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The relationship between acute stress and memory performance, with a particular focus on gender differences and the role of the frontal lobe. the effects of cortisol on memory and neurological responses, as well as the impact of stress on executive functions and initial memory encoding. It also touches upon the differences in stress responses between males and females.
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Winter 2010
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Thesis Signature (Approval) Page
We hereby certify that this thesis, submitted by Randy Denis, conforms to accepted standards and is fully adequate in scope and quality to fulfill the thesis completion for the Divisional Honors Thesis citation.
__________________ Randy Denis Student Researcher
Jaime L. Tartar, PhD Faculty Advisor for Divisional Honors Thesis
Thomas Fagan, PhD Director, Division of Social and Behavioral Sciences
Don Rosenblum, PhD Dean, Farquhar College of Arts & Sciences
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My deepest gratitude goes to my wonderful adviser, Dr. Jaime Tartar; you have transformed me into a meticulous researcher and provided me with a toolbox full of skills and experiences. Your positive energy, dedication, and enthusiasm throughout this project are commendable. This project has satisfied my inquisitive mind. I would also like to express my gratitude to Kara Faso for helping me during the initial data collection phase of this study. Additionally, I would like to acknowledge Dr. Aurelien Tartar for supplying me with ice, gloves, and a refrigerator to store the saliva samples. There have been many other invaluable resources, such as Dr. Weylin Sternglanz and Dr. Allan Schulman, who have dedicated time to guide me in the right direction. Special thanks to Dr. Jason Gershman for providing support with the data analysis and interpretation. I am forever indebted to the supportive staff from the Division of Social and Behavioral Sciences, especially Raquel Palacios for her help with the budget and ordering logistics. Lastly, all this would have been impossible without the support from my parents, my life partner Kenrick Raza, and the NSU community. I hope for this thesis to inspire all students, especially those from disadvantaged backgrounds, to be involved academically and never give up.
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Previous research on emotional arousal and memory performance has demonstrated that acute stressors work to enhance memory consolidation while chronic, or unremitting, stress usually results in a decrease in memory performance. Both of these alterations in memory performance are thought to be mediated by the stress hormones cortisol and norepinephrine.model of stress, natural stressors in humans is increasingly commonly used to investigate While the bulk of the research in this area typically involves a male rat the potential effects of a stress response on memory performance. However, since males (rats and humans) are most commonly used in stress research, it is currently unclear if there are gender differences in the influence of stress on memory performance. Moreover, the type of stressors used in human research includes both physical stressors(e.g. cold water immersion) and psychological stressors (e.g. public speaking in laboratory environment). Although physical and psychological stress is mediated through unique neurological and endocrine pathways, they are not typically differentiated from each other in the literature. This study sought to use an academic examination as ethologically-relevantpsychological stress on memory performance in both males and females. and natural stressor to investigate the influence of an To that end, acute this study tested a total of 56 participants (46 with complete data, 16 males and 30 females) in two sessions, the first took place three weeks prior to their examination and the second took place 15-minutes prior to their examination. As expected, compared to the baseline testing session, salivary cortisol levels significantly increased during theexamination testing session with a concomitant significant increase in short term memory and non-significant increase in long-term memory. Gender differences were found in the potential influence of stress on memory performance. These results show that for females, but not males, increases in cortisol are associated with decreased memory performance. For males, there was a non-significant trend for improved short- and long- term memory performance independent of cortisol levels during the examination sessioncompared to baseline testing session. Probable explanations and future directions are discussed.
cellular metabolism alters important organ systems directly linked to survival. For instance, these hormones increase cardiovascular activity, enlarge the pupils, expand lung capacity for respiration, and constrict blood vessels in the extremities. Such increase in cellular activity results from the power of epinephrine to increase cellular metabolism and promote the liver to release carbohydrates. As a result, an increase in energy allows for quick energy consumption which is directly linked to survival (Panter-Brick & Worthman, 1999). Without this fast response, the body would take minutes to mobilize enough resources to respond to the threat, and this would not be evolutionarily advantageous. Additionally, the body has another hormonal mechanism which prepares the body for an extended usage of resources (Sapolsky, 2004).
