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Behavioural Brain Research 189 (2008) 220–225

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Emotional memory and migraine: Effects of amitriptylineand sex related difference

Antonella Gasbarri a,∗, Benedetto Arnone a, Assunta Pompili a, Agata Cifariello a,Carmine Marini b, M. Clotilde Tavares c, Carlos Tomaz c

a Department of Sciences and Biomedical Technologies, University of L’Aquila, Italyb Department of Internal Medicine, University of L’Aquila, Italy

c Laboratory of Neurosciences and Behavior, University of Brasilia, CEP 70910-900 Brasilia, DF, Brazil

Received 1 October 2007; received in revised form 10 December 2007; accepted 13 December 2007Available online 23 December 2007

bstract

Many studies suggest that emotional arousal improves memory storage. The aim of this study was to evaluate the effects of emotional contentn explicit memory in untreated cephalalgic patients and in migraineurs treated with the antidepressant amitriptyline. We utilized an adaptationf two versions of the same story, with different arousing properties (neutral or emotional), which have been already employed in experimentsnvolving the enhancing effects of emotions on memory retention.

Subjects of the present study were healthy subjects and cephalalgic patients, suffering from migraine headache, which included untreatedigraineurs and migraineurs treated with the antidepressant amitriptyline. The findings of our experiments suggest that chronic migraine is related

o memory impairment. Taking into account that migraine is associated with major depression, in the present research the effect of the antidepressantmitriptyline was also evaluated. Our results showed that amitriptyline has an impairment effect on memory. In fact, the untreated migraineurs,

ompared to treated, recalled the most emotional phase of the arousal story significantly better. Then, our data suggest that amitriptyline preventshe enhancing effects of emotional content on memory processes. Moreover, in agreement with our previous data, this study suggests the existencef gender differences in the processing of emotional stimuli and underscores the importance of sex on emotional memory mechanisms.

2007 Elsevier B.V. All rights reserved.

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eywords: Emotional stimuli; Antidepressant amitriptyline; Migraineurs

It is very well known that emotional events are better mem-rized than neutral events.

Migraine represents a common headache disorder with sig-ificant mental, physical and social health implications [16], andan be influenced by adrenergic, peptidergic and serotonergicystems [25,30]. Contradictory evidence exists about the effectf migraine on cognitive functions. Previous studies reportedhat the performance of migraineurs, compared to controls, wasignificantly lower on a variety of cognitive measures, including

ests assessing attention, information processing, and memory24,30]. Therefore, chronic migraine could cause a persistent,ubtle central nervous system dysfunction. Conversely, other

∗ Corresponding author at: Department of Biomedical Sciences and Technolo-ies, University of L’Aquila, Via Vetoio, Coppito 67100 L’Aquila, Italy.el.: +39 0862 433447; fax: +39 0862 433318.

E-mail address: antonella.gasbarri@cc.univaq.it (A. Gasbarri).

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166-4328/$ – see front matter © 2007 Elsevier B.V. All rights reserved.oi:10.1016/j.bbr.2007.12.009

nvestigations failed to find impairing of cognitive functions ofigraine headache patients, compared to controls, supporting

he hypothesis that migraine is typically a neurologically benignyndrome [2,17].

The aim of this research was to evaluate the effects of emo-ional content on declarative memory on patients suffering of

igraine, comparing differences in memory between subgroupsf treated and untreated patients, and evaluating sex differencesmong the groups.

In this research, we utilized the adaptation to an Italian samplef two stories with different arousing properties (neutral andmotional), already employed in experiments with both brainnjured and healthy subjects, involving the enhancing effects of

motions on memory retention [8,9,11,13,28].

We evaluated two kinds of migraineurs: one untreated andnother treated with amitriptyline, a reference tricyclic antide-ressant [1,29].

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We also investigated the influence of gender on the evaluationf emotional content, taking into account that recent evidencerom research on animals and humans revealed apparently large,ut formerly unsuspected, sex-related effects on nervous mech-nisms subserving the relation between emotion and memory3,11,12,35,36]. Therefore, understanding brain responses tomotional material may require careful attention to the effectsf sex.

Subjects were 151 volunteers divided into three groups,quivalent in terms of age (mean age 30 ± 3,7), gender, cul-ural level (college education with urban background), race,ducation: 48 (24 men and 24 women) healthy subjects (controlroup), 55 (24 men and 31 women) untreated migraineurs, 48 (24en and 24 women) migraineurs treated with the antidepressant

mitriptyline.Healthy subjects were individuals with no physical or mental

isorders. The migraine patients were recruited at the Neurologi-al Clinic of the University of L’Aquila; migraine was diagnosedy clinic specialists based on the criteria of the Headache Clas-ification Committee of the International Headache Society2004). The two samples of patients were comparable and sim-lar in the severity of illness, such as frequency and intensity ofttacks, comorbidity with depressive illness, etc.

Self medicate migraineurs were excluded from the groups ofigraineurs that were not on prescribed treatment.The patients included in this study were not suffering from

ther conditions that may affect memory performance.In this study, the patients participated at the experiments dur-

ng headache-free intervals, as reversible cognitive decline wasbserved during migraine attacks [22,30]. In fact, it has beeneported that subjects with headache pain during a memory taskhowed poorer performance because the pain interferes withheir ability to pay attention during the memory task, rather thanith retrieval [20].In this study, we used the same procedure as in previous

esearches [8,11,13,28,35]. Participants gave informed consento participate in the study. The stimulus materials, alreadytilized in previous studies [8,11,13,35], consists in a set oflides, accompanied by the narrative of two versions of a simpletory—one neutral and one arousal. The slides were the same,ven though there was a difference in the arousing properties ofhe story content.

According to previous findings [8,11,13,35], the story can beivided into 3 phases: phases 1 and 3, consisting of relatively nonmotional material, and phase 2 containing emotionally arousinglements; memory was tested by means of both free recall andecognition test.

A three-way ANOVA with repeated measures was utilizedo analyze the data obtained. ANOVA included story (neu-ral, arousal), patients (healthy, untreated migraineurs, treated

igraineurs), phase of story (1, 2, 3) as within-subjects factornd gender as between-subject factor. ANOVA was followedy the Tukey’s Honestly Significant Different (HSD) test. All

esults are presented as mean ± SEM. Statistical significanceas set at p < 0.05.The evaluation of the ratings of emotionality showed that

n men, in the arousal group, the treated migraineurs rated the

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Research 189 (2008) 220–225 221

tory as being more emotional compared to healthy subjectsF(1, 22) = 5.03; p < 0.035]. The healthy subjects and both thentreated and treated patients rated the emotionally arousing nar-ative as being more emotional than the neutral [F(1, 22) = 8.74;< 0.007], [F(1, 22) = 6.64; p < 0.017] and [F(1, 22) = 25.09;< 0.0001], respectively. The values of the mean emotional rat-

ng for the arousing versus the neutral story were the following:n the healthy subjects 6.00 (±0.36) versus 4.25 (±0.46), in thentreated migraineurs 6.25 (±0.59) versus 4.58 (±0.25), and inhe treated migraineurs 7.16 (±0.36) versus 4.16 (±0.47).

In women, the healthy subjects and both the untreated andreated patients rated the arousing narrative as being moremotional than the neutral [(F(1, 22) = 10.53; p < 0.003)],(F(1, 29) = 23.01; p < 0.0001)] and [F(1, 22) = 38.59;< 0.0001], respectively. The values of the mean emo-

ional rating for the arousing versus the neutral story were theollowing: in the healthy subjects 7.16 (±0.38) versus 4.66±0.66), in the untreated migraineurs 7.47 (±0.47) versus 4.33± 0.33), and in the treated migraineurs 7.83 (± 0.29) versus.25 (±0.49), respectively.

The influence of the emotional content on memory was eval-ated by means of free recall and recognition test.

In men (Fig. 1A), the results of free recall showed that,n the arousal condition, the three groups showed a betteremory in the healthy subjects, compared to both untreated

F(1, 22) = 8.96; p < 0.009] and treated [F(1, 22) = 10.28;< 0.007] migraineurs; furthermore, the difference between

he two groups of migraineurs was statistically differentF(1, 22) = 9.86; p < 0.004]. In the neutral group, significant dif-erences between the total amount of information recalled wasound between the treated migraineurs and healthy subjectsF(1, 22) = 7.97; p < 0.009]. The healthy subjects of the arousalroup, compared to neutral, recalled a number of units of infor-ation significantly higher [F(1, 22) = 13.92; p < 0.001].Mean recall of healthy subjects, in the arousal and neu-

ral conditions, was 12.92 (±1.22) and 6.25 (±1.29) unitsf information for participants, respectively. In the untreatedigraineurs, mean recall was 10.33 (±0.68) and 9.25 (±0.87)

nits of information for participants in the arousal and neutralonditions, respectively. In the treated migraineurs, mean recallas 10.83 (±0.50) and 10.17 (±0.48) units of information forarticipants in the arousal and neutral conditions, respectively.

In women (Fig. 1B), in the arousal group, signifi-ant differences were found between the total amount ofnformation recalled by the healthy subjects and both thentreated [F(1, 29) = 11.31; p < 0.002] and treated migraineursF(1, 22) = 9.86; p < 0.004]; moreover, the difference betweenhe two groups of migraineurs was statistically differentF(1, 29) = 10.98; p < 0.008]. In the neutral group, significant dif-erences were found between the healthy subjects and both thentreated [F(1, 22) = 14.35; p < 0.001] and treated migraineursF(1, 22) = 15.31; p < 0.0007].

Mean recall of healthy subjects was 17.58 (±1.70) and 16.50

±1.46) units of information for participants in the arousal andeutral conditions, respectively. In the untreated migraineurs,ean recall was 12.00 (±0.79) and 10.58 (±0.52) units of infor-ation for participants in the arousal and neutral conditions,

222 A. Gasbarri et al. / Behavioural Brain Research 189 (2008) 220–225

Fig. 1. Free recall in men (A) and women (B), and sex related differences in the arousal (C) and neutral (D) conditions. (A) The figure shows the levels of significancein the arousal group of controls compared both to untreated and treated migraineurs (*p < 0.009 and **p < 0.007, respectively), and the difference between the twogroups of migraineurs (***p < 0.004). The differences between controls and treated migraineurs of the neutral group (�p < 0.009) and between controls of the arousaland neutral groups are also indicated (�p < 0.001). (B) The figure shows the levels of significance in the arousal group of controls compared to both untreated and

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reated migraineurs ( p < 0.002 and p < 0.004, respectively), and the differenontrols and both the untreated (�p < 0.001) and treated migraineurs (��p < 0.0omen in the arousal condition (*p < 0.036). (D) Difference between healthy m

espectively. In the treated migraineurs, mean recall was 11.75±0.73) and 10.33 (±0.56) units of information for participantsn the arousal and neutral conditions, respectively.

In the free recall of the arousal story (Fig. 1C), the compari-on between male and female healthy subjects showed in womenbetter memory compared to men [F(1, 22) = 4.94; p < 0.036].

n the free recall of the neutral story (Fig. 1D), the comparisonetween male and female healthy subjects showed a better mem-ry in women, compared to men [F(1, 22) = 27.34; p < 0.0001].

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ig. 2. Recognition memory in men (A) and women (B). (A) The figure indicates: th

nd treated migraineurs for phase A2, compared to the N condition (�p < 0.0009,hase A2 in controls compared to both untreated and treated patients (*p < 0.002 aigraineurs (�p < 0.0006). (B) The figure indicates: the levels of significance in rela

hase A2, compared to the N condition (�p < 0.001, �p < 0.015, and ��p < 0.001, reo both untreated and treated migraineurs (�p < 0.008 and ��p < 0.0001, respectively

tween the two groups of migraineurs ( p < 0.008). The difference betweenof the neutral group is also indicated. (C) Difference between healthy men andd women in the neutral condition (�p < 0.0001).

The recognition test (Fig. 2) evidenced no overall differ-nce between all the groups, but a phase-by-phase comparisonevealed a difference between the groups for phase 2 of the sto-ies, which contains the emotional informations. The numbersfter the letters indicate the story phase of the arousal (A) andeutral (N) conditions.

As shown in Fig. 2A, in men, in the healthy subjects, the totalecognition in phase 2 of the arousal group statistically differedrom those of the neutral group [F(1, 22) = 14.56; p < 0.0009];

e levels of significance in relation to the total recognition in controls, untreated

p < 0.0008, and p < 0.019, respectively), the better recognition memory fornd **p < 0.0001, respectively), and the difference between the two groups oftion to the total recognition in controls, untreated, and treated migraineurs forspectively), the better recognition memory for phase A2 in controls compared), and difference between the two groups of migraineurs (♦p < 0.001).

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oreover, both in the untreated and treated migraineurs, in phase, the recognition for participants who heard the emotionallyrousing narrative statistically differed from the subjects of theeutral group [F(1, 22) = 14.59; p < 0.0008] and [F(1, 22) = 6.29;< 0.019], respectively. The comparison of the three maleroups for the phase 2 of the arousal version highlightedstatistically better recognition memory in the healthy sub-

ects compared to both untreated [F(1, 22) = 12.37; p < 0.001]nd treated migraineurs [F(1, 22) = 36.33; p < 0.0001]. Fur-hermore, the two groups of migraineurs were statisticallyifferent [F(1, 22) = 15.82; p < 0.0006]. No statistically sig-ificant difference between the participants in the neutralnd arousal condition was evidenced for both phase 1 andhase 3.

In addition, the healthy subjects in the neutral conditionsnswered an average of 54% and 60% of the questions, respec-ively. The untreated and treated migraineurs in the neutralondition answered an average of 51% and 42% of the questions,espectively, and participants in the arousal condition correctlynswered 52% and 48%, respectively.

In the healthy women, the total recognition for participantsf the arousal group statistically differed from the subjects ofhe neutral group [F(1, 22) = 13.50; p < 0.001]. Moreover, bothn the untreated and treated migraineurs, the total recogni-ion for subjects of the emotional group statistically differedrom those of the neutral group [F(1, 29) = 6.68; p < 0.015] andF(1, 22) = 14.34; p < 0.001], respectively (Fig. 2B).

The comparison of the three female groups for the phase 2f the arousal version of the story highlighted a statistically bet-er recognition memory in healthy subjects compared to bothntreated [F(1, 29) = 7.87; p < 0.008] and treated migraineursF(1, 29) = 79.66; p < 0.0001]. Furthermore, the two groupsf migraineurs were statistically different [F(1, 29) = 13.25;< 0.001].

The healthy subjects of the neutral and arousal conditionsnswered an average of 65% and 71%, respectively. Bothhe untreated and treated migraineurs in the neutral conditionnswered an average of 56% and 48% of the questions, respec-ively, while participants in the arousal condition were correctn 57% and 50%, respectively.

No statistically significant difference between the partici-ants in the neutral and arousal condition was evidenced in theecognition memory for both phase 1 and phase 3.

The comparison between men and women of the three groupsid not show any statistical difference both in arousal and neutralersions of the story.

Our results support the view that processes promoting recol-ection are facilitated for negative events [18,33] and that chronic

igraine is associated with memory impairment. Pain negativelympacts cognitive functioning, such as learning and memory, and

emory dysfunctions in migraineurs have already been reported7,23,30]. These cognitive defects, however, were not confirmedy other authors who did not find significant differences between

igraineurs and controls [26]. These discordances might be

xplained by differences in the choice of subjects: the patientsf previous studies [4], together with the subjects we examinedn the present research, came from headache clinics, whereas

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Research 189 (2008) 220–225 223

thers [21,24] were recruited among the general population ortudents.

In addition, results from headache pain and memory studiesuggest that pain, as it adversely affects memory, may operatet a threshold level rather than on a dose-response continuum20].

Our data suggest that chronic migraine is related to memorympairment. In fact, the performance of both the memory testsf men and women in the arousal group evidenced significantifferences between the healthy subjects and the two groups ofigraineurs (Fig. 2). In the female neutral group (Fig. 2A), sig-

ificant differences were found between the healthy subjectsnd both the treated and untreated migraineurs; in the maleeutral group (Fig. 2B), differences were found between thereated migraineurs and healthy subjects: this apparent discrep-ncy could be explained in terms of higher level of attentionhowed by treated migraineurs, who expressed to the experi-enters their great motivation for any scientific study focused

n migraine.Taking into account that migraine can be associated with

ajor depression, we also evaluated the effect of the antide-ressant amitriptyline, which represented the treatment of theubjects of one of the two groups of migraineurs we examined.ertiary tricyclic antidepressants (TCAs), such as amitriptyline,re very effective in the treatment of panic disorder, migrainend major depression, which is also associated with migraine14,29]. Even though, antidepressants may ameliorate the socialnd occupational life of depressed patients, they can also have aegative effect due to the negative impact on psychomotor andognitive functions [37]. The risk of impairment varies widelymong antidepressants, depending also on their pharmacologicalroperties. TCAs block histaminergic, adrenergic and cholin-rgic receptors, which may induce sedation and performancempairment in a variety of tasks [37]. Moreover, drugs with anti-holinergic properties may interfere particularly with attentionnd memory processes, although very few studies report conclu-ions on the specificity of the cognitive effects of TCAs [6]. Ourndings show that expectations concerning the effects on mem-ry of the amitriptyline were confirmed. In fact, the performancef both the memory tests of men and women in the arousal groupvidenced significant differences between the healthy subjectsnd the two groups of migraineurs; in the neutral group, statis-ically significant differences were found between the healthyubjects and both the treated and untreated migraineurs. More-ver, statistical differences in the recognition test were foundetween treated and untreated migraineurs, both in male andemale, suggesting that amitriptyline prevents the enhancingffects of emotional content on memory processes.

In our experiments, we considered separately men andomen, taking into account that a rapidly increasing number of

tudies involving human subjects document neurobiological dif-erences between the sexes. Functional sex-related differencesave been reported in brain correlates of emotional [10,12] and

acial processing [19,38], auditory [27,31] and language pro-essing [5,32], working memory [15,34]. In agreement with ourrevious data [11,12], the findings from free recall suggest thexistence of gender differences in the processing of emotional

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timuli and, therefore, the importance of taking these differencesnto account during investigation of emotional processing. Theyre also consistent with the interpretation that women are moreusceptible than men towards negative experiences and loweredood, and this may have implications on the pathophysiology

f mood disorders, such as depression [18].Although, memory disturbances in migraineurs have already

een reported, the mechanisms relating emotional memory andigraine, and the brain regions involved are still unknown.

n migraine patients, brain perfusions abnormalities, mostlyypoperfusion areas, were found. It has been postulated thatersistent abnormalities in regional cerebral blood flow ofigraineurs could reflect vascular factors involved in the patho-

enesis of the headache [4]. However, as decreased brainerfusion could result also from impaired neuronal activity,n alternative explanation is that these changes could be theonsequence of frequently repeated migraine attacks. This lastossibility would be coherent if a link between neuropsy-hological disturbances and hypoperfusion of specific areas,uch as medial temporal lobe (MTL) structures, involved inmotional memory, can eventually be established. Then, aonnection between MTL structures and migraine could beypothesized. Future research will need to examine the possi-ility that migraine could impair memory consolidation throughmechanism involving MTL.

cknowledgements

We thank Dr. Liliana Ercole for language assistance and Dr.aria Luisa Battistini for statistical evaluation assistance.

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