ArticleLiterature Review

Emotional tagging of memory formation - In the search for neural mechanisms

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Abstract

Memory-related areas, such as the hippocampus, should be able to sort out the more significant from the less relevant aspects of an experience in order to transform only the earlier into long-term memory. We have recently suggested the Emotional Tagging concept, according to which the activation of the amygdala in emotionally arousing events mark the experience as important and aids in enhancing synaptic plasticity in other brain regions. Here, we review evidence from both human and animal studies that lend support to the Emotional Tagging hypothesis and to the central role the amygdala may play in its formation. We further speculate on potential neural mechanisms that may underlie emotional tagging. Long-term memory formation is considered to involve lasting alterations in synaptic efficacy, known as synaptic plasticity. It has been suggested that two factors are crucial for obtaining a synapse-specific long-term plasticity: (a) the successful activation of a synapse-specific, protein synthesis-independent tag, and (b) the activation of synapse-non-specific protein synthesis. The activation of protein synthesis can then induce lasting plasticity only in those synapses marked by a tag. Interestingly and relevant to the Emotional Tagging hypothesis, it has been recently shown that the activation of the amygdala could transform transient into long-lasting plasticity. These recent findings seem to fit well with the Emotional Tagging hypothesis. It seems reasonable to assume that the activation of the amygdala triggers neuromodulatory systems, which in turn reduce the threshold for the activation of the synaptic tag, and by this facilitate the transformation of early- into late-phase memory.

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... 11 The hippocampus is involved in most neurodegenerative diseases; it seems to play a major role in the integration of motor responses associated with emotionally arousing events since it forms part of the emotional memory system. 12,13 Multiple studies in rats have shown that consumption of the cycad Dioon spinulosum, 14,15 or the intrahippocampal microinjection of one of its neurotoxic metabolites (methylazoxymethanol), induces motor alterations characterised by immobility and spinning in the forced swimming test. 15,16 Similarly, rats receiving treatment with cassava root juice (with a linamarin concentration of 0.30 mg/2 mL) also developed such motor alterations as poor motor coordination and lateral swimming, 17 which seemed to be associated, al least in part, with a decrease in the number of neurons in hippocampal area CA1. ...
... 14 Spinning has also been observed after dorsal hippocampus microinjections of neurotoxic cycad derivatives, such as methylazoxymethanol. 15,16 In our study, spinning during the swimming test was not linked to damage to the vestibular system: rats with vestibular damage display this type of behaviour not only in the forced swimming test but also in the locomotor activity test (they walk in circles), 12,35 but this behaviour was not observed in our sample. This indicates that behavioural alterations in the swimming test were linked to damage at a motor level rather than at the vestibular level. ...
Article
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Introduction Cassava, also known as yuca or manioc (Manihot esculenta Crantz), is a staple food in tropical and subtropical regions since it is an important source of carbohydrates. Nevertheless, it contains cyanogenic compounds including lotaustralin and linamarin, which have been shown by experimental models to affect brain structures such as the thalamus, the piriform cortex, the hippocampus, and others. These findings may explain the presence of such neurological diseases as konzo and tropical ataxic neuropathy. However, hippocampal involvement in the neurological alterations associated with the chemical compounds in cassava has yet to be explored. Method Male Wistar rats (3 months old), were assigned to 4 groups (n = 8 per group) as follows: a vehicle-control group (receiving injectable solution 1 μl) and three groups receiving linamarin (10, 15, and 20 mM). The substances were microinjected intrahippocampally (CA1) every 24 hours for 7 consecutive days, and their effects on locomotor activity, rotarod, and swim tests were assessed daily. Results Linamarin microinjected into the dorsal hippocampus produced hyperactivity and loss of motor coordination which became more evident as treatment time increased. In the swim test, rats treated with linamarin displayed lateral rotation beginning on the fourth day of microinjection. Conclusions Microinjection of linamarin into the dorsal hippocampus of the rat is associated with impaired motor coordination, suggesting that the dorsal hippocampus, among other brain structures, may be affected by the neurological changes associated with inappropriate consumption of cassava in humans.
... However, it is the connections between the hippocampus and the amygdala that are important for associating a specific stimulus with a particular context (Dunsmoor & Paz, 2015). It has been suggested that during an emotional experience the amygdala interprets the emotional value of the incoming information while attaching emotional significance to its different aspects (Richter-Levin & Akirav, 2003). This evaluation is then past to the hippocampus that forms a specific context for the events' episodic memory trace. ...
... The hippocampus mediates declarative memory functions and plays an important role in the integration of memory elements at the time of retrieval by assigning significance for events within space and time (Squire & Zola-Morgan, 1991). It has been suggested that during an emotional experience the amygdala interprets the emotional value of the incoming information while attaching emotional significance to its different aspects (Richter-Levin & Akirav, 2003). This evaluation is then past to the hippocampus that forms a specific context for the events' episodic memory. ...
Thesis
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Human reactions to trauma exposure are extremely diverse, with some individuals exhibiting only time-limited distress and others qualifying for posttraumatic stress disorder diagnosis (PTSD). Furthermore, whereas most PTSD patients mainly display fear-based symptoms, a minority of patients displays a co-morbid anhedonic phenotype. This diversity in the response to trauma suggests that PTSD is induced through distinctive dysfunctions in the mechanisms of stressful memory processing. The mediation of the formation and retrieval of memories, particularly emotional ones, is often attributed to the mutual activation of different limbic regions. In accordance, PTSD is often conceptualized in terms of excessive conditioned fear, mediated by the activation and connectivity of fear processing limbic regions, such as the amygdala, hippocampus and the medial prefrontal cortex (mPFC). In this dissertation I examine the microanatomical correlates of extreme stress reactions within the limbic system, using different combinations of behavioral and biochemical protocols to increase the translational power of a rat model of PTSD. Applying the “underwater trauma” protocol to generate a traumatizing experience, the narrative of that model is presented in sequential chapters which are thereafter joined to form a single storyline. This storyline demonstrates how the “underwater trauma” protocol can be modified to increase the translational power of the model and better represent the complex characteristics of the human psychopathology. Finally, it is demonstrated how a novel profiling approach can reveal the microanatomical correlates of abnormal trauma reactions when combined with immunohistochemical assessments for activation and activation of inhibition.