HPA Axis: Slow Response Stress can also activate a slower response which is mediated by the HPA axis. The HPA axis responds to stress by providing sufficient resources for prolonged periods. As the brain becomes aware of the stressor, as indicated by signals from the amygdala and higher cortex, the paraventricular nucleus of the hypothalamus begins to secrete higher quantities of corticotropin releasing hormone (CRH) (as reviewed in Greenberg, 2009). CRH secretion from the hypothalamus to the anterior pituitary gland results in a release of adrenocorticotropin hormone (ACTH) into the bloodstream. An increase in ACTH in the blood activates sensitive receptor cells in the adrenal cortex to produce larger quantities of cortisol and also stimulates the liver to increase gluconeogenesis (as reviewed by Friedman, Charney & Deutch, 1995; Greenberg, 2009). Cortisol can also produce various neurological and lymphatic responses, such as an initial increase in immune functioning and alterations to learning and memory, respectively (Tsigos &
Chrousos, 2002; Lupien et al., 2007). In addition, cortisol also works as a neurotransmitter by increasing glucose usage in the brain. This increase in metabolism provides a sense of alertness, vigilance, and mental sharpness.
Importantly, the HPA axis is a self-regulating system at all levels; the body mobilizes resources to counteract damaging effects associated with the chronic release of cortisol (Kolb & Whishaw, 2004). One component of the HPA axis negative-feedback regulation occurs when higher than normal levels of cortisol bind to the glucocorticoid receptors in the hippocampus. This induces the HPA axis to regulate towards homeostasis; for instance, areas such as the pituitary gland and hypothalamus will decrease cortisol output (De Kloet et al., 1998). However, if the HPA axis becomes dysregulated, it will continue to release cortisol and elevated levels of cortisol damage neurons in the hippocampus (Salposkly, 2004). For instance, various studies have noted memory impairments among people with Cushing‟s disease, which is associated with heightened cortisol levels, and as a consequence, decreased hippocampal functioning (Forget, Lacroix & Cohen, 2002).
Overall, cortisol provides and increases energy and mental activity for prolonged periods (Panter-Brick & Worthman, 1999). Even though a surge in glucose is theorized to help the body contends with stressors, chronic stress has been linked to various pathologies (Lupien et al, 2007). Pathologies associated with chronic stress include immune suppression, hippocampus shrinkage, cardiovascular disease, ulcerations in the intestinal walls and psychological depression (Toates, 1995; Friedman, Charney, Deutch, 1995; Sapolsky, 2004).
use psychological stressors such as the Trier Social Stress Test and naturalistic stressors (e.g. examinations or bereavement) (reviewed in Bondi and Picardi, 1999). In addition, some studies assess both norepinephrine and cortisol, while others only use one biochemical measurement. Furthermore, this body of research with human participants has employed a multitude of memory tasks, all which are dependent on particular brain regions. Overall, some studies have found acute stress to enhance memory performance while others have found a decrease in performance (reviewed in Porcelli et al., 2008). Of note to the present study, one study has revealed that a reduction in cortisol is linked with an enhancement of short-term memory in humans (Vedhara et al., 2000). During stressful periods, the locus coeruleus becomes activated and this result in the release of norepinephrine to the prefrontal cortex (reviewed in Qin et al., 2009). Changes in the LC-NE pathway impact an area of the brain associated with temporary memory storage, the prefrontal cortex (PFC), due to its sensitivity to norepinephrine. One theory suggests that the LC-NE system modules PFC-dependent working memory in a U- shaped relationship (reviewed in Qin et al., 2009). More importantly to the current study, an initial increase in norepinephrine during the examination week might be helpful for the short-term memory task. It is possible for norepinephrine and cortisol to be released during the examination period and produce various changes in pre-frontal activity simultaneously. For instance, Qin and colleagues (2009) found that psychological stress reduces working memory activity and this was correlated with a hypoactivity in the PFC. Overall, changes in the neurochemistry during the examination period could influence memory in both memory tasks.
Hippocampus Functioning In studies measuring the levels of concentration of cortisol in the brain, the hippocampus has been noted to have the highest concentration of mineralocorticoid and glucocorticoid cortisol receptors in comparison to other brain regions (as noted by Daimond & Kim, 2002). Such abundance of cortisol receptors in the hippocampus must be further investigated due to its significance in initial memory consolidation. For many decades, researchers have been using animal models to understand spatial navigation, a form of memory which involves navigating in the environment and it dependency on the hippocampus. For instance, Bear and colleagues (2001) have reported that rats with damage to their hippocampus have a decrease in performance when locating food in a radial arm maze. Others have noted that chronic stress negatively impacts performance on a spatial navigation task (Diamond et al., 2007). Based on these studies, investigators are beginning to untangle the impact of stress on memory formation through a variety of avenues.
