Hormonal contraception usage is associated with altered memory for an emotional story

Substantial evidence now documents sex-related influences on the neurobiology of emotional memory. Robust sex influences exist, for example, on the amygdala’s role in emotional memory formation, as well as on retention of central information (gist) and detail for an emotional event. Evidence also suggests that the well-documented effects of stress hormones on memory depend upon sex hormone levels. Since hormonal contraception alters sex hormone levels, and must by extension alter sex/stress hormone interactions in memory, we examined whether the use of hormonal contraception also alters memory for an emotional story. Two groups of healthy female subjects—one naturally cycling, one using hormonal contraception—viewed either a brief, emotionally arousing story, or a closely matched, but more emotionally neutral story. Each subject’s eye movements and pupil dilation changes were recorded as they viewed the story. Additionally, saliva samples were taken throughout the experimental session to examine salivary alpha-amylase, a biomarker for norepinephrine. A surprise free recall test one week later measured story memory in all subjects. Naturally cycling women exhibited enhanced memory of story details, but not of central information (gist), in the emotional compared with neutral story conditions. In contrast, women using hormonal contraception exhibited enhanced memory of gist, but not story details, in the emotional compared with neutral story conditions. Analysis of eye movements made while watching the stories indicated that the differences in memory could not be attributed either to a differential attention focus or to the degree of arousal induced by the stories in the two groups. These findings suggest that the use of hormonal contraception alters memory for an emotional event, perhaps by altering sex/stress hormone interactions in memory formation. They also suggest that further investigation of the mnemonic effects of these very widely used treatments is warranted.     

Sex-related impairment of memory for emotional events with beta-adrenergic blockade

On the basis of recent evidence indicating a sex-related lateralization of amygdala function in memory for emotional events, together with substantial evidence suggesting hemispheric specialization in processing global (central) versus local (detail) aspects of a situation, and the established dependence of the amygdala's memory modulating function on beta-adrenergic receptor activation, we predicted differential effects of a beta-adrenergic receptor antagonist (propranolol) on long-term memory for an emotionally arousing story in men and women. Specifically, we predicted that, relative to placebo, propranolol would impair memory for information central to the story line, but not memory for peripheral story details in men. Conversely, propranolol would impair memory for peripheral details, but not for central information in women. Here we confirm this prediction with a novel analysis of data from our two published studies of propranolol's effect on memory for an emotionally arousing story. These findings demonstrate a sex-related impairment of memory for emotional information by beta-adrenergic blockade. Additionally, they provide support for the hypothesis that, in this paradigm, emotional arousal enhances long-term memory for central information in men via activation of right amygdala/hemisphere function, and enhances long-term memory for peripheral details in women via activation of left amygdala/hemisphere function.     

Boys don't cry: Cognitive load and priming increase stereotypic sex differences in emotion memory

The results of three experiments provide evidence that the relative accessibility of stereotypes about sex difference influences people's memory of very recent emotions. Being under high rather than low cognitive load caused females compared with males to recall experiencing more intense emotional reactions to saddening stimuli (Experiments 1 and 2), and relatively less intense reactions to angering stimuli (Experiment 2). Being directly primed with stereotypes about sex differences and being under high cognitive load both caused females to recall more intense reactions to saddening stimuli compared with females who were neither primed with stereotypes nor under cognitive load (Experiment 3). These results imply that the relative accessibility of stereotypes influences memories of emotion in a manner similar to stereotypes' influence on social perception. Implications of these findings for theories of emotion memory and for self-perpetuating stereotypes about emotional sex differences are discussed.     