... Emotional-tagging hypothesis (Richter-Levin & Akirav 2003) Memories for emotional events are tagged, which allows for subsequent arousal to selectively enhance memory for preceding emotional events. ...
... How can inducing arousal enhance memory for preceding emotional items but not neutral items? Investigators proposed that emotional arousal "tags" synapses associated with representations of emotional items, making these synapses the selective target of protein synthesis-dependent long-term potentiation (Bergado et al. 2011;Richter-Levin & Akirav 2003;Segal & Cahill 2009;Tully & Bolshakov 2010). The emotional tagging hypothesis predicts that emotionally salient stimuli are remembered better than neutral stimuli because emotional tags allow those particular synapses to capture the plasticity-related proteins released with subsequent inductions of arousal. ...
Article
Full-text available
Mather and colleagues provide an impressive cross-level account of how arousal levels modulate behavior, and they support it with data ranging from receptor pharmacology to measures of cognitive function. Here we consider two related questions: (1) Why should the brain engage in different arousal levels? and (2) What are the predicted consequences of age-related changes in norepinephrine signaling for cognitive function?
... Emotional-tagging hypothesis (Richter-Levin & Akirav 2003) Memories for emotional events are tagged, which allows for subsequent arousal to selectively enhance memory for preceding emotional events. ...
... How can inducing arousal enhance memory for preceding emotional items but not neutral items? Investigators proposed that emotional arousal "tags" synapses associated with representations of emotional items, making these synapses the selective target of protein synthesis-dependent long-term potentiation (Bergado et al. 2011;Richter-Levin & Akirav 2003;Segal & Cahill 2009;Tully & Bolshakov 2010). The emotional tagging hypothesis predicts that emotionally salient stimuli are remembered better than neutral stimuli because emotional tags allow those particular synapses to capture the plasticity-related proteins released with subsequent inductions of arousal. ...
Article
The GANE (glutamate amplifies noradrenergic effects) model proposes that local glutamate–norepinephrine interactions enable “winner-take-more” effects in perception and memory under arousal. A diverse range of commentaries addressed both the nature of this “hotspot” feedback mechanism and its implications in a variety of psychological domains, inspiring exciting avenues for future research.
... Emotional-tagging hypothesis (Richter-Levin & Akirav 2003) Memories for emotional events are tagged, which allows for subsequent arousal to selectively enhance memory for preceding emotional events. ...
... How can inducing arousal enhance memory for preceding emotional items but not neutral items? Investigators proposed that emotional arousal "tags" synapses associated with representations of emotional items, making these synapses the selective target of protein synthesis-dependent long-term potentiation (Bergado et al. 2011;Richter-Levin & Akirav 2003;Segal & Cahill 2009;Tully & Bolshakov 2010). The emotional tagging hypothesis predicts that emotionally salient stimuli are remembered better than neutral stimuli because emotional tags allow those particular synapses to capture the plasticity-related proteins released with subsequent inductions of arousal. ...
Article
The GANE (glutamate amplifies noradrenergic effects) model described by Mather et al. offers a neurophysiological basis for the arousal mechanism which is essential for empirical aesthetics and Gestalt processing. More generally, the core principle of perception can be interpreted as a continuous processing of competing arousal states, yielding selective amplification and inhibition of percepts to deduce the meaning of a scene.
... The Effect of Arthrospira (Spirulina) maxima … 69 memories. This is known as emotional tagging [105]. Therefore, any disturbance in this will give rise to alterations in the formation of associations between spatial and behavioral stimuli, which are elementary in the learning and memory processes. ...
... Index 186 biodegradability, 6 bioenergy, 130, 150 biological activities, 9, 18, 94, 95, 100, 102, 106, 109, 110, 130, 165 biological activity, 7, 102 biological processes, 107 biologically active compounds, 105 biomass, vii, ix, 2, 3, 4, 11, 13, 14, 15, 19, 28, 29, 80, 93, 94, 95, 96, 97, 98, 99, 101, 102, 105, 107, 109, 110, 111, 112, 113, 114, 115, 117, 119, 121, 122, 127, 128, 145, 163 biomass growth, 102 biomedical applications, 4 biomolecules, vii, ix, 16, 94, 95, 96, 98, 117 biosynthesis, 20, 42, 104, 108 biotechnological applications, 40, 178 biotechnology, 33, 97, 122 blood circulation, 48 blood pressure, 12, 119, 145, 169 blood transfusion, 167 blood urea nitrogen, 143 blood vessels, 12 blood-brain barrier, 140 body composition, 168 body weight, 10, 116, 137, 144, 168 bone marrow, 142, 152 bone resorption, 163 brain, viii, x, 15, 46, 49, 51, 55, 66, 68, 70, 71, 73, 76, 78, 83, 84, 86, 91, 134 brain structure, viii, 46, 66, 78 Complimentary Contributor Copy Index 191 systolic blood pressure, 13,14 T temperature, 107,108,114,146,158,160 therapeutic benefits,3 therapeutic effect,28,135,145 therapeutic interventions,36 therapeutics,43,7,15,16,18,19,21,25,42,165 toxic effect,71 toxic substances,viii,46 toxicity,3,8,29,81,135,143,148,169 treatment,5,11,13,15,16,17,19,21,23,35,58,66,95,113,116,142,153,156,167,179 tumor,vii,2,3,5,10,15,106,139,141,165 tumor development,106 tumor growth,5,141 tumor necrosis factor,15,165 V viral infection,viii,2,3,160,169 viruses,viii,4,15,24,27,46,50,139 vitamin A,95,102,105,135,142,152 vitamin B1,138,163,178 vitamin E,138 vitamin K,50 vitamins,viii,ix,46,66,93,119,135,137,147,156,160,163 ...
