter only trials in non-depressed and depressed groups.

Group Target only Cue only Target plus cue Distracter only

Mean S.D. Mean S.D. Mean S.D. Mean S.D.

Accuracy

Non-depressed 0.92 0.06 0.68 0.22 0.61 0.17 0.95 0.04

Depressed 0.93 0.06 0.46 0.19 0.36 0.12 0.94 0.06

Reaction time

Non-depressed 1536.96 473.20 2169.21 771.09 1937.54 692.92 2055.91 641.58

Depressed 1883.16 556.83 3422.17 951.75 3036.61 904.46 2699.89 826.70

Table 3Mean number of fixations, average fixation durations (ms), total fixation durations (ms) for target only, cue only, target plus cue, and distracter only trials in non-depressed

and depressed groups.

Group Target only Cue only Target plus cue Distracter only

Mean S.D. Mean S.D. Mean S.D. Mean S.D.

Non-depressed

Mean number of fixations 1.48 0.17 2.27 0.15 1.97 0.41 1.62 0.30

Average fixation durations 196.89 16.71 201.87 29.42 206.36 35.74 192.76 20.86

Total fixation durations 286.36 30.67 424.74 57.42 397.15 97.05 307.85 76.23

Depressed

Mean number of fixations 1.87 0.22 2.61 0.30 2.37 0.21 2.06 0.39

Average fixation durations 208.49 22.47 214.55 26.62 233.64 20.70 207.62 26.41

Total fixation durations 385.25 66.17 547.84 60.08 544.34 64.75 429.30 124.30

S. Chen et al. / Psychiatry Research 209 (2013) 453–458456

fixations than those in the non-depressed group, F (1, 35)¼44.66,Po0.00001, Zp

2¼0.56, in all the c‘onditions. The analysis of the

average fixation duration data revealed longer average fixationdurations for participants with depression than for those in thenon-depressed group, F (1, 35)¼4.62, P¼0.039, Zp

2¼0.12. For the

non-depressed group, there were no differences between stimu-lus types; for the depressed group, the average fixation durationswere marginally longer for target-plus-cue trials than for target-only (P¼0.086) and distracter-only trials (P¼0.065). For totalfixation duration, the depressed group had longer total fixationdurations than the non-depressed group, F (1, 35)¼40.37,Po0.00001, Zp

2¼0.54, in all the conditions.

3.3. Analysis of target-plus-cues

We examined the probability of gazing at the cue and the targeton misses and hits for target-plus-cue trials (Table 4). A 2(response: hit or miss)�2 (group: depressed or non-depressed)�2 (focus of fixation: cue or target) MANCOVA wasconducted. The main effect of response was not significant, Fo1. Asignificant main effect of group was found, F (1, 35)¼82.33,Po0.00001, Zp

2¼0.70, and there was an interaction between

response and group, F (1, 35)¼43.33, Po0.00001, Zp2¼0.55; the

gaze rate was greater for the depressed group on hits than onmisses, but there was no difference for the non-depressed group.The main effect of focus of fixation was not significant, Fo1. Therewas a significant interaction between focus of fixation andresponse, F (1, 35)¼20.72, Po0.00001, Zp

2¼0.37, with higher gaze

rates for cues on hits than on misses and higher gaze rates fortargets on misses than on hits. No interaction between group andfocus of fixation was found, Fo1. Interaction between focus offixation, group and response was significant, F (1, 35)¼19.34,Po0.00001, Zp

2¼0.36, resulting from higher gaze rates on cues

and targets for the depressed group than for the non-depressed

group when cues were hit; the gaze rates on targets were higherfor the depressed group than for the non-depressed group andthere were no significant differences in gaze rate on cues betweenthe two groups when cues were missed.

3.4. Correlations

We examined relations between depression, as measured bythe BDI, and performance on the tasks. The results indicated thatdepression was negatively correlated with accuracy in cue-onlyand target-plus-cue trials, r¼–0.51 and –0.66, P’so0.01, andpositively correlated with RT and average fixation duration incue-only and target-plus-cue trials, r¼0.37 and 0.39, P’so0.01.Depression was also positively correlated with the number offixations and total fixation duration in all conditions, r¼0.47 to0.68, P’so0.001. These results were consistent with those in theMANCOVAs.

4. Discussion

Deficits in time-based PM have been discovered in depression.However, the nature and extent of depression-associated event-based PM impairment are poorly understood and need to beinvestigated because PM is of both theoretical and clinicalrelevance. The present study examined the cue detection in thenon-focal event-based PM of individuals with major depressivedisorder in comparison with individuals who were non-depressedusing behavioural and eye tracking methods. We found that theparticipants with depression performed more poorly on PM tasks(under cue-only and target-plus-cue conditions) than those in thenon-depressed group; the depressed group had lower accuracyand longer RTs under cue-only and target-plus-cue conditionsthan the non-depressed group. There were no significant

Page 5: Deficits in cue detection underlie event-based prospective memory impairment in major depression: an eye tracking study

Table 4Gaze rate (%) of cue and target for target plus cue trials.

Group Target plus cue

Hit Miss

Cue Target Cue Target

Mean S.D. Mean S.D. Mean S.D. Mean S.D.