The Impact of Anxiety on Memory for Details in Spider Phobics

According to the attentional narrowing account of emotional memory, physiological arousal results in attention being directed towards central rather than peripheral characteristics of the situation. Consequently, memory for central details would be relatively good, whereas memory for peripheral information would be impaired. The present experiment sought to test this attentional narrowing hypothesis under highly stressful conditions. Spider phobics and low-fear controls were confronted with a large live spider, eliciting high levels of emotion in the phobic group. Afterwards, subjects' memory for the experimental situation was tested. On a cued recall test, phobics displayed a poor memory for peripheral detail information relative to control subjects. There were no differences between phobics and controls with respect to central detail information. Thus, the present data provide partial support for the attentional narrowing account of emotional memory. © 1997 by John Wiley & Sons, Ltd.     

Sex differences in the correlation of memory span with scan and other episodic memory tasks

Three studies of the relationship between memory span and other measures of memory and information processing are reported here. These other measures included memory scanning rate, the short- and long-term components of free recall, and word recognition from long-term memory. All three studies produced evidence for a sex difference in the correlation of these tasks with memory span. The first study produced a partial replication of Chiang and Atkinson's report (Memory & Cognition, 1976, 4,661–667) of a sex difference: for males, span and scanning rate were unrelated, while for females they were positively correlated. The second study showed that span and the primary memory component of free recall had a modest positive correlation for females but not for males, while span was unrelated to measures of secondary or long-term memory for females but was consistently positively related for males. In the third study, recognition accuracy and span were uncorrelated for females, but positively correlated for males. Finally, a reanalysis of data from a large-scale study by Underwood, Baruch, and Malmi (Journal of Experimental Psychology: General, 1978, 107, 393–419) also showed evidence of similar sex differences. Sex differences involving the correlation of memory span with other cognitive test performances seem quite general and need to be taken account of in the analyses of individual differences in memory and cognitive processes. A tentative theory is presented to account for the differences found in these studies.     

A male advantage for spatial and object but not verbal working memory using the n-back task

Sex-related differences have been reported for performance and neural substrates on some working memory measures that carry a high cognitive load, including the popular n-back neuroimaging paradigm. Despite some evidence of a sex effect on the task, the influence of sex on performance represents a potential confound in neuroimaging research. The present study investigated sex-related differences in verbal, spatial, and common object versions of the high cognitive load "n-back" working memory task. Eighteen male and 18 female undergraduates completed all 3 versions of the task. A mixed ANOVA, with Sex (male and female) as the between-subjects factor and Condition (verbal, spatial, and object) as the within-subjects repeated measure revealed that males were significantly more accurate than females on the spatial and object versions of the n-back task and performed equivalently to females on the verbal version of the task. Although the expected female advantage for verbal working memory was not found using this effortful n-back task, these results support a male advantage for high cognitive load spatial and object working memory. Future research should take into account the influence of sex on performance of the n-back task, and examine sex-related differences in working memory using other paradigms.     

Effect of negative emotional pictures on associative memory for peripheral information

We investigated the influence of negative emotional pictures on associative memory. A visual object was embedded in the periphery of negative emotional or neutral pictures. Memory was assessed for central item (pictorial) information, peripheral (object) information, and the association between item and peripheral information. On tests of item information, negative emotional pictures were remembered better than neutral pictures. However, associative memory between item and peripheral information was less accurate when the pictures were negative compared to neutral. This occurred despite equivalent recall (Experiments 1 and 2) and recognition (Experiment 2) for the peripheral objects themselves. Further experiments confirmed that performance on the associative test was not influenced by testing order (Experiment 3). These findings suggest that negative emotional arousal can particularly disrupt the associative binding of peripheral information to a central emotional event.     

Cross-cultural differences for three visual memory tasks in Brazilian children

Norms for three visual memory tasks, including Corsi's block tapping test and the BEM 144 complex figures and visual recognition, were developed for neuropsychological assessment in Brazilian children. The tasks were measured in 127 children ages 7 to 10 years from rural and urban areas of the States of S?o Paulo and Minas Gerais. Analysis indicated age-related but not sex-related differences. A cross-cultural effect was observed in relation to copying and recall of Complex pictures. Different performances between rural and urban children were noted.     

Do sex differences in emotionality mediate sex differences in traits of psychosis-proneness?

The aim of the study was to determine if sex differences in emotionality might account for sex differences in distinct traits of proneness to psychosis (or "schizotypy"). Females report higher levels of "positive" schizotypy (e.g., magical thinking) than males, along with a tendency toward greater schizotypal disorganisation, whereas males report higher levels of "negative" schizotypal traits, such as social anxiety (Jackson & Claridge, 1991; Raine, 1992). Given the affect-oriented nature of "negative" schizotypal traits, we tested the hypothesis that higher levels of "negative" schizotypy among males would be accounted for by more general sex differences in emotionality; that is, by less frequent and less intense emotional experiences. A total of 81 student participants were administered the Cognitive-Perceptual Deficits, the Disorganisation, and the Interpersonal Deficits components of Raine's (1991) Schizotypal Personality Questionnaire (SPQ), indexing respectively, "positive" schizotypy, schizotypal disorganisation, and "negative" schizotypy. Frequency of emotional experience was assessed using the Emotionality subscale (Buss & Plomin, 1984) and intensity, the Affect Intensity Measure (Larsen & Diener, 1987). As predicted, males scored significantly higher than females on the SPQ Interpersonal Deficits component but no sex differences emerged for the other two components. Males reported significantly less intense, although not less frequent, experiences than females. A reduced intensity of positive emotions in particular was found to mediate the sex difference in "negative" schizotypy. Our results suggest that a less intense experience of positive affect might contribute to males' propensity to develop negative symptoms should a schizophrenic breakdown occur.     

Are attentional resources a mediator for sex differences in memory?

The divided attention paradigm was used to investigate sex differences in encoding and retrieval processes of memory. Participants performed a memory and reaction time (RT) task under full attention and two divided attention conditions, that is, at encoding and retrieval. Results revealed that females recalled significantly more words than males under the full attention and divided attention at encoding conditions. Results further showed that secondary task costs were larger for males than females during divided attention at retrieval. Furthermore, regardless of sex, recall was best under full attention and worst under divided attention at encoding conditions. In relation to the RT task, RTs were shorter under full attention and longer under the divided attention at retrieval condition. Overall, these results show that females recall more words than males possibly due to a more severe effect of reduced attention during encoding than retrieval for males. The current findings thus suggest that a reduction in attentional resources may mediate sex‐related decreases in word recall.     

The role of overt attention in emotion-modulated memory

The presence of emotional stimuli results in a central/peripheral tradeoff effect in memory: memory for central details is enhanced at the cost of peripheral items. It has been assumed that emotion-modulated differences in memory are the result of differences in attention, but this has not been tested directly. The present experiment used eye movement monitoring as an index of overt attention allocation and mediation analysis to determine whether differences in attention were related to subsequent memory. Participants viewed negative and neutral scenes surrounded by three neutral objects and were then given a recognition memory test. The results revealed evidence in support of a central/peripheral tradeoff in both attention and memory. However, contrary with previous assumptions, whereas attention partially mediated emotion-enhanced memory for central pictures, it did not explain the entire relationship. Further, although centrally presented emotional stimuli led to decreased number of eye fixations toward the periphery, these differences in viewing did not contribute to emotion-impaired memory for specific details pertaining to the periphery. These findings suggest that the differential influence of negative emotion on central versus peripheral memory may result from other cognitive influences in addition to overt visual attention or on postencoding processes.     

Effects of repeated retrieval of central and peripheral details in complex emotional slides

Research has demonstrated that repeated retrieval enhances memory for practised verbal information, but undermines correct recall of unpractised related verbal information, a phenomenon known as retrieval-induced forgetting (RIF). This paper addresses the question of what happens with memory for unrehearsed aspects of an emotional picture when retrieval of other aspects of that picture is practised. In two experiments we investigated whether repeated retrieval of certain details of negative emotional slides undermines recall of unrehearsed details of such slides. In Experiment 1 retrieval of peripheral details was practised. The results demonstrated that recall for peripheral details was enhanced. However, correct recall of unpractised central details remained unaffected. Furthermore, retrieval practice did not alter the number of commission errors. Experiment 2 revealed that repeated retrieval of central details enhanced memory for these details. Although more commission errors were produced, again correct recall was not impaired for the unrehearsed central and peripheral details. This failure to find retrieval-induced forgetting effects for complex visual material is at odds with the RIF literature, and potential reasons for this are discussed. The data also extend previous studies in demonstrating that extensive retrieval can increase the number of commission errors.     

Emotional memory for central and peripheral details in children with callous-unemotional traits

A limited number of studies have shown that adults and adolescents with psychopathic traits suffer from emotional memory impairment. The present study examined whether this finding could be replicated in a sample of children between 8 and 12?years of age with callous-unemotional (CU) traits. Children with high CU traits (n?=?24) were compared with children with low CU traits (n?=?18) with regard to performance on a peripheral memory recognition test that examined memory for central and peripheral components of neutral and negative pictures. Results showed that overall recognition rates did not differ between the high- and low-CU groups. For negative pictures, both groups demonstrated better recognition of the central component at the expense of the peripheral component, while for neutral pictures, the peripheral component was better recognized than the central component. This study is the first to demonstrate that children with high CU traits do not suffer from an impaired emotional memory. Copyright ? 2012 John Wiley & Sons, Ltd.     

Simultaneity in Processing of Verbal and Spatial Information

Recent studies involving recall of verbal and spatial information produced conflicting results. In some cases investigators found males recalled verbal and spatial information equally well whereas females did less well on spatial than verbal information, but in other cases no sex differences were found. They also differed in that one study found processing of verbal and spatial information to be independent whereas others suggested trade-offs might occur. Using college-age subjects (17-25 yrs) with equal numbers of males and females (total n = 186) two experiments were performed to examine these differences. Although overall differences were found favoring verbal recall, females’ recall of spatial information was relatively poorer than males. Using a procedure designed to avoid possible artifactual depression of combined performance, we concluded that processing of spatial and verbal information is simultaneous in nature.

     

Sex differences in object location memory and spatial navigation in Long-Evans rats

In both humans and rodents, males typically excel on a number of tasks requiring spatial ability. However, human females exhibit advantages in memory for the spatial location of objects. This study investigated whether rats would exhibit similar sex differences on a task of object location memory (OLM) and on the watermaze (WM). We predicted that females should outperform males on the OLM task and that males should outperform females on the WM. To control for possible effects of housing environment, rats were housed in either complex environments or in standard shoebox housing. Eighty Long-Evans rats (40 males and 40 females) were housed in either complex (Complex rats) or standard shoebox housing (Control rats). Results indicated that males had superior performance on the WM, whereas females outperformed males on the OLM task, regardless of housing environment. As these sex differences cannot be easily attributed to differences in cognitive style related to linguistic processing of environmental features or to selection pressures related to the hunting gathering evolutionary prehistory of humans, these data suggest that sex differences in spatial ability may be related to traits selected for by polygynous mating strategies.     

Differences in Acquisition, Not Retention, Largely Contribute to Sex Differences in Multitrial Word Recall Performance

Approximately 2,500 adults (ages 18-97) completed multiple study-test trials of a list of unrelated words. Consistent with past research, females outperformed males in the recall task. To assess whether sex differences in recall performance were attributable to differences in acquiring and/or retaining information, the data were analyzed at the individual item level to distinguish gains (i.e., items not recalled on Trial n that were recalled on Trial n+1) and losses (i.e., items recalled on Trial n that were not recalled on Trial n+1). Being a male, increased age, lower verbal episodic memory ability, and lower vocabulary ability were associated with smaller gains and greater losses. Even when controlling for the influence of other individual difference variables, being a male was still associated with fewer gains across the majority of trials. These results suggest that one factor contributing to sex differences in recall performance are differences in acquiring new items rather than differences in retaining information across trials.     

Progesterone at encoding predicts subsequent emotional memory

Significant sex differences in the well-documented relationship between stress hormones and memory have emerged in recent studies. The potentiating effects of glucocorticoids on memory vary across the menstrual cycle, suggesting a potential interaction between these stress hormones and endogenously cycling sex hormones. Here, we show that memory for emotional materials changes significantly in accordance with hormonal changes across the menstrual cycle, suggesting that ovarian sex hormones influence the modulation of emotional memories. Sixty healthy, naturally cycling women rated 120 images on arousal and valence. One week later they completed free recall and recognition memory tests. Their menstrual cycle phases were estimated by self-report and confirmed by salivary assay of 17β-estradiol and progesterone. Memory for emotional items only was significantly better in the high hormone (luteal) phase compared with the low hormone (follicular) phase on the free recall test; on both tests memory correlated positively with progesterone collected at the time of encoding. These findings suggest that emotional memory performance changes across the menstrual cycle, and that this change is in part mediated by endogenous progesterone cycling.     

Sex differences in maternal behaviors of immature rats: The role of emotionality

Immature rats are able to give maternal care to pups and may increase their inclusive fitness by helping newborn siblings. Immature males are generally reported to be more maternal than females. In this research we studied sex differences and the extent to which they may be due to a different emotional response to novelty. We studied maternal response in two groups of immature rats of both sexes: in the naive group, juveniles aged from 18 to 30 days were given one test and showed clear-cut sex differences. The experience group was submitted to repeated tests from 18 to 30 days of age, thus eliminating the effects of novelty: as a result, all differences between sexes disappeared. A second experiment was designed in 24-day-old females to differentiate the effects of repeated handling and exposure to the test situation from that of repeated exposure to pups; moreover, the effects of an anxiety-reducing drug (diazepam) were studied. Exposure to pups is particularly efficient in facilitating maternal response. Diazepam injection was also effective, but its control showed that the injection per se was responsible for the effect. In conclusion, our results stress the importance of response to novelty and suggest that sex differences in maternal behavior of immature rats may be modulated by different emotional responses by males and females. In fact, emotionality competes with, and may exert an inhibitory effect on, the expression of a vast array of behaviors. © 1994 Wiley-Liss, Inc.     

POSITIVE EMOTIONS ENHANCE RECALL OF PERIPHERAL DETAILS

Emotional arousal and negative affect enhance recall of central aspects of an event. However, the role of discrete emotions in selective memory processing is understudied. Undergraduates were asked to recall and rate autobiographical memories of eight emotional events. Details of each memory were rated as central or peripheral to the event. Significance of the event, vividness, reliving and other aspects of remembering were also rated for each event. Positive affect enhanced recall of peripheral details. Furthermore, the impairment of peripheral recall was greatest in memories of anger, not of fear. Reliving the experience at retrieval was negatively correlated with recall of peripheral details for some emotions (e.g., anger) but not others (e.g., fear), irrespective of similarities in affect and intensity. Within individuals, recall of peripheral details was correlated with less belief in the memory's accuracy and more likelihood to recall the memory from one's own eyes (i.e., a field perspective).     

Development of sex differences in spatial memory.

Males typically perform better than females on tests of spatial abilities. However, Silverman and Eals (1992) found that females can surpass males on certain tasks, in particular recall of object location. This study investigated the age at which females begin having greater recall in object location. Recall was tested with object arrays (sets of line drawings of common objects) using samples of 80 adults (M age = 21 yr.) and 139 children at 3 age groups. Adult data replicated earlier findings, indicating significantly greater recall by women. The samples of children at different ages--4 yr. (n = 43), 10-11 yr. (n = 53), and 15-16 yr. (n = 43)--did not show significant sex differences in this type of recall. The findings suggest that females may surpass males in this spatial ability as adults, apparently due to gradual improvements in spatial memory through childhood and adolescence.