From the area of clinical neurology, a famous neurological patient H.M. made researchers realize the importance of the hippocampus in memory processes. From this case study, which involved a man with complete removal of both temporal regions, Carlson (1999) summarizes the importance to the field of memory. Researchers found for long-term memories to not store in the hippocampus, short-term memory to be independent of the hippocampus, motor tasks to not dependent on the hippocampus functioning, and the importance of the hippocampus in memory consolidation. The case of H.M. has revealed that factual knowledge (explicit) is processed differently than motor
Cognitive Memory Model Psychologists interested in cognitions have created models which seek to describe and clarify the human memory system. For the most part, many agree that learning involves the process of acquiring information, while memory refers to the retrieval of memories. Learning has been extensively studied in both humans and other animals (Diamond et al., 2007). In cognitive psychology, the widely known Atkinson and Shiffrin‟s Control Process model explains memory processing as involving three stages: sensory memory, short-term memory, and long term memory (Kandel et al., 2000). According to this model, rehearsal of the material is required for the information to have permanent storage in the long-term memory system. Current molecular evidence supports the idea of neurological changes to only occur during the consolidation from short-term to long-term memories (Kandel, 2000). To begin with, this model describes sensory memory (SM) as a simple memory system which involves remembering information for about one-twentieth of a second. Increasing in complexity, short-term memory process (STM) holds unrehearsed material for roughly twenty seconds and seven plus or minus two items; short-term memory is theorized to provide a stage ground for more permanent storage. Furthermore, STM is typically confused with working memory; but, from the cognitive perspective, working memory uses previously known information and a visual- sketch pad in order to process incoming information and uses previous knowledge (Bear et al., 2001). Moreover, working memory integrates current information with previously stored material from the long-term memory system (as reviewed by Terry, 2003). In this study, participants are not retrieving information from the long-term memory. Hence, the memory task could best be described as short-term and dependent on frontal-lobe
processes. The most complex memory system is known as long-term memory (LTM). This concept describes our ability to hold unlimited amounts of information for longer periods of time and is known to require protein synthesis within the neurons (Stickgold & Walker, 2005). It is important to note that the Atkinson and Shiffrin model, also known as the three-stage processing , has various limitations such as the inability to account for the powerful effects of emotional memories (reviewed by Myers, 2007). For example, emotional memories do not require rehearsal and are more vivid than other personal events. Of note to the present study, many researchers have used distraction tasks, such as the Brown-Peterson distraction task, with the idea of interfering with the limited capacity of short-term memory (Fuchs & Melton, 1974). A variety of distraction tasks have been developed, for example, some researchers have participants count aloud back from a certain number while others have participants listen to music (reviewed by Meyers, 2007). Interrupting the limited short-term memory system prevents accurate recall. For the current long-term memory task, participants were exposed to the long term memory words initially in order to have a variety of tasks in-between the encoding and retrieval part. More specifically, the participants in this study had to complete a demographic questionnaire, provide salivary samples, participate in a short term memory task, and even had to complete a self-report stress scale between the encoding and retrieval. Rather than using a distraction task, participants had to follow directions and their attention was distracted with other procedures. Based on this paradigm of long-term memory, participants had to use some effort to encode memories into their long-term memory storage system.
Walter Cannon: Fight-or-Flight Response In the early twentieth century, Walter Cannon coined the term fight-or-flight to describe the involvement of the ANS when exposed to a potential stressor in the environment (Cannon, 1934). Cannon further theorized that emotions are experienced for the duration of the physiological response (reviewed in LeDoux, 1996). In other words, individuals experience fear due to the physiological response to the stressor, resulting in an increase of heart rate and heightened alertness. Seeking to explain this phenomenon, he developed the Cannon-Bard theory of emotion which purports the importance of the hypothalamus as the hub of neural-endocrine communication. His theory provided groundwork for later research to further understand the effects of various stressors on a wide variety of areas including memory performance, immune functioning, cardiovascular activity, diabetes regulation and psychosomatic disorders (Sapolsky, 2004).
Hans Selye: General Adaptation Syndrome Hans Selye was another pioneer in the area of stress research. His research began through serendipitous observations of the stress response in laboratory rats. While trying to understand the effect of „noxious agents‟ on the adrenal glands of these animals, he began to notice a wide variety of pathologies (Selye, 1978). From these observations, he later noted that compared to unstressed rats, stressed rats experienced a wider range of pathologies including adrenal hypertrophy, atrophy to various lymphatic systems, and a greater number of stomach ulcerations as a result from the release of a stress hormone (Selye, 1978). This resulted in Selye operationalizing stress as any demand which takes the body away from homeostasis. He later became widely known as the architect of the
general adaption syndrome (GAS) model (Selye, 1978). His theory was the first extended view of the stress response beyond the initial sympathetic system activation. From a medical perspective, he believed the stress-response to be an important process because it terminates in a depletion of resources, and causes mental and physical exhaustion. More specifically, the initial phase in the GAS involves an alarm response; this is similar to the fight-or-flight response as proposed by Cannon, which promotes a cellular mobilization of resources to overcome a potential threat. The second phase involves a consistent elevated usage of bodily resources; this biochemical process continuously provides energy to overcome the perceived challenge. After a prolonged exposure to the stressor, resources become limited and chronic stress results in physiological and emotional exhaustion (Selye, 1978).
Yerkes-Dodson Law: Arousal Levels and Performance Another relevant concept to the present research is the Yerkes-Dodson Law. For many decades, the law was incorrectly interpreted as an inverted „U-shaped‟ relationship between arousal levels and memory performance (as reviewed in Diamond et al., 2007). This confusion about the correct interpretation of the discrimination avoidance task studies carried by Yerkes and Dodson has recently been revisited. The incorrect interpretation states that memory performance improves with an increment in arousal, to an optimal arousal; after that point, performance begins to decrease. In reality, the previous statement only applies to difficult tasks. For easier tasks, individuals continue to improve as arousal level increases (as reviewed in Diamond et al., 2007). In general, only relatively difficult tasks are affected when arousal level continues to increase after the
stressor, and coping mechanism to affects the physiological stress response (Selye, 1978; Sapolsky, 2004). Thus, rather than analyzing groups, the purpose here is to understand individual differences because individual variability uniquely affect their respective physiological response.
Herman & Cullinan: Processive vs. Systemic Pathways
In addition, Herman and Cullinan (1997) have proposed the existence of two different forms of stressors, each with unique stress-activating pathways resulting in the activation of the HPA axis. More specifically, systemic (immediate threats) and processive (requiring higher cognitive processes) stressors have been shown to depend on different brain pathways. Processive stressors result from processes occurring in the prefrontal and limbic structures, such as the hippocampus and amygdala. In humans, processive stressors are noted for their usage of higher cognition, such as the anticipation of an upcoming evaluation. In contrast, systemic stressors mainly depend on neurological pathways leaving the hypothalamic PVN (Herman & Cullinan, 1997). This pathway is responsible for helping the organism survive an immediate biological threat, such as a lack of oxygen or a severe decrease in temperature. It has been noted that animals, with lesions to their limbic system, have a stress reaction while experiencing physiological stressors, such as a decrease in air supply, but not to systemic stressors, such as being introduced to a new environment (Herman & Cullins, 1997). In other words, the limbic system might only be involved with psychosocial stressors, such the pressure surrounding examinations, while the other responds to biological needs. Overall, rather than viewing the activation of the HPA axis as an uniform process for all forms of stressors, Herman
and Cullinan (1997) noted different structures and pathways to activate, and help regulate, an endocrine response.
Research on Psychological Stress: Examination Stress The research conducted by Herman and Cullinan has expanded an interest in both processive and systemic stressors. While some have been interested in using ways of activating the systemic pathway through the usage of the cold-press test (systemic), others have been investigating the effects of psychological (processive) stressors on the endocrine system (Pascualy et al., 1999). More specifically, contemporary researchers are using laboratory processive stressors, such as the Trier Social Stress Test, as well as real life stressors, such as bereavement and college examinations, to understand their respective effects on both the HPA and ANS response (Biondi & Picardi, 1999; Kelly et al., 2007). For instance, studies using examination as the stressor have mainly focused on hormonal activation, immune functioning, anxiety scores, sex hormone secretion, and even prefrontal-dependent executive functioning (Biondi & Picardi, 1999 & Oaten & Cheng, 2005).
In one study, researchers were interested in self-control regulation between non- examination and examination periods. The researchers sought to understand the effect of examination stress on frontal lobe-dependent executive functions. Participants were asked to complete inventories with the intent of measuring self-care habits, appointment adherence, emotional control, and take part of the Stroop test; then, a comparison was made between baseline (4 weeks prior the examination) and the academically stressful period. Results suggest a decrease in self-regulatory behaviors, in both laboratory and