Non-depressed (N¼19) 30.45 10.46 13.70 4.12 12.08 4.15 34.01 10.10

Depressed (N¼19) 67.77 10.69 34.05 11.96 12.86 4.53 53.67 11.85

S. Chen et al. / Psychiatry Research 209 (2013) 453–458 457

differences in accuracy and RTs between the two groups underongoing conditions (under target-only and distracter-only condi-tions). The results suggest possible PM damage in individualswith depression, which are in support of the previous study byAltgassen et al. (2009), who reported that the individuals withdepression displayed impaired PM function in the non-focalcondition.

For the eye movement data, the depressed group showed agreater number of fixations and longer average and total fixationdurations than did controls in both the ongoing and PM condi-tions, suggesting that participants with depression exertedgreater cognitive effort and focussed more attention on proces-sing displays when performing tasks. The average fixation dura-tions of participants with depression were longer for target-plus-cue trials than for target-only and distracter-only trials; however,there were no differences in controls between different types oftrials. Thus, individuals with depression may have difficultyfocussing on extracting information, especially under target-plus-cue conditions. These results were consistent with those ofcorrelational analyses. According to the resource allocation model(Ellis and Ashbrook, 1988), reduced overall cognitive capacity ofindividuals with depression may cause them to perform worse onPM tasks because they devote their attentional resources tointrusive, task-irrelevant or depression-related thoughts. A lowerlevel of cognitive capacity and decreased processing efficiencyrequire individuals with depression to make greater effort toperform on the tasks.

The results of the analyses of target-plus-cue trials wereconsistent with our hypothesis. The behavioural data revealedthat the depressed group had lower scores on accuracy in target-plus-cue trials than in cue-only trials, whereas there were nosignificant differences in the non-depressed group between thetwo types of trials. The results indicated that the presentation of atarget might hinder the performance of individuals with depres-sion on PM tasks. A comparison of eye movement data on the cueor target in target-plus-cue trials provided further evidence. Thedepressed group had a higher gaze rate of targets on hits andmisses than did controls but that there were no significantdifferences between the two groups in gaze rate of cue on misses,which also indicated that participants with depression had atendency to fixate on targets and that they had difficulty inshifting attention from ongoing trials to prospective trials. Thefindings are consistent with the literature that individuals withdepression may have deficits in executive functions such asset-shifting and inhibition (Beats et al., 1996; Purcell et al.,1997; Murphy et al., 1999; MacQueen et al., 2000; Austin et al.,2001; Markela-Lerenc et al., 2006; Holmes and Pizzagalli, 2008;Hugdahl et al., 2009) because of neuropsychological malfunctionsin the ACC and the PFC (Drevets, 2000; Brody et al., 2001).

The greater difficulty of individuals with depression on PMtasks is likely due to their ineffectiveness in strategically mon-itoring the environment for the presence of the cue event. Theexpending of relatively more resources on emotional processing

in individuals with depression may lead to a decline in cognitivecontrol function (Lemelin et al., 1997; Banich et al., 2009), whichin turn may weaken the inhibition of mood processing or facil-itate excessive activation in the amygdala and the fusiform brainareas (Ramel et al., 2007). Smith and Bayen (2004) proposed thatthe realisation of delayed intentions is dependent on the engage-ment of preparatory attentional processes that serve to monitorthe environment for prospective cues and on memory processesthat serve to discriminate prospective cues from non-cues (seealso Guynn, 2003). A critical assumption of this theory is thatpreparatory processes (i.e., strategic monitoring) must be engagedfor an intention to be realised. Our current findings indicated thatindividuals with depression had less cognitive capacity availableduring cognitive tasks and were thus unable to sufficiently engagethe preparatory attentional processes that served to monitor theenvironment for prospective cues.

The results of the present study constituted a significantcontribution to our understanding of relations between depres-sion and cognition. The study also had practical implications: itmight help professionals develop treatment methods that con-sider improving the availability of the cue to facilitate the realisationof intention, thus solving the daily problems such as treatment non-adherence in affective disorders (Lingam and Scott, 2002). A majorlimitation of our study was a relatively modest sample size.However, in the present study we were able to detect a large effectsize for each dependent variable with our current sample size.Future studies should aim at recruiting a larger number of partici-pants to confirm our findings. A potential bias might have occurredby comparing the depressed sample to a control non-depressedgroup with more years of education; however, the years of educa-tion was taken into account as a covariate in the data analysis.Moreover, the current study focussed on the cue detection in theevent-based PM. It will be important to investigate other phases ofPM process such as intention formation and retrieval for futureresearches.

In conclusion, the study shows evidence for the relationshipbetween depression and event-based PM function, pointing topossible PM damage in individuals with major depressivedisorder in the non-focal event-based PM condition. Investigatingthe visual attentional processing in cue detection showed thatparticipants with depression showed more fixations and longertotal and average fixation durations in both ongoing and PMconditions and target disturbed the detection of the cue forparticipants with depression. The state of depression may impairtop-down cognitive control function, which in turn results inparticular deficits in the engagement of monitoring for PM cues.

Acknowledgements

This work was supported by the Fundamental Research Fundsfor the Central Universities (2009SC-3), the National SocialScience Fund Project of China (11 & ZD187) and Shang Shan Fund.

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