## Abstract

Prospective memory (PM) is the ability to remember to do something in the future without explicit prompts. To date, little has been known about PM deficits in bipolar disorder (BD). This study examined the nature and correlates of PM in patients with BD. Forty clinically stable BD patients and 40 matched healthy controls formed the study sample. Socio-demographic characteristics, PM, psychosocial functioning, retrospective memory (RM), and IQ were measured in all participants, whereas clinical condition was measured in patients with standardized assessment instruments. Patients performed significantly more poorly on the time-based PM task than controls (10.6 ± 5.0 vs. 14.6 ± 3.0, p < .001). In correlation analyses, older age, lower education, more severe depressive and manic symptoms, poor psychosocial functioning, poor RM, and lower scores in IQ were significantly associated with poor performance in the time-based PM task, whereas poor RM and lower scores in IQ associated with poorer performance in the event-based PM task in patients. In multivariate analyses, severity of depression and older age significantly contributed to poor performance in the time-based PM task, whereas poor RM contributed to poor performance in the event-based PM task in patients. The time-based PM is impaired in BD patients. Depressive symptoms, age, and RM were determinants of certain aspects of impaired PM performance in BD patients.

## Introduction

Prospective memory (PM), a relatively new construct in memory research, was identified in the 1980s. PM, defined as “memory for activities to be performed in the future” (Einstein & McDaniel, 1990), is gaining attention in research and clinical practice (Kliegel, McDaniel, & Einstein, 2007) because it has potential impact on patients' activity of daily living and the management of their illness. Impairment of PM, such as forgetting to attend appointments as scheduled or take medication, could lead to poor outcome.

PM involves the encoding of an intention, retaining the information, executing the intention, and evaluating the outcome (Elvevag, Maylor, & Gilbert, 2003). Einstein and McDaniel (1990) identified two subtypes of PM: Time- and event-based PM. Time-based PM is defined as remembering to perform an action at a specific time, such as telephoning someone in the afternoon, whereas event-based PM refers to remembering to perform an action when an external cue appears, such as taking a look at a message when a particular person is seen. Subsequently, Kvavilashvili and Ellis (1996) advanced the notion of activity-based PM that is similar to event-based PM and it involves the retrieval of an intended action based on the appearance of an external cue at the end of an activity. Examples of activity-based PM tasks include switching off the oven after cooking or turning off the light when leaving a room.

Of the three subtypes of PM, time-based PM is the most difficult one because it requires more self-initiation, whereas there is no specific external cue to elicit the intention so the time has to be checked regularly to respond at the right moment. Compared with its time-based counterpart, event-based PM places less demand on self-initiation since it depends on an external cue as trigger. Activity-based PM is the easiest subtype since the external cue coincides with the end of an ongoing activity; thus, there is no need to interrupt an ongoing activity as in time- and event-based PM (Shum, Valentine, & Cutmore, 1999).

To date, only a few studies addressed PM and its correlates in psychiatric disorders and they mainly focusing on schizophrenia (e.g., Kumar, Nizamie, & Jahan, 2005, 2008; Shum, Ungvari, Tang, & Leung, 2004; Ungvari, Xiang, Tang, & Shum, 2008; Woods, Twamley, Dawson, Narvaez, & Jeste, 2007). Schizophrenia patients were found to perform significantly worse than controls in all PM tasks in these studies. PM deficits were also proposed to be trait-dependent characteristics constituting a primary deficit of the illness (Kumar et al., 2005; Wang et al., 2008).

A number of studies suggested that cognitive dysfunctions including memory, attention, and executive function deficits have to be considered as one of the features of bipolar disorder (BD) related to impaired psychosocial functioning and disability in BD patients (Robinson et al., 2006; Torres, Boudreau, & Yatham, 2007). However, most research was restricted to retrospective memory (RM; i.e., the memory for past information). To the best of our knowledge, to date no study has evaluated PM deficits and its correlates in BD.

We set out to evaluate two subtypes (time- and event-based) of PM in a sample of BD patients. The primary objective of the study was to compare PM performance between BD patients and healthy controls matched on basic demographic variables. The secondary objective was to clarify the potential relationships between PM and socio-demographic and clinical variables, psychosocial functioning, RM, and IQ in both BD patients and healthy controls.

The first hypothesis was that BD patients would perform significantly worse on both types of PM compared with controls. This hypothesis was based on well-established findings that BD patients show deficit in executive functioning and RM (Frantom, Allen, & Cross, 2008; Mur, Portella, Martinez-Aran, Pifarre, & Vieta, 2008a, 2008b), which, in turn, are associated with poor performance on PM (Kliegel, Martin, McDaniel, & Einstein, 2002; Shum et al., 1999). The second hypothesis was that one or more socio-demographic and clinical characteristics including age, education level, severity of depressive or manic symptoms, psychosocial functioning, RM, and IQ would be significantly associated with the performance on PM tasks in BD patients, whereas one or more of the above variables associated with the performance on PM tasks in controls as they were in healthy controls (Ungvari et al., 2008) or patients with schizophrenia (Henry, Rendell, Kliegel, & Altgassen, 2007; Kliegel et al., 2002; Ungvari et al., 2008).

## Materials and Methods

### Study Settings and Participants

The study was conducted during the period between October 2008 and June 2009. A convenience sample of 40 patients with BD was recruited from the outpatient clinic of a university-affiliated general hospital that has a catchment area with approximately 800,000 people. Forty healthy controls without a history of substance abuse and psychiatric, neurological, or major medical disorder approximately matched according to age (±2 years), sex, and education level (±2 years) were selected from a vocational training center (Hong Kong College of Technology).

Patients who met the following inclusion criteria entered the study: (a) diagnosis of BD according to ICD-10 (World Health Organization, 1992) and having been clinically stable for at least 3 months before recruitment (Deicken, Eliaz, Feiwell, & Schuff, 2001; Lobana, Mattoo, Basu, & Gupta, 2001); (b) Chinese ethnicity; (c) age between 18 and 65 years; and (d) at least primary education and ability to understand the requirements of the study. Exclusion criteria were: (a) electroconvulsive therapy in the past 12 months; (b) past or current significant drug/alcohol abuse; and (c) history of or current significant medical and neurological condition. Each participant was paid HK$300 (∼US$40) for travel expenses and to defray the cost of missing work.

The study protocol was approved by the Human Research and Ethics Committee of the Chinese University of Hong Kong-New Territories East Cluster (CUHK-NTEC). Written consent was obtained from all patients and controls.

### Outcome Measures and Assessment

The patients' socio-demographic data were collected by the raters with a questionnaire designed for the study. The 21-item Hamilton Depression Rating Scale (HAMD; Hamilton, 1960) was used to assess the severity of depressive symptoms. The severity of manic symptoms was rated with the 11-item Young Mania Rating Scale (YMRS; Young, Biggs, Ziegler, & Meyer, 1978). The overall psychosocial functioning was evaluated with the Global Assessment Scale (GAS; Endicott, Spitzer, Fleiss, & Cohen, 1976).

PM was assessed with the locally validated, Chinese version of the Cambridge PM Test (CAMPROMPT; Lou, Dou, Zheng, & Man, 2009). CAMPROMPT is the first standardized test to assess PM in an ecologically plausible context (Wilson et al., 2005). It consists of three event-based and three time-based PM tasks that take about 25 min to administer. The performance of each task is rated on a scale of 0–6 for a final score ranging from 0 to 36.

The Rivermead Behavioral Memory Test-Chinese version (RBMT; Wilson, Cockburn, & Baddeley, 1985) was used to measure RM. It consists of nine subtests. For each subtest, a score of 2 indicates normal functioning; borderline performance is scored as 1, and 0 indicates performance that with few exceptions is at a level at or below the lowest 5% of the population standard. The Total Profile Score is the sum of the subtest scores. The Chinese version of this test has been validated in Hong Kong (Man & Li, 2001).

IQ was assessed with the Test of Nonverbal Intelligence-Third Edition (TONI-3; Brown, Sherbenou, & Johnsen, 1997), a language-free intelligence test measuring intellectual functioning, aptitude, abstract reasoning, and problem solving. A 45-item picture book is presented and the correct answer has to be selected on each item. The items are arranged in the order of difficulty. An estimated intelligence quotient that ranges from 60 to 150 is obtained according to the raw score and the age of the subject.

### Procedures

Patients with BD completed all the above assessments, whereas healthy controls only completed the tests for intelligence, PM, and RM. All tests were administered in one session that usually lasted 2 h. If the participants seemed uncertain, instructions and explanation were repeated. A trained research assistant was responsible for assessing PM. A psychiatrist (EL), who was blind to the patients' performance on the PM tasks, rated the psychiatric symptoms, daily functioning, RM, and the level of intelligence after receiving training in administering these tests. Basic socio-demographic and clinical variables were collected during the interviews supplemented by a chart review and, whenever possible, interviewing patients' relatives.

### Statistical Analysis

The data were analyzed using SPSS 13.0 for Windows. The comparisons between the patients and the matched healthy controls were performed by the independent sample t-test, Mann–Whitney U-test, and chi-squared test as appropriate. The correlations between performances on time- and event-based PM tasks and socio-demographic and clinical factors were conducted for the two groups of participants separately using Pearson's correlation analysis given that the data followed normal distribution; otherwise, Spearman's rank correlation analysis was performed. Stepwise multiple linear-regression analyses were used to identify factors that predict performance on each PM task for the BD patients. Time- or event-based PM task was the dependent variable, and the independent variables were the significant correlates in the bivariate correlation analyses. To avoid multicolinearity, tolerance was used to measure the strength of the linear relationships between the independent variables; a tolerance value of 0.6 and above was regarded as acceptable. The normality of distributions for continuous variables was checked with the one-sample Kolmogorov–Smirnov test. Two-tailed tests were used in all analyses with the significance level set as .05.

## Results

Table 1 shows the socio-demographic and clinical factors separately for the 40 patients and the 40 healthy controls. Patients' scores were lower than those of the controls on the time-based PM task and RBMT scores, whereas there was no significant difference between the two groups on the event-based PM task. After controlling for the potential confounding effects of sex, age, education, RBMT total profile, and the TONI-3 deviation quotients scores by ANCOVA, the patients' performance on the time-based task—F(1,73) = 7.9, p = .006—remained lower than those of the controls, whereas there was still no significant difference between the two groups on the event-based PM task—F(1,73) = 0.02, p = .9.

Table 1.

Comparison of BD patients and healthy controls with respect to demographic and clinical characteristics

Patients (n = 40)

Controls (n = 40)

Statistics

N Percent N Percent χ2 df p-value
Men 15.0 17.5 0.1 .8
Mean SD Mean SD t df p-value
Age (year) 43.6 9.8 42.1 9.0 0.7 78 .5
Education (year) 10.3 2.7 10.2 1.7 0.2 78 .8
Age at onset (year) 29.3 9.0 — — — — —
Length of illness (year) 14.3 9.2 — — — — —
HAMD total score 10.8 7.2 — — — — —
YMRS total score 1.8 3.2 — — — — —
GAS score 71.5 9.7 — — — — —
Time-based PM task 10.6 5.0 14.6 3.0 −4.4 78 <.001
Event-based PM task 13.8 3.3 14.9 2.3 −1.7 78 .09
RBMT total profile score 18.5 4.7 22.1 2.3 −4.3 78 <.001
TONI-3 deviation quotients 86.5 10.7 91.3 14.2 −1.7 78 .09
Patients (n = 40)

Controls (n = 40)

Statistics

N Percent N Percent χ2 df p-value
Men 15.0 17.5 0.1 .8
Mean SD Mean SD t df p-value
Age (year) 43.6 9.8 42.1 9.0 0.7 78 .5
Education (year) 10.3 2.7 10.2 1.7 0.2 78 .8
Age at onset (year) 29.3 9.0 — — — — —
Length of illness (year) 14.3 9.2 — — — — —
HAMD total score 10.8 7.2 — — — — —
YMRS total score 1.8 3.2 — — — — —
GAS score 71.5 9.7 — — — — —
Time-based PM task 10.6 5.0 14.6 3.0 −4.4 78 <.001
Event-based PM task 13.8 3.3 14.9 2.3 −1.7 78 .09
RBMT total profile score 18.5 4.7 22.1 2.3 −4.3 78 <.001
TONI-3 deviation quotients 86.5 10.7 91.3 14.2 −1.7 78 .09

Notes: HAMD = Hamilton Depression Rating Scale; YMRS = Young Mania Rating Scale; BD = bipolar disorder; PM = prospective memory; RBMT = Rivermead Behavioral Memory Test; TONI-3 = Test of Nonverbal Intelligence-Third Edition.

The significance level was set as 0.05.

The correlations between PM performances and socio-demographic and clinical factors in the patients and healthy controls are shown in Table 2. For patients, older age, lower education, more severe depressive or manic symptoms, poorer psychosocial functioning, and lower scores in RBMT and TONI-3 were significantly associated with poorer performance in the time-based PM task, whereas lower scores in RBMT and TONI-3 associated with poorer performance in the event-based PM task. No variable was associated with any subtype of PM tasks for the controls.

Table 2.

Correlation between PM tasks and demographic and clinical characteristics in patients and controls

Time-based Event-based
Controls (n = 40)
Age (year) −.29 −.18
Educational level (year) −.19 .02
RBMT total profile score .19 .08
TONI-3 deviation quotients .23 .08
Patients (n = 40)
Age (year) −.42** −.45
Educational level (year) .38* .20
Age at onset (year) −.17 −.18
Length of illness (year) −.28 −.31
HAMD total score −.47** −.09
YMRS total score −.33* .17
GAS score .33* .11
RBMT total profile score .45** .59**
TONI-3 deviation quotients .38* .32*

Time-based Event-based
Controls (n = 40)
Age (year) −.29 −.18
Educational level (year) −.19 .02
RBMT total profile score .19 .08
TONI-3 deviation quotients .23 .08
Patients (n = 40)
Age (year) −.42** −.45
Educational level (year) .38* .20
Age at onset (year) −.17 −.18
Length of illness (year) −.28 −.31
HAMD total score −.47** −.09
YMRS total score −.33* .17
GAS score .33* .11
RBMT total profile score .45** .59**
TONI-3 deviation quotients .38* .32*

Notes: RBMT = Rivermead Behavioral Memory Test; PM = prospective memory; TONI-3 = Test of Nonverbal Intelligence-Third Edition; HAMD = Hamilton Depression Rating Scale; YMRS = Young Mania Rating Scale; GAS = Global Assessment Scale.

*p < .05; **p < .01.

Table 3 presents the results of stepwise multiple regression analyses exploring the predictors of performance on PM tasks. Severity of depression and older age significantly contributed to poor performance in the time-based PM task, whereas the lower score in RBMT contributed to poor performance in the event-based PM task.

Table 3.

Results of the stepwise multiple regression analysis (patients; n = 40)

PM task Predictor Beta p-value 95% CI
Time-based: Adjusted r2 = .41; r2 change = .22; F(2,37) = 14.5; p < .001 HAMD total score −0.5 <.001 −0.5, −0.2
Age −0.5 <.001 −0.4, −0.1
Event-based: Adjusted r2 = .33; r2 change = .35; F (1,38) = 20.2; p < .001 RBMT total profile score 0.6 <.001 0.2, 0.6
PM task Predictor Beta p-value 95% CI
Time-based: Adjusted r2 = .41; r2 change = .22; F(2,37) = 14.5; p < .001 HAMD total score −0.5 <.001 −0.5, −0.2
Age −0.5 <.001 −0.4, −0.1
Event-based: Adjusted r2 = .33; r2 change = .35; F (1,38) = 20.2; p < .001 RBMT total profile score 0.6 <.001 0.2, 0.6

Notes: HAMD = Hamilton Depression Rating Scale; YMRS = Young Mania Rating Scale; PM = prospective memory; RBMT = Rivermead Behavioral Memory Test.

## Discussion

This is the first study to examine PM impairment in BD patients and its relationship with socio-demographic and clinical variables, RM, IQ, and social functioning.

The first hypothesis that BD patients would show impairment in the two subtypes of PM compared with controls was partly confirmed. Patients had a significantly worse performance in time-based PM compared with controls (p < .001, effect size = 0.44). Although they also had a worse performance in event-based PM than controls, the difference did not reach a statistically significant level (p = .09, effect size = 0.19).

Previous neuropsychological and neuroimaging studies suggested that PM is associated with impairment in prefrontal-lobe functions (Henry et al., 2007; Shum et al., 2004; Simons, Scholvinck, Gilbert, Frith, & Burgess, 2006; Woods et al., 2007) and executive dysfunctions (Kondel, 2002; Shum et al., 2004; Ungvari et al., 2008; Woods et al., 2007). Converging evidence from a number of studies indicated that cognitive impairment, particularly deficit in executive functions, persistently exists in BD patients (Bora, Yucel, & Pantelis, 2009; Frangou, Donaldson, Hadjulis, Landau, & Goldstein, 2005; Frantom et al., 2008; Martinez-Aran et al., 2004; Mur et al., 2008a, 2008b; Thompson et al., 2007). Therefore, it is plausible to assume that executive dysfunctions in BD patients would possibly impair PM functions.

The fact that the time-based task yields a greater difference between patients and controls than does the event-based task could be interpreted by the different processes involved in them. The time-based PM task requires self-initiated retrieval and subsequent interruption of an ongoing activity in contrast to the event-based task that only requires interruption of an ongoing activity (Kvavilashvili & Ellis, 1996). Time-based tasks place more demand on the prefrontal cortex (Einstein, McDaniel, Richardson, Guynn, & Cunfer, 1995) that mediates executive functions (Ritch, Velligan, Tucker, Dicocco, & Maples, 2003). These results are in line with our earlier findings (Shum et al., 2004; Ungvari et al., 2008) and those of others (Kumar et al., 2008; Wang et al., 2008) in schizophrenia patients.

The second hypothesis that one or more socio-demographic and clinical characteristics would be significantly associated with the performance on PM tasks in BD patients, whereas one or more of them associated with the performance on PM tasks in controls was also partly confirmed. In accord with earlier findings in both schizophrenia patients (Henry et al., 2007; Shum et al., 2004; Ungvari et al., 2008; Woods et al., 2007), better time-based PM performance was associated with younger age and higher educational level in this study.

Little is known about the impact of affective symptoms on PM. Rude, Hertel, Jarrold, Covich, and Hedlund (1999) published the only study of PM in patients with depression. These authors investigated time-based PM in 20 clinically depressed adults and 20 healthy controls and found that depressed subjects had impairments in time-based PM. Schmidt (2004) examined the impact of the September 11, 2001, attacks on college students' PM and found that participants who had highly emotional reactions to the attack demonstrated poor PM suggesting the effect of negative affects on PM. Consistent with these findings, an inverse relationship between depressive symptoms and the time-based PM task was found in this study. The negative impact of depressive symptoms on PM performance could be accounted for by the “resource allocation model” (Ellis & Ashbrook, 1988), that is, a person's emotional state allocates processing resources. Negative affective states give rise to intrusive, irrelevant thoughts, which then compete with relevant cognitive activities including PM performance in BD (Kliegel et al., 2005). Harris and Menzies (1999) reported that event-based PM was only influenced by anxiety, but not depressive symptoms. Partly supporting this notion, in this study, event-based PM was also unrelated to depressive symptoms; anxiety was not measured. This study also demonstrated the negative impact of manic symptoms on PM that has not previously been reported in the literature. The relative influence of specific emotional states on different PM performances needs to be further explored.

There is growing evidence that overall cognitive functions and social adaptation in patients with severe psychiatric disorders are closely related (Addington & Addington, 2008). Therefore, it was expected that deficits of PM in BD patients would lead to disorganized life and psychosocial functioning. This was borne out by the fact that time-based PM performance was positively associated with psychosocial functioning in this study.

Time-based PM is a complex concept that involves multiple cognitive processes including an RM component—the process of retrieving the content of the intention—and a specific action that will be carried out at a specific time (Einstein & McDaniel, 1996; Kliegel et al., 2002). Neuroimaging studies also suggested that PM is related to the frontal lobe and medial temporal structures, whereas RM is related to the latter (Altgassen, Kliegel, Rendell, Henry, & Zollig, 2008). The MRI findings could explain the association between PM and RM in BD patients found in this study. Similar to earlier findings in schizophrenia patients (Henry et al., 2007), higher IQ was associated with better performances in both time- and event-based PM.

In multivariate analysis, only the severity of depression and older age independently contributed to poor performance in time-based PM task, while poor RM contributed to poor performance in event-based PM task. Both depression and aging lead to dysfunction of the prefrontal cortex (Bergfield et al., 2010; Drevets, 2000; Manji, Drevets, & Charney, 2001) that mediates PM. Our results also replicated an early finding in healthy subjects that aging was related to the time-based PM only, but not with the event-based PM (Einstein et al., 1995). The association between RM and event-based PM could be accoutered for by the retrospective component included in PM tasks (Livner, Berger, Karlsson, & Bäckman, 2008).

This sample was recruited from the psychiatric outpatient clinic of a teaching hospital; therefore, the findings could approximate the real clinical situation regarding the PM impairment of BP patients. However, the results should be interpreted with caution because of methodological limitations. First, theoretically, in order to minimize the state- and medication-dependent biases on PM, stricter criteria of stability (such as HAMD total score below 8 and YMRS total score below 6) should have been used and medication-free or drug-naïve patients should have been enrolled. For obvious ethical and logistical reasons, this was not possible nor would it have reflected routine clinical practice. Second, illiterate and more severely ill patients who could not cooperate were excluded from the study; thus, the results may not be applicable to patients at other stages of their illness. Third, a more thorough selection of cognitive measures should be included in future studies. Fourth, the study was cross-sectional; therefore, the causality of relationships could not be explored. Further limitations included the predominantly male sample and the use of the GAS that relies upon subjective ratings.

### Clinical Implication

This preliminary study adds new insight into the cognitive deficits in BD. The results indicate that BD patients' impaired PM could contribute to their difficulties in psychosocial functioning, making re-entry to the community difficult. Good understanding of the PM deficit in BD could facilitate the development of more efficient management and rehabilitation for these patients. A practical approach to alleviate patients' impairment in time-based PM (e.g., forgetting medication at a specific time) would be to convert these tasks into event-based PM tasks (e.g., linking drug taking to the ring of an alarm clock).

## Funding

This study was supported by a grant from the Chinese University of Hong Kong (Direct Grants for Research: Project No. 2041452).

None declared.

## Acknowledgements

The work was part of a dissertation to complete the Hong Kong College of Psychiatrists Part III Examination (unpublished). The authors would like to thank Professor Barbara Wilson and Pearson Assessment for permission to translate the CAMPROMPT into Chinese and to use it for research purpose. They also thank all of the patients and healthy controls involved in the project for their assistance.

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