Chapter
Microalgae usually called “Spirulina” in the literature and in commercial packages have been studied as potential sources of protein for food and feed supplementation. These microalgae are produced industrially worldwide, being recognized as GRAS (Generally Recognized as Safe) by the Food and Drug Administration (USA) and accepted by the European Union for human consumption. Apart from a high protein content and balanced amino acid composition, its biomass contains compounds with antioxidant, anti-inflammatory, anti-tumor, anti-viral and anti-microbial activities. Some of these compounds have been determined to boost the immune system and prevent diseases such as hyperglycemia, cancer, diabetes, hypertension, cardiovascular and respiratory disorders. It has also been suggested that the supplementation with Spirulina biomass and/or its extracts could help immune systems to fight different viral infections, including those by SARS-CoV2, the etiologic agent of COVID-19. This immunity boosting activity has been related to the presence of some polysaccharides, carotenoids, phycobiliproteins, fatty acids and biopeptides in the biomass. In this context, this chapter will address the boosting effect of the immune system by Spirulina exploring its antiviral activity and respective mechanisms. The applications of the biomass as a supplement and nutraceuticals production will be also address.
... The Effect of Arthrospira (Spirulina) maxima … 69 memories. This is known as emotional tagging [105]. Therefore, any disturbance in this will give rise to alterations in the formation of associations between spatial and behavioral stimuli, which are elementary in the learning and memory processes. ...
... Index 186 biodegradability, 6 bioenergy, 130, 150 biological activities, 9, 18, 94, 95, 100, 102, 106, 109, 110, 130, 165 biological activity, 7, 102 biological processes, 107 biologically active compounds, 105 biomass, vii, ix, 2, 3, 4, 11, 13, 14, 15, 19, 28, 29, 80, 93, 94, 95, 96, 97, 98, 99, 101, 102, 105, 107, 109, 110, 111, 112, 113, 114, 115, 117, 119, 121, 122, 127, 128, 145, 163 biomass growth, 102 biomedical applications, 4 biomolecules, vii, ix, 16, 94, 95, 96, 98, 117 biosynthesis, 20, 42, 104, 108 biotechnological applications, 40, 178 biotechnology, 33, 97, 122 blood circulation, 48 blood pressure, 12, 119, 145, 169 blood transfusion, 167 blood urea nitrogen, 143 blood vessels, 12 blood-brain barrier, 140 body composition, 168 body weight, 10, 116, 137, 144, 168 bone marrow, 142, 152 bone resorption, 163 brain, viii, x, 15, 46, 49, 51, 55, 66, 68, 70, 71, 73, 76, 78, 83, 84, 86, 91, 134 brain structure, viii, 46, 66, 78 Complimentary Contributor Copy Index 191 systolic blood pressure, 13,14 T temperature, 107,108,114,146,158,160 therapeutic benefits,3 therapeutic effect,28,135,145 therapeutic interventions,36 therapeutics,43,7,15,16,18,19,21,25,42,165 toxic effect,71 toxic substances,viii,46 toxicity,3,8,29,81,135,143,148,169 treatment,5,11,13,15,16,17,19,21,23,35,58,66,95,113,116,142,153,156,167,179 tumor,vii,2,3,5,10,15,106,139,141,165 tumor development,106 tumor growth,5,141 tumor necrosis factor,15,165 V viral infection,viii,2,3,160,169 viruses,viii,4,15,24,27,46,50,139 vitamin A,95,102,105,135,142,152 vitamin B1,138,163,178 vitamin E,138 vitamin K,50 vitamins,viii,ix,46,66,93,119,135,137,147,156,160,163 ...
... Emotional-tagging hypothesis (Richter-Levin & Akirav 2003) Memories for emotional events are tagged, which allows for subsequent arousal to selectively enhance memory for preceding emotional events. ...
... How can inducing arousal enhance memory for preceding emotional items but not neutral items? Investigators proposed that emotional arousal "tags" synapses associated with representations of emotional items, making these synapses the selective target of protein synthesis-dependent long-term potentiation (Bergado et al. 2011;Richter-Levin & Akirav 2003;Segal & Cahill 2009;Tully & Bolshakov 2010). The emotional tagging hypothesis predicts that emotionally salient stimuli are remembered better than neutral stimuli because emotional tags allow those particular synapses to capture the plasticity-related proteins released with subsequent inductions of arousal. ...
Article
The ascending fibers releasing norepinephrine and acetylcholine are highly active during wakefulness. In contrast, during rapid-eye-movement sleep, the neocortical tone is sustained mainly by acetylcholine. By comparing the different physiological features of the norepinephrine and acetylcholine systems in the light of the GANE (glutamate amplifies noradrenergic effects) model, we suggest how to interpret some functional differences between waking and rapid-eye-movement sleep.
... Emotional-tagging hypothesis (Richter-Levin & Akirav 2003) Memories for emotional events are tagged, which allows for subsequent arousal to selectively enhance memory for preceding emotional events. ...
... How can inducing arousal enhance memory for preceding emotional items but not neutral items? Investigators proposed that emotional arousal "tags" synapses associated with representations of emotional items, making these synapses the selective target of protein synthesis-dependent long-term potentiation (Bergado et al. 2011;Richter-Levin & Akirav 2003;Segal & Cahill 2009;Tully & Bolshakov 2010). The emotional tagging hypothesis predicts that emotionally salient stimuli are remembered better than neutral stimuli because emotional tags allow those particular synapses to capture the plasticity-related proteins released with subsequent inductions of arousal. ...
Article
In this commentary we focus on individual differences in proposed mechanisms underlying arousal-based enhancement of prioritized stimuli. We discuss the potential of genotyping studies for examining effects of noradrenergic processes on stimulus prioritization in humans and stress the importance of potential individual differences in the activity of specific receptor subtypes in hotspot processes proposed by the GANE model.
... Even with low-intensity high-frequency stimulation, various reinforcing factors are known to be able to induce and enhance latent and in all probability subthreshold (from the point of view of detecting signifi cant changes) modifications [Frey and Frey, 2008]. Emotionally signifi cant actions in vivo can be used as such factors [Richter-Levin and Akirav, 2003], for example transient stress [Ahmed et al., 2006;Kudryashova and Gulyaeva, 2016], an enriched environment [Duffy et al., 2001], a training procedure [Uzakov et al., 2005], presentation of food and aversive stimuli [Seidenbecher et al., 1997], novelty [Kemp and Manahan-Vaughan, 2004], and activation of the reticular formation [Bloch and Laroche, 1985] of the amygdala [Richter-Levin and Akirav, 2003] and medial septum [Frey et al., 2003]. The proposed neurochemical basis of this reinforcement is activation of certain modulatory systems. ...
... Even with low-intensity high-frequency stimulation, various reinforcing factors are known to be able to induce and enhance latent and in all probability subthreshold (from the point of view of detecting signifi cant changes) modifications [Frey and Frey, 2008]. Emotionally signifi cant actions in vivo can be used as such factors [Richter-Levin and Akirav, 2003], for example transient stress [Ahmed et al., 2006;Kudryashova and Gulyaeva, 2016], an enriched environment [Duffy et al., 2001], a training procedure [Uzakov et al., 2005], presentation of food and aversive stimuli [Seidenbecher et al., 1997], novelty [Kemp and Manahan-Vaughan, 2004], and activation of the reticular formation [Bloch and Laroche, 1985] of the amygdala [Richter-Levin and Akirav, 2003] and medial septum [Frey et al., 2003]. The proposed neurochemical basis of this reinforcement is activation of certain modulatory systems. ...
Article
Full-text available
The phenomenon of long-term potentiation (LTP) is used for studies of the effects of various factors on the long-term plasticity of synapses in health and disease. One of the most important problems for these experiments is selection of a suitable stimulation protocol for comparing individual and group characteristics. Experiments on living hippocampal slices from Wistar rats aged 1–1.5 months addressed the individual features of the induction and maintenance of LTP (tetanization at 100 Hz for 1 sec) depending on the initial magnitude of the overall response of CA1 neurons to the stimulation of Schaffer collaterals used for tetanization and testing. The statistical relationship between the intensity of the synaptic input at the moment of tetanization and the magnitude of the post-tetanic increase after induction of LTP was assessed. Early potentiation was found to depend on the parameters of the test stimulation but not the amplitude of the response to the stimulation used for tetanization; the two factors acted independently. On testing with variable intensities, weak (near-threshold) responses were potentiated significantly more strongly than near-maximal responses. The saturation effect was found to limit mainly early LTP and only indirectly influenced the remaining potentiation. When differences in the level of early potentiation were excluded, late LTP depended on the intensity of tetanization but not the parameters of the test stimulation. The optimum tetanization of Schaffer collaterals for maintenance of LTP was the level inducing overall postsynaptic neuron responses of 1–2 mV, both weak and excessively strong activation on induction having negative impact on the efficiency with which LTP was maintained. This pattern may be due to a low level of depolarization, including in conditions of quite intense activation, due to the involvement of inhibitory interneurons in the response. These data provide evidence that all the study factors need to be considered for adequate comparison of groups of animals exposed to various environmental factors, including stress factors, particularly when the input characteristics of the connections of interest change.
... Specifically, the release of norepinephrine in the BLA is assumed to elicit modulatory effects on previous encoding-related synaptic changes in adjacent structures of the MTL (particularly in the hippocampus). In this regard, the concept of "emotional tagging" (Bergado et al., 2011;Richter-Levin & Akirav, 2003) has been brought forward. This account assumes that secondary effects of amygdala activation (via catecholaminergic and | 20 cholinergic projections) may contribute to the release of plasticity-related proteins, which facilitate the maintenance of potentiated states in weakly tetanized synapses (early LTP elicited during encoding) and thus support progression into late phase LTP, enabling longlasting changes in synaptic efficacy (Clopath, 2012). ...
... Bergado et al., 2011;Richter-Levin & Akirav, 2003), enhancing effects of REM sleep may be limited to source features in spatiotemporal proximity of the respective emotional item (as in our study the screen location at which the pictures were presented). This could plausibly account for the absence of similar effects in other recent studies, such as the Lehman et al (2016) study, in which cuing emotional associations during REM sleep did not elicit any significant retention benefits in contrast to uncued associations. ...
... One account of emotional memory trade-offs proposes that processes that operating near the initial learning event can tag emotional aspects of an experience and set the stage for downstream sleep-based consolidation processes (Kim & Payne, 2020;Payne & Kensinger, 2018; also see, Richter-Levin & Akirav, 2003). This "tag and capture" mechanism has been proposed to explain how encoding and sleep-based consolidation processes interact to promote later stabilization of memories. ...
... The present results also provide support for theories of the selective consolidation of emotional information (Kim & Payne, 2020;Payne & Kensinger, 2018;Richter-Levin & Akirav, 2003). Specifically, excitatory stimulation (i.e., neuromodulation) of the dorsal mPFC during encoding may have affected subsequent memory performance by upregulating regions important for emotional memory encoding and retrieval, including the ventral mPFC, amygdala and hippocampus (Bennion et al., 2015;Kensinger & Corkin, 2004;Murty et al., 2010;. ...
Preprint
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Previous research points to an association between retrieval-related activity in the medial prefrontal cortex (mPFC) and preservation of emotional information compared to co-occurring neutral information following sleep. Although the role of the mPFC in emotional memory likely begins at encoding, little research has examined how mPFC activity during encoding interacts with consolidation processes to enhance emotional memory. This issue was addressed in the present study using transcranial magnetic stimulation in conjunction with an emotional memory paradigm. Healthy young adults encoded negative and neutral scenes while undergoing concurrent TMS with a modified short intermittent theta burst stimulation (sTBS) protocol. Participants received stimulation to either the mPFC or an active control site (motor cortex) during the encoding phase. Recognition memory for scene components (objects and backgrounds) was assessed after a short (30-minute) and a long delay (24-hour, including a night of sleep) to obtain measures of specific and gist-based memory processes. The results demonstrated that, relative to control stimulation, sTBS to the mPFC enhanced memory for negative objects on the long delay test (collapsed across specific and gist-based memory measures). mPFC stimulation had no discernable effect on memory for objects on the short delay test nor on the background images at either test. These results suggest that mPFC activity occurring during encoding interacts with consolidation processes to preferentially preserve negatively salient information. Significance Statement Understanding how emotional information is remembered over time is critical to understanding memory in the real world. The present study used noninvasive brain stimulation (repetitive transcranial magnetic stimulation, rTMS) to investigate the interplay between mPFC activity that occurs during memory encoding and its subsequent interactions with consolidation processes. rTMS delivered to the mPFC during encoding enhanced memory for negatively valenced pictures on a test following a 24-hr delay, with no such effect on a test occurring shortly after the encoding phase. These results are consistent with the hypothesis that emotional aspects of memories are differentially subjected to consolidation processes, and that the mPFC might contribute to this “tag-and-capture” mechanism during the initial formation of such memories.
... Moreover, long-term memory is enhanced also for neutral stimuli by increasing participants' arousal, either through the presentation of emotional pictures (Anderson et al., 2006a;Ventura-Bort et al., 2016) or through the administration of chemical compounds usually released during emotional arousal (Buchanan and Lovallo, 2001). The latter suggests the existence of an emotional tagging which is able to increase the salience of non-emotional stimuli (Richter-Levin and Akirav, 2003). ...
... This "ABC" begins with perception, increasing the perceptual capability for binding features (such as object location) when stimulus competition occurs. The advantage yielded by arousing stimuli is maintained in the working memory system, where emotionally tagged information dominates the competition for mental resources (Richter-Levin and Akirav, 2003;Mather and Sutherland, 2011;Lee et al., 2014;Dunsmoor et al., 2015;Hur et al., 2017;Schweizer et al., 2019). The advantage exerted by emotion in "competition" condition could explain the improving effect of the emotional content of stimuli on spatial working memory performance observed in Experiments 1B and 1C. ...
Article
Full-text available
Remembering places in which emotional events occur is essential for individual’s survival. However, the mechanisms through which emotions modulate information processing in working memory, especially in the visuo-spatial domain, is little understood and controversial. The present research was aimed at investigating the effect of incidentally learned emotional stimuli on visuo-spatial working memory (VSWM) performance by using a modified version of the object-location task. Eight black rectangles appeared simultaneously on a computer screen; this was immediately followed by the sequential presentation of eight pictures (selected from IAPS) superimposed onto each rectangle. Pictures were selected considering the two main dimensions of emotions: valence and arousal. Immediately after presentation, participants had to relocate the rectangles in the original position as accurately as possible. In the first experiment arousal and valence were manipulated either as between-subject (Experiment 1A) or as within-subject factors (Experiment 1B and 1C). Results showed that negative pictures enhanced memory for object location only when they were presented with neutral ones within the same encoding trial. This enhancing effect of emotion on memory for object location was replicated also with positive pictures. In Experiment 2 the arousal level of negative pictures was manipulated between-subjects (high vs. low) while maintaining valence as a within-subject factor (negative vs. neutral). Objects associated with negative pictures were better relocated, independently of arousal. In Experiment 3 the role of emotional valence was further ascertained by manipulating valence as a within-subject factor (neutral vs. negative in Experiment 3A; neutral vs. positive in Experiment 3B) and maintaining similar levels of arousal among pictures. A significant effect of valence on memory for location was observed in both experiments. Finally, in Experiment 4, when positive and negative pictures were encoded in the same trial, no significant effect of valence on memory for object location was observed. Taken together results suggest that emotions enhance spatial memory performance when neutral and emotional stimuli compete with one another for access into the working memory system. In this competitive mechanism, an interplay between valence and arousal seems to be at work.
... Recent accounts in the literature suggest that emotional associations are preferentially retained only when they entail features that are Bintrinsic^, thus, perceptually inherent to the stimulus (such as color or location), whereas the process of associative binding appears to be impaired for Bextrinsic^features (Chiu et al., 2013;Kensinger, 2009;Mather, 2007). Taking into account that REM sleep-related emotional memory processing may only occur as a sequel of arousal-induced changes in synaptic plasticity during initial encoding (Bergado et al., 2011;Richter-Levin & Akirav, 2003), enhancing effects of REM sleep may thus be limited to intrinsic source features that previously underwent emotion-facilitated perceptual integration. In support of this notion, recent findings by Bennion, Payne, and Kensinger (2017) establish a relationship between activation changes along the ventral visual stream during successful retrieval of emotionally associated material and preceding REM sleep duration. ...
Article
Full-text available
When an episode of emotional significance is encountered, it often results in the formation of a highly resistant memory representation that is easily retrieved for many succeeding years. Recent research shows that beyond generic consolidation processes, rapid eye movement (REM) sleep importantly contributes to this effect. However, the boundary conditions of consolidation processes during REM sleep, specifically whether these extend to source memory, have not been examined extensively. The current study tested the effects of putative consolidation processes emerging during REM sleep and slow wave sleep (SWS) on item and source memory of negative and neutral images, respectively. Results demonstrate superior emotional relative to neutral item memory retention after both late night REM sleep and early night SWS. Emotional source memory, on the other hand, exhibited an attenuated decline following late night REM sleep, whereas neutral source memory was selectively preserved across early night SWS. This pattern of results suggests a selective preservation of emotional source memory during REM sleep that is functionally dissociable from SWS-dependent reprocessing of neutral source memory. This was further substantiated by a neurophysiological dissociation: Postsleep emotional source memory was selectively correlated with frontal theta lateralization (REM sleep), whereas postsleep neutral item memory was correlated with SWS spindle power. As such, the present results contribute to a more comprehensive characterization of sleep-related consolidation mechanisms underlying emotional and neutral memory retention. Subsidiary analysis of emotional reactivity to previously encoded material revealed an enhancing rather than attenuating effect of late night REM sleep on emotional responses.
... Moreover, this effect was observed only in the shock-context pairing group. Actually, in order to form a contextual representation with relevant emotional content, the incoming stimuli that is transmitted to the DH demands support from the basolateral amygdala (BLA) (Richter-Levin and Akirav, 2003;Sparta et al., 2014). The BLA activation facilitates contextual aversive memory consolidation through hippocampal neuroplasticity potentiation (McIntyre et al., 2005;Huff et al., 2006). ...
Article
The main κ opioid receptors (κORs) subtypes already described (κ1ORs and κ2ORs) are expressed in brain regions involved in aversive memory consolidation, including the dorsal hippocampus (DH). However, the role of DH κORs in consolidation of aversive memories with varied intensity and specificity is still uncertain. The present study aimed to investigate this question using pharmacological agents in rats subjected to a weak, moderate or strong contextual aversive conditioning (CAC) protocol. Antagonizing DH κORs with nor-binaltorphimine (nor-BNI), immediately after, but not 6 h later, a moderate CAC leads to intensified freezing behavior in the re-exposure to the paired context. Thus, indicating that DH κORs have an inhibitory role in the consolidation of an aversive memory. Increased DH κORs expression 1 h and 3 h after the moderate CAC was also observed. This up-regulation was absent in animals only exposed to the context or to the shock, indicating that this phenomenon requires a shock-context pairing to occur. Intra-DH nor-BNI infusion induced no changes following a weak CAC, but it was able to potentiate the expression of freezing behavior in novel and unpaired context after a strong CAC, indicating that DH κORs also modulate the consolidation of a generalized memory. Moreover, infusing the κ2ORs agonist GR 89696, but not the κ1ORs agonist U-69593, into the DH reduced the conditioned freezing expression. Nor-BNI pretreatment in a sub-effective dose prevented the κ2ORs agonist effects. Altogether, the present findings provide convergent evidence that κORs activation negatively modulates contextual aversive memory consolidation in rat dorsal hippocampus.
... The hippocampus mediates declarative memory functions and plays an important role in the integration of memory elements at the time of retrieval by assigning significance for events within space and time (Squire and Zola-Morgan, 1991). It has been suggested that during an emotional experience the amygdala interprets the emotional value of the incoming information while attaching emotional significance to its different aspects (Richter-Levin and Akirav, 2003). This evaluation is then past to the hippocampus that forms a specific context for the events' episodic memory. ...
Conference Paper
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Mediation of the formation and recollection of memories, particularly emotional ones, can partially be attributed to the activation of the Amygdala, prefrontal cortex and the Hippocampus. Persistent re-experiencing is a core symptom in posttraumatic stress disorder (PTSD) which includes elements of recurrent and intrusive recollections. Such intrusive recollections are often triggered by reminder cues associated with the traumatic event. However, there are indications that often cues are not those stimuli that were directly part of the traumatic experience but rather, cues experienced immediately prior to the trauma. Therefore, the present study examined the impact of exposure to an odor or context (i.e. reminder cue) which immediately precedes a stressful experience (i.e. under water trauma) on the behavior and the neural circuitry of the adult rat. Rats were first exposed to a novel chamber or a novel odor and then to an underwater trauma. 25 days later rats were re-exposed to the chamber or the odor and then were tested in the Open Field and the Elevated Plus Maze tests. On the final day of the experiment rats were sacrificed 90 min following exposure to the reminder cue. The characterization of the neural circuitry underlying the retrieval of stressful memories was carried out by c-Fos immunohistochemistry. Initial findings indicate that a reminder cue that immediately precedes a stressful experience does initiate PTSD-like symptoms. We now examine brain maps of activation associated with these symptoms. Acknowledgements: This research was funded by a grant from the USA Department of Defense (DoD Award: 10071009) to GRL, and a grant of the Institute for the Study of Affective Neuroscience University of Haifa, which was endowed by the Hope for Depression Research Foundation.
... Another biologically adaptive way some memories will be given priority comes from their level of emotional content (Richter-Levin and Akirav 2003). In some experimental paradigms, sleep appears to play a role in this prioritization. ...
Chapter
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The human brain faces a fundamental information storage challenge—forming useful new memories while not over-writing important old ones. Memory consolidation, and the corresponding interplay between the hippocampus and neocortex, is a protracted process to adjudicate between these two competing factors. Converging evidence from behavioral, cellular, and systems neuroscience strongly implicates a special role for sleep in stabilizing new declarative memories. In this chapter, we review evidence that during sleep the reactivation of newly acquired neuronal traces has lasting implications for memory transformation and stabilization. We first summarize relevant theoretical issues in memory research and then outline the physiological properties of sleep that may allow for this reactivation. We consider many factors that affect spontaneous memory reactivation, and we highlight research showing that memories can be selectively targeted and modified using learning-related stimuli. Ultimately, the ability to rescue otherwise fleeting episodes from oblivion plays a vital role in human life. Research elucidating this ability will also be critical for understanding how memory breaks down in aging and disease.
... The evidence that the BLA modulates hippocampal synaptic plasticity, as well as memories of various kinds, suggests that sensory input determines the specific synapses targeted for plasticity and that BLA actions influence consolidation of functional changes at those synapses (McIntyre et al., 2005;McReynolds and McIntyre, 2012). This hypothesis shares some characteristics with the emotional tagging hypothesis described by Richter-Levin and Akirav (2003). Both attempt to explain why most memories are lost almost instantly, whereas emotionally arousing memories frequently persist. ...
Article
Memory consolidation involves the process by which newly acquired information becomes stored in a long-lasting fashion. Evidence acquired over the past several decades, especially from studies using post-training drug administration, indicates that emotional arousal during the consolidation period influences and enhances the strength of the memory and that multiple different chemical signaling systems participate in this process. The mechanisms underlying the emotional influences on memory involve the release of stress hormones and activation of the basolateral amygdala, which work together to modulate memory consolidation. Moreover, work suggests that this amygdala-based memory modulation occurs with numerous types of learning and involves interactions with many different brain regions to alter consolidation. Additionally, studies suggest that emotional arousal and amygdala activity in particular influence synaptic plasticity and associated proteins in downstream brain regions. This review considers the historical understanding for memory modulation and cellular consolidation processes and examines several research areas currently using this foundational knowledge to develop therapeutic treatments. © 2017 by The American Society for Pharmacology and Experimental Therapeutics.
... Thus, any alteration in the prefrontal cortical control over sub-cortical areas might affect the consolidation of a memory at the systems level, be it by direct or indirect (via the amygdala) modulation of hippocampal activity. In addition to its reciprocal connections with the hippocampus (Pikkarainen, Ronkko, Savander, Insausti, & Pitkanen, 1999;rev Petrovich, Canteras, & Swanson, 2001), the amygdala modulates the storage of hippocampus-dependent memories (e.g., McIntyre, McGaugh, & Williams, 2012;McIntyre, Power, Roozendaal, & McGaugh, 2003;McIntyre et al., 2005;Roozendaal, Nguyen, Power, & McGaugh, 1999) and affects synaptic plasticity and memory processes in relation to stress, emotional, or experimental stimulation (e.g., rev; Bergado, Lucas, & Richter-Levin, 2011;Fa et al., 2014;Richter-Levin & Akirav, 2003). Therefore, alteration of c-Fos expression in the amygdala after ReRh lesions might have contributed to alter the hippocampus-and/or mPFC-dependent systems-level consolidation. ...
Article
Lesions of the reuniens and rhomboid (ReRh) thalamic nuclei in rats do not alter spatial learning but shorten the period of memory persistence (Loureiro et al. 2012, J. Neurosci. 32, 9947). Such persistence requires a hippocampo-cortical (prefrontal) dialog leading to memory consolidation at the systems level. Evidence for reciprocal connections with the hippocampus and the medial prefrontal cortex (mPFC) makes the ReRh a potential hub for regulating hippocampo-cortical interactions. As environmental enrichment (EE) fosters recovery of declarative-like memory functions after diencephalic lesions (e.g., anterior thalamus), we studied the possibility of triggering recovery of systems-level consolidation in ReRh lesioned rats using a 40-day postsurgical EE. Remote memory was tested 25 days post-acquisition in a Morris water maze. The functional activity associated with retrieval was quantified using c-Fos imaging in the dorsal hippocampus, mPFC, intralaminar thalamic nuclei, and amygdala. EE enhanced remote memory in ReRh rats. Conversely, ReRh rats housed in standard conditions were impaired. C-Fos immunohistochemistry showed a higher recruitment of the mPFC in enriched vs. standard rats with ReRh lesions during retrieval. ReRh rats raised in standard conditions showed weaker c-Fos expression than their sham-operated counterparts. The reinstatement of memory capacity implicated an EE-triggered modification of functional connectivity: EE reduced a marked lesion-induced increase in baseline c-Fos expression in the amygdala. Thus, enriched housing conditions counteracted the negative impact of ReRh lesions on spatial memory persistence. These effects could be the EE-triggered consequence of an enhanced neuronal activation in the mPFC, along with an attenuation of a lesion-induced hyperactivity in the amygdala.
... In future work, I hope to explore two main directions: how players' emotional response to the game affects in-game learning, and how intelligent game features can address individual or demographic learning differences. Since emotional events are remembered more easily [6] and commercial video games focus more on emotional experiences than cognitive training games like Lumosity, provoking player emotion may increase learning effectiveness. I plan to test this hypothesis by adding emotional, character-driven ingame interactions to Homeworld Bound. ...
Conference Paper
This document gives an overview of my current research project investigating how children develop spatial reasoning skills through video game training. I describe the motivation and goals of the project and the progress made so far.
... According to the emotional tagging hypothesis (Richter-Levin & Akirav, 2003), the arousal caused by an emotional experience tags a salient event and promotes facilitation of its consolidation in memory. Faces with emotional expressions can elicit an emotional experience consistent with this hypothesis. ...
Article
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Face recognition occurs when a face is recognised despite changes between learning and test exposures. Yet there has been relatively little research on how variations in emotional expressions influence people’s ability to recognise these changes. We evaluated the ability to discriminate old and similar expressions of emotions (i.e. mnemonic discrimination) of the same face, as well as the discrimination ability between old and dissimilar (new) expressions of the same face, reflecting traditional discrimination. An emotional mnemonic discrimination task with morphed faces that were similar but not identical to the original face was used. Results showed greater mnemonic discrimination for learned neutral expressions that at test became slightly more fearful rather than happy. For traditional discrimination, there was greater accuracy for learned happy faces becoming fearful, rather than those changing from fearful-tohappy. These findings indicate that emotional expressions may have asymmetrical influences on mnemonic and traditional discrimination of the same face.
... There is substantial evidence that the amygdala modulates memory traces stored in other brain regions, particularly through the BLA's projections to the hippocampus (McGaugh, 2000;see Fig. 4). An influential theory, called "synaptic tagging and capture" (Frey and Morris, 1998), describes the amygdala as being able to "tag" or "mark" an arousing event as important to remember by strengthening the synaptic plasticity in the hippocampus (Richter-Levin and Akirav, 2003). More specifically, this molecular tag would allow the activated synapses to capture more newly synthesized proteins to ensure that early long-term potentiation (LTP) persists into late LTP, leading to long-lasting plasticity in the activated synapses. ...
Article
This chapter reviews some key aspects of the relationship between emotion and episodic memory, focusing on the cognitive and neural systems that underlie the relationship. We differentiate between effects of emotion on early and late long-term memory, review evidence for the selectivity of these effects, and discuss existing models that best account for them. We reflect on and evaluate current practices in emotional memory research.
... While it is clear that the sleeping brain preferentially processes emotional content, the question of how it mechanistically triggers such processing remains unknown. The concept of "emotional tagging" (Richter-Levin and Akirav, 2003) suggests that the encoding of arousing material activates neural mechanisms, likely involving the amygdala and other key memory regions, resulting in longterm plasticity in those synapses marked by the tag (Morris, 2006). Payne et al. have recently suggested that, working in concert with the arousal generated by the emotional stimuli themselves, elevations in arousal-related neuromodulators, including NE and cortisol, might help set tags at a synaptic level at the time of encoding. ...
Chapter
An extensive body of research demonstrates the rich relationship between sleep and memory. This chapter reviews evidence that sleep involves a highly active collection of brain states with unique properties that support the acquisition and consolidation of learned information. We discuss the impact of both nocturnal and daytime sleep, as well as the lack of sleep, on memory formation, focusing primarily on episodic memories. Beyond this, we consider the role of sleep in the transformation of memory, including the selective consolidation of elements of our experience that are most important to remember and the flexible recombination of that information, which better serves us in the future.
... Our results are consistent with previous studies showing that the amygdala is involved in gaze orientation and attention [27][28][29][30][31], including a study suggesting that the amygdala enhances attention to visual stimuli associated with rewarding or aversive experiences [32]. ...
Article
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Author summary The amygdala is known to control passive fear responses (e.g., freezing), but it is unclear if it also contributes to active behaviors. To reach certain goals, we (humans and animals) often need to go through fearful environments. We hypothesized that the amygdala contributes to such an active behavior and devised a new foraging task for macaque monkeys in which various emotional contexts changed across many environments. This “exciting” task provoked extremely fast learning and high-capacity memory of objects and environments, and thereby caused extremely fast goal-directed behaviors. We found that the goal-directed behavior was affected by the emotional context in two dimensions (dangerous–safe and rich–poor) separately from the object values. Then, many neurons in the amygdala responded to the environments before any object appeared and did so selectively, depending on the emotional context of the environment. The neuronal activity was tightly correlated with the reaction time of goal-directed behavior across the contexts: faster behavior in dangerous or rich context. These results suggest that the amygdala facilitates goal-directed behavior by focusing on emotional contexts. Such a function is also important for emotional–social behavior and its disorder, including averted eye gaze in autism.
... Information associated with negative emotions may be particularly advantaged in memory due to its potential relevance for survival. Arousal during encoding may "tag" negative representations for subsequent processing during sleep (Bennion, Payne, & Kensinger, 2015;Cunningham et al., 2014;Richter-Levin & Akirav, 2003). The emotional response, or reactivity, associated with memories may also be processed during sleep, particularly REM sleep (Genzel, Spoormaker, Konrad, & Dresler, 2015;Walker & van der Helm, 2009). ...
Article
Sleep benefits memory in young adults, and this effect may be particularly strong for representations associated with negative emotion. Many aspects of sleep important for memory consolidation change with aging, particularly by middle age, suggesting that sleep-related consolidation may be reduced. However, the influence of sleep on memory has rarely been investigated in a middle-aged population. In the current study, young and middle-aged adults viewed negative and neutral pictures and underwent a recognition test after sleep or wake. Subjective emotional reactivity was also measured. Compared to waking, sleep benefited memory in young adults. Performance did not differ between sleep and wake groups in middle-aged adults, and it matched the level of young adults who slept. The effect of sleep versus wake was not influenced by memory valence in either age group. These results suggest the relative influence of sleep compared to wake on memory declines with aging, specifically by middle age, and that this decline extends to negative memory.
... It is also consistent with recent findings related to stress. Like novelty-related memory enhancement, stress-related memory enhancement has been linked to processes akin to those hypothesised in tag-and-capture theory (Bergado et al., 2011;McIntyre et al., 2012;Richter-Levin & Akirav, 2003). For example, spatial recognition memory in rats was promoted from STM to LTM by acute stress after weak but not after strong training (Lopes da Cunha et al., 2019), and stressrelated increases of cortisol in humans only predicted memory for weakly learned neutral words, but not for strongly learned reward-predicting words (Quent et al., 2018;see Dunsmoor et al., 2015, for similar effects using Pavlovian fear conditioning). ...
Article
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The experience of novelty can enhance memory for information that occurs close in time, even if not directly related to the experience – a phenomenon called “behavioural tagging”. For example, an animal exposed to a novel spatial environment shows improved memory for other information presented previously. This has been linked to neurochemical modulations induced by novelty, which affect consolidation of memories for experiences that were encoded around the same time. Neurophysiological research in animals has shown that novelty benefits weakly-encoded but not strongly-encoded information. However, a benefit that is selective to weak memories seems difficult to reconcile with studies in humans that have reported that novelty improves recollection, but not familiarity. One possibility is that the novelty increases activity in hippocampus, which is also associated with processes that enable recollection. This is consistent with another prediction of behavioural tagging theory, namely that novelty only enhances consolidation of information that converges on the same neuronal population. However, no study has directly explored the relationship between encoding strength and retrieval quality (recollection versus familiarity). We examined the effects of exposure to a novel immersive virtual reality environment on memory for words presented immediately beforehand, under either deep or shallow encoding tasks, and by testing both recall memory immediately, and recognition memory with remember/know instructions the next day. However, Bayes Factors showed no evidence to support the behavioural tagging predictions: that novelty would improve memory, particularly for shallowly-encoded words, and this improvement would differentially affect familiarity versus recollection.
... 20,21 Although these neurological aspects of learning are known today, chemistry teaching practices still address mainly cognitive modes of learning. The affective component of learning, which plays a significant role in retention and recall, 22 as well as targeting multisensory pathways for processing information, are both often left unattended. ...
Article
Full-text available
Using three-dimensional models in chemistry is a common teaching practice aimed at elevating the level of understanding of abstract concepts. However, the experience of using chemical models is still quite passive in terms of students’ input, requiring the students to utilize mainly visual, auditory, and some tactile information processing pathways. We present here a sequence of four short activities, which together constitute a change in the traditional teaching practice regarding molecular geometry. The goal is to offer a more active approach to working with models, one that involves multiple content processing pathways and exposes the learner to varied modes of learning. This set of activities was developed in line with the neuropedagogical literature while keeping in mind the brain mechanisms expected to affect learning and memory consolidation. We kept the activities simple so that implementation requires only minor adjustments to the routine practice, thus making this neuropedagogical approach accessible to chemistry teachers. A positive contribution of this kind of approach was evident from the scores of 10th grade chemistry students during consequent pilots.
... These findings have led to the viewpoint that the amygdala's predominant role may be the detection of and response to motivationally important stimuli [101]. In addition, it was proposed that the amygdala was responsible for forming an "affective tag" to the salient stimuli [102]. Therefore, the amygdala activations that we found in current meta-analysis are likely to reflect the salience and emotional impacts of high-calorie food cues. ...
Article
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Overconsumption of high-