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Abstract

Introduction

Prospective memory is the ability to carry out a delayed intended action, so to maintain and retrieve future plans, goals and activities. Deficits of prospective memory negatively impact on patients and caregivers’ everyday living and determine poor adherence to treatment. Since frontal regions are involved in both event- and time-based prospective memory tasks and are impaired in migraine without aura, defects of prospective memory might occur in migraine without aura patients; until now this issue has not been investigated. The aim of the current study was to explore time- versus event-based prospective memory in migraine without aura.

Patients and methods

Ninty-one consecutive migraine without aura patients and 84 healthy subjects were enrolled in the study. They underwent a standardized measure of prospective memory evaluating both time-based and event-based prospective memory, and the Montreal Cognitive Assessment assessing global cognitive status. Moreover, all participants completed the Beck Depression Inventory-II and a self-administered version of the Apathy Evaluation Scale, to assess severity of depressive symptoms and apathy, respectively.

Results

Migraine without aura and healthy subjects did not differ on demographic aspects (i.e. age, education and gender). However, individuals with migraine without aura demonstrated impaired prospective memory performance compared to healthy subjects, with a greater impairment demonstrated for the time-based tasks. Within the migraine without aura group, no significant association was found between prospective memory performance and clinical scores, apathy, and depression.

Conclusions

Individuals with migraine without aura experience particular difficulty executing a future intention; therefore, migraine without aura is associated with dysfunction of prospective memory.

Keywords

Migraine prospective memory cognitive deficit cognitive dysfunction depression apathy

Introduction

Prospective memory (PM) is the ability to carry out a delayed intended action, so to maintain and retrieve future plans, goals and activities (1). PM is crucial for everyday life, for example someone remembering to buy milk on the way home from work when they see groceries, and remembering to take medication at a specific time. In other terms, an intention can be triggered by occurrence of an external event (event-based PM) or after a defined amount of time (time-based PM) (1). According to an influential multiprocess model (2), PM involves several phases: a) forming an intention; b) associating the intention with a retrieval cue (i.e. time based or event-based); c) retaining this association over an interval that can vary from minutes to weeks, during which the intention representation must be retained; d) upon noticing the retrieval cue, disengaging from an ongoing task; e) retrieving the appropriate intention, and f) properly implementing the intention.

Neuroimaging studies have consistently revealed the involvement of the rostral prefrontal cortex (RPFC; BA 10) in PM tasks (3,4). Active maintenance of intention while performing another task would be related to increased activity in the lateral RPFC (3), whereas disengagement from an ongoing task would relate to deactivation of the medial part of the RPFC (4). The increased activation of lateral RPFC and deactivation of medial RPFC is consistently found during both time-based and event-based PM tasks (5 –10), whatever the characteristics of the cues (4,11). A recent fMRI study confirmed that time-based and event-based PM tasks share a similar cerebral network, mainly centered on frontal and parietal regions, but also showed engagement of further differential cortical regions as a function of the task. Among these, event-based tasks would involve stronger activation in occipital areas compared with time-based tasks, likely reflecting continuous monitoring of the environment until visual cues are encountered, whereas time-based tasks would mainly recruit frontal regions, likely involved in time estimation processes (12). Impairments of PM are often associated with frontal dysfunctions in several neurological disorders (i.e. Parkinson’s disease, multiple sclerosis) (13,14).

Patients affected by migraine without aura (MwoA) can present dysfunctions in the executive/attention and visuospatial domains (15 –17). These observations are consistent with neuroimaging findings revealing that MwoA is associated with reduced functional connectivity in the fronto-parietal network even in the absence of clinically-overt executive dysfunctions (18). Since frontal regions are involved in both event- and time-based PM tasks, it is highly likely that fronto-parietal functional alterations are related to impaired functioning of PM in MwoA patients. Occurrence of possible impairments of PM in MwoA patients could have relevant clinical implications, since deficits of PM could negatively impact on patients’ everyday living (19), reduce adherence to treatment (20), and ultimately contribute to maladaptive stress responses (21). However, until now, no study has investigated PM in MwoA patients. Therefore, in the present study, we used a standardized test assessing time- and event-based PM to compare performance of a sample of MwoA patients not receiving treatment for prevention of migraine attacks (drug-naive) with a sample of age- and education-matched healthy subjects.

Materials and methods

Subjects

In the present study, consecutive patients with clinical diagnosis of MwoA were recruited at the Headache clinic of the First Division of Neurology of the University of Campania “Luigi Vanvitelli”, Naples. Each patient had to fulfill the following inclusion and exclusion criteria to be eligible for in the present study: a) Diagnosis of MwoA according to the ICHD-III beta version of the International Headache Society (e-1); b) normal neurological examination; c) no other ICHD-III diagnosis (e.g. tension type headache, chronic migraine, migraine symptoms compatible with acute confusional migraine), somatic or psychiatric disorders; d) no current or previous intake of any pharmacological migraine preventive therapy.

In each patient, we recorded the following clinical aspects: Disease duration; migraine attacks per month; mean pain intensity during migraine attacks by means of visual analogic scale (VAS). Moreover, to obtain an accurate assessment of patients’ headache-related disability, migraineurs completed the Migraine Disability Assessment Scale (e-2) and the Headache Impact Test -6 (e-3).

To avoid any possible interference related to migraine attacks or to pharmacological treatment on cognitive functions, all MwoA patients were migraine free, and not taking rescue medications, for at least 3 days before and after the neuropsychological assessment. To ascertain this point, patients were interviewed 3 days after neuropsychological assessment.

After enrolment of MwoA patients, we selected a sample of healthy individuals (HCs) with demographic features as similar as possible to those of the patients. HCs were recruited from among patients’ friends and employees at the university centres, and were included if they gave their written informed consent to participate on a voluntary basis. HCs had to meet the following selection criteria: Lack of history of migraine or any other type of headache according to clinical criteria; lack of migraine familiarity in first degree relatives; lack of previous or current psychiatric diseases (e.g. major depression, or psychosis according to DSM-V criteria); no use of psychoactive drugs. The references of clinical diagnostic criteria and tools used in the present study are reported in supplemental material 1 (e-1 to e-8).

Standard protocol approvals, registrations, and patient consents.

All selected patients and HCs gave their written informed consent to participate in the study, which was approved by the Local Ethics Committee and was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.

Materials and procedures

MwoA patients and HCs underwent the Italian version of Montreal Cognitive Assessment (MoCA) to assess the global cognitive status and different cognitive domains: Attention, memory, language, visual-spatial orientation and executive functions (e-4). The total score ranges from 0 (worst performance) to 30 (best performance). To assess depressive symptoms and apathy, all participants completed the Beck Depression Inventory (BDI) - II (e-5), and a self-administered version of the Apathy Evaluation Scale (AES) (e-6) respectively.

To evaluate PM, all MwoA patients and HCs underwent the Italian version of the Memory for Intentions Screening Test (MIST) (e-7), a standardized test that requires delayed execution of intended actions to be performed in the context of an ongoing foreground task.

The MIST is characterized by internal reliability (e-8). It includes eight PM tasks balanced for delay interval (2-min or 15-min delay), cue (time-based or event-based), response modality (verbal or motor response). Series of word search puzzles are provided as a foreground (i.e. distractor) task to prevent overt rehearsal of the prescribed intentions. The score of each trial is rated 0 to 2: Two points are credited for a correct recall of the task carried out at the right time (±1 minute) and for a correct response provided within a given time window after an associative cue; one point is credited for a correct response produced out of time and for a wrong response given at the right time; 0 points are assigned for no response, wrong responses to an associative cue, or a wrong response produced at the wrong time.

Additionally, participants complete a three-choice recognition test for cue-target association immediately after completion of the MIST (recognition task score ranges 0–8). Finally, to obtain a 24-hour probe, participants were instructed to leave a telephone message for the examiner the following day specifying the number of hours slept the night after the assessment (24 h item score ranges 0–2).

The Italian version of the MIST also provides guidelines for standardized qualitative error coding. Therefore, it allows identification of the following error types: a) no response (i.e. omission errors, NR); b) task substitution (TS) errors (e.g. when the participant substitutes an action for a verbal response, or vice versa, or provides a novel response, i.e. an intrusion); c) Loss of Content (LC), when a participant recognizes a PM cue, but indicates that he/she has forgotten all or part of the task; d) Loss of Time (LT), when a subject performs a correct response at the wrong time (i.e. ± 15% of the target execution time); e) Loss of Function (Omissions), when the subject performs only a part of the task or gets distracted prior to task completion; f) Random (R) error is coded for those responses that cannot otherwise be classified (e-8).

Statistical analysis

Data were checked for normality by the Shapiro-Wilks test of normality (p < 0.05), revealing that all behavioural and cognitive variables were significantly non-normally distributed.

We used nonparametric statistics to analyze data. Group differences on the demographic, behavioural variables and cognitive performance on all subtests of the MIST were analyzed using Chi-square, Mann-Whitney U tests and Quade’s rank analysis of covariance (a nonparametric equivalent of analysis of covariance, ANCOVA, e-9), as appropriate. Spearman’s rank correlations were used to examine relationships between clinical, cognitive (i.e. MoCA total and domains scores) and behavioral variables (BDI-II, AES) and performance on each of the subtests of the MIST in the MwoA group. The critical alpha level for all analyses was set at 0.05.

The same analyses were performed to compare two subgroups of MwoA patients and HCs matched for level of global cognitive functioning, as assessed by MoCA total score.

All statistical analyses were performed by the SPSS program.

Results

In the present study, we enrolled 91 consecutive MwoA patients and 84 healthy subjects. The two groups did not differ on demographic variables, AES and BDI-II, but MwoA patients had significantly lower MoCA scores than HCs (Table 1).

Table 1.

Demographic and clinical aspects of migraineurs without aura (MwoA) and healthy subjects (HC).

Parameters	MwoA (Mean ± SD)	HC (Mean ± SD)	p
Age (years)	33.82 ± 10.53	32.27 ± 1041	0.315
Gender (Females/males)	75/16	66/18	0.521
Education (years)	13.71 ± 3.34	14.13 ± 2.9	0.408
MoCA adjusted total score	22.61 ± 2.76	23.92 ± 2.24	0.003
MoCA: n of subjects with impairment*	1	0	–
BDI-II	9.74 ± 7.83	8.23 ± 6.31	0.306
AES-S: Total	30.58 ± 6.37	29.11 ± 5.54	0.104
Disease duration (years)	12.18 ± 9.11
Attacks per month	4.42 ± 3.65
MIDAS score	21.06 ± 13.48
HIT-6 score	58.08 ± 8.56
VAS score	8.21 ± 0.89

MoCA: Montreal Cognitive Assessment; BDI - II: Beck Depression Inventory – II; AES - S: Self-version of Apathy Evaluation Scale; MIDAS: Migraine Disability Assessment Scale; HIT-6: Headache Impact Test -6; VAS: Visual Analogue Scale.

MoCA score below Italian cut-off value.

Descriptive data on the MIST in the MwoA and HC groups are displayed in Table 2. The Mann-Whitney U test revealed that MwoA patients performed significantly worse than HCs on each subscale of MIST (i.e. time-based and event-based scales, the multiple choice recognition test, and 24-h item). As for the type of errors produced on MIST, the Mann-Whitney U test revealed that MwoA patients made significantly more TS than HCs. No significant difference was found for other types of errors (Table 3).

Table 2.

Descriptive data on the Memory for Intentions Screening Test (MIST) in groups of migraineurs without aura (MwoA) and healthy subjects (HC).

Parameters	MwoA (Mean ± SD)	HC (Mean ± SD)	p from Mann-Whitney U test	Cliff’s delta	p from Quade test	η ²
Total time-based	5.22 ± 1.59	6.20 ± 1.63	<0.001	−0.37	<0.001	0.082
Total event-based	6.81 ± 1.49	7.33 ± 1.11	0.018	−0.18	0.067	0.019
Recognition	7.67 ± .59	7.90 ± 0.33	<0.001	−0.18	0.003	0.049
24 h	1.10 ± 0.97	1.45 ± 0.87	0.014	−0.18	0.049	0.022

Note. Significant differences are reported in bold.

Table 3.

Comparison between migraineurs without aura (MwoA) and healthy subjects (HC) on type of errors produced on Memory for Intentions Screening Test.

Parameters	MwoA (Mean ± SD)	HC (Mean ± SD)	p from Mann-Whitney U test	Cliff’s delta	p from Quade test	η ²
NR	0.77 ± 1.03	0.51 ± 0.76	0.100	0.13	0.312	0.006
TS	0.67 ± 0.90	0.32 ± 0.64	0.004	0.21	0.009	0.039
LC	0.54 ± 0.72	0.33 ± 0.62	0.030	0.16	0.049	0.022
LT	0.27 ± 0.44	0.21 ± 0.44	0.287	0.07	0.258	0.007
PLO	0.12 ± 0.39	0.13 ± 0.37	0.692	−0.02	0.535	0.002
PLR	0.00 ± 0.00	0.00 ± 0.00	1		–	–
R	0.09 ± 0.35	0.04 ± 0.18	0.355	0.03	0.208	0.009

NR: Omission error; TS: task substitution; LC: Loss of Content; LT: Loss of Time; PLO: Loss of Function (omission); PLR: Loss of Function (repetition); R: random.

Since MwoA and HC groups significantly differed on MoCA, we used Quade’s rank analysis of covariance to control for the potential effect of such a difference on MIST measures. In this supplementary analysis (see Table 2), the group was considered as the independent variable and the MoCA total score as the covariate, with all subtests of the MIST as the dependent variables. This statistical analysis confirmed the significant differences between the two groups on the time-based scale, recognition task and 24-h item, but did not confirm the differences between the two groups on the event-based scale.

To avoid the confounding effect of difference between the two groups on MoCA, we also used Mann-Whitney tests to compare the MIST scores achieved by two subgroups of patients and controls who were matched for demographic features and global cognitive functioning (n = 78 for each group). The results showed that the two subgroups differed for time-based PM score and on the recognition task, but not on the event-based PM score and on the 24-h item score (Table 4).

Table 4.

Comparisons between migraineurs without aura (MwoA) and healthy subjects (HC) matched for demographic features and global cognitive functioning.

Parameters	MwoA (Mean ± SD)	HC (Mean ± SD)	p for Mann-Whitney U test	Cliff’s delta
Age (years)	33.47 ± 11.02	32.41 ± 10.61	0.561	0.05
Education (years)	13.92 ± 3.34	14.14 ± 2.94	0.713	−0.03
Gender (F/M)	63/15	62/16	0.841
MoCA adjusted total score	23.39 ± 1.92	23.57 ± 1.88	0.401	−0.08
Total time based	5.36 ± 1.48	6.15 ± 1.66	<0.001	−0.33
Total cue based	6.86 ± 1.49	7.28 ± 1.13	0.082	−0.14
Recognition	7.69 ± 0.56	7.90 ± 0.34	0.006	−0.17
24 h	1.19 ± 0.96	1.41 ± 0.88	0.154	−0.11
NR	0.59 ± 0.813	0.53 ± 0.78	0.510	0.05
TS	0.74 ± 0.94	0.35 ± 0.66	0.003	0.23
LC	0.55 ± 0.73	0.36 ± 0.64	0.062	0.15
LT	0.28 ± 0.45	0.23 ± 0.45	0.385	0.06
PLO	0.14 ± 0.41	0.14 ± 0.38	0.834	0.01
PLR	0.00 ± 0.00	0.00 ± 0.00	1	–
R	0.10 ± 0.38	0.03 ± 0.15	0.143	0.05

MoCA: Montreal Cognitive Assessment; F: Female; M: Male; NR: Omission error; TS: task substitution; LC: Loss of Content; LT: Loss of Time; PLO: Loss of Function (omission); PLR: Loss of Function (repetition); R: random. Note. The significant differences are reported in bold.

Correlational analysis

In the MwoA group, the correlational analysis showed no significant association of total MIST score and of all MIST subscales with apathy, depression and clinical scores. Moreover, no significant correlation was found between total MIST score and of all MIST subscales with MoCA (Table 5).

Table 5.

Correlational analysis between Memory for Intentions Screening Test, clinical, cognitive and behavioral variables within group of migraineurs without aura (MwoA).

		Memory for Intentions Screening Test
		Total Time based	Total Event based	Recognition	24 h
MoCA score	rho	0.229	0.14	−0.016	0.184
	p	0.029	0.187	0.878	0.08
BDI-II	rho	0.1	−0.006	0.027	–0.211
	p	0.348	0.956	0.797	0.045
AES-S- Total	rho	−0.001	0.038	−0.018	–0.109
	p	0.996	0.723	0.867	0.303
Disease duration	rho	−0.197	−0.032	−0.005	0.044
	p	0.099	0.793	0.967	0.713
Attacks per month	rho	−0.063	0.152	0.078	0.038
	p	0.6	0.206	0.52	0.751
MIDAS score	rho	−0.09	0.003	0.205	0.039
	p	0.456	0.979	0.086	0.748
HIT-6 score	rho	−0.144	−0.092	0.233	–0.103
	p	0.229	0.446	0.051	0.391
VAS score	rho	−0.057	−0.046	0.044	–0.058
	p	0.609	0.683	0.692	0.601

MoCA: Montreal Cognitive Assessment; BDI – II: Beck Depression Inventory – II; AES – S: Self-version of Apathy Evaluation Scale; MIDAS: Migraine Disability Assessment Scale; HIT-6: Headache Impact Test -6; VAS: Visual Analog Scale for pain.

In the HC group, the total MIST and its subscales scores were not significantly associated with any cognitive and behavioural variables (Supplemental Material 2).

Discussion

The present study investigated time- and event-based PM in consecutive outpatients affected by MwoA compared with HC. The direct comparison between the two groups showed that MwoA patients achieved lower scores on time-based and event-based PM tasks than HCs, although the deficit was slightly stronger for time-based tasks. These findings could not be explained by demographic factors, as the two groups were closely matched for these variables, but in principle they could be ascribed to differences in cognitive status assessed by MoCA, consistent with findings from a previous study (22). To control for this potential bias, we applied two different procedures: On one hand, we covariated MIST scores on the basis of MoCA scores by means of a non-parametric statistical test (i.e. the Quade’s rank analysis of covariance); on the other hand, we performed a comparison on the MIST scores achieved by two subgroups of MwoA patients and HCs matched for demographic features and global cognitive functioning. These two procedures provided convergent results in showing that the difference between the two groups on the time-based PM score and the recognition score is more solid than that on the event-based PM score. Moreover, the additional analysis for the two subgroups with the same level of global cognitive functioning also showed no difference on the 24-h item.

The deficit in time-based PM might be explained by the fact that this kind of task requires high levels of cognitive control (23). In fact, efficient performance on time-based PM tasks strongly requires engagement of self-initiated monitoring (e.g. clock checking) and retrieval (e.g. time perception) processes compared to event-based tasks, as reported in Raskin et al. (24). The deficit on the time-based PM task found in our patients suggests that MwoA patients might experience particular difficulty in managing the concurrent cognitive demands of the ongoing task and of strategic time monitoring. Previous studies showed that a longer delay interval between intention formation and subsequent retrieval would have a negative impact on PM accuracy in both healthy (25,26) and clinical populations (24,27), although different findings have been reported for longer delays, over days or weeks (28). Indeed, during the delay interval, one needs to maintain the deferred intent to act and remember the content of the intention-cue pairing in the face of possible decay and interference. In this respect, the multiprocess model (2) posits that long delay between intention formation and execution of the intention may influence PM performance negatively: A longer delay may require more strategic control by placing greater demands on limited executive resources supporting cue detection and monitoring (2).

The finding that error analysis showed significantly more task substitution errors in MwoA patients than in HCs might indirectly support the idea of less efficient executive functions in our patients, since task substitution errors (including intrusions and perseverations) are often ascribed to executive control deficits (29), likely reflecting perseverative tendencies.

In the present study, the analysis of the total sample of MwoA patients showed significantly lower scores than HCs on the MIST recognition task. Consistent with the idea of a dysexecutive origin of PM deficit, this difficulty might also be ascribed to impairments in attentional control with consequent proactive interference, often reported in dysexecutive syndromes (30). However, since the recognition task can be employed to assess the retrospective memory component of PM (i.e. encoding, retention, and retrieval of intentions), our findings, together with high rate of TS, might also suggest a failure of retrospective memory in MwoA patients who could monitor for and detect the right cue, but would fail to recall the correct intention.

It is noteworthy that significant difference between the two groups on the 24-h item was found even after applying the Quade test, but not after comparing MwoA and HCs subgroups with similar demographic features and level of global cognitive functioning. This evidence suggested that the successful performance on this item might be strongly related to efficient global cognitive functioning. Moreover, since this item has been related to more naturalistic memory tasks compared to the remaining MIST tasks (24), we could then infer that MwoA patients with efficient global cognitive functioning likely develop effective strategies (e.g. use of compensatory devices or reminders) to limit the impact of memory deficits on daily life, as in other patient populations (25), thus reducing interictal and postictal allostatic load. In individuals with decreased global cognitive functioning, such strategies might not be developed properly.

The present study is characterized by some limitations. The first is related to the fact that the present samples of MwoA patients and HCs, although showing similar demographic features, differed significantly on a measure of global cognitive functioning (MoCA), as previously demonstrated (22); however, we controlled for the possible confounding effect of this cognitive difference by applying two different procedures (i.e. the Quade test and Mann-Whitney test to compare PM scores between MwoA patients and HCs with similar levels of global cognitive functioning).

The second limitation is related to the lack of a thorough neuropsychological assessment. In this study we only used MoCA, which can provide an estimate of functioning in several cognitive domains (31,32), but future studies might consider including specific neuropsychological tests for the relevant cognitive domains, including retrospective long-term memory, frontal/executive functions, but also time monitoring (33). This seems particularly important to assess possible correlations between scores on PM tasks and performance on memory and executive tests. Indeed, such correlational analysis would provide further cues for interpretation of the failure of PM in MwoA patients.

In conclusion, our results revealed an impaired PM in migraineurs, which seems to be associated with a dysfunctioning of prefrontal systems. Since some lesion and neuroimaging studies have showed the engagement of prefrontal systems particularly in time-based PM tasks (7,12,34), our findings are consistent with neuroimaging studies on MwoA patients revealing significant reduction of functional connectivity within the fronto-parietal networks known to be associated with executive functions (18,35). Since deficits in PM increase the risk of poor medication adherence across different clinical populations, deficient PM could be an important target for cognitive neurorehabilitation efforts. Early identification of patients having difficulty with PM would allow detection of individuals in need of cognitive interventions aimed at safeguarding personal autonomy and quality of life.

Clinical implications

Prospective memory (PM) is the ability to carry out a delayed intended action, so to maintain and retrieve future plans, goals and activities.

Individuals with migraine without aura (MwoA) demonstrated impaired prospective memory performance compared to healthy subjects (HCs).

A greater impairment was demonstrated for the time-based tasks in MwoA.

Individuals with MwoA experience particular difficulty executing a future intention, which seems to be associated with a dysfunctioning of prefrontal systems frequently reported in MwoA.

Since deficits in PM increase the risk of medication adherence across various clinical populations, deficient PM could be an important target for cognitive neurorehabilitation efforts to improve medication adherence.

Early identification of patients experiencing difficulty with PM would allow addressing them with cognitive interventions aimed at improving PM and thus safeguarding personal autonomy and quality of life.

Supplemental Material

Supplementary material 1 -Supplemental material for Prospective memory is dysfunctional in migraine without aura

Supplemental material, Supplementary material 1 for Prospective memory is dysfunctional in migraine without aura in Cephalalgia

Supplemental Material

Supplementary material 2 -Supplemental material for Prospective memory is dysfunctional in migraine without aura

Supplemental material, Supplementary Material 2 for Prospective memory is dysfunctional in migraine without aura in Cephalalgia

Footnotes

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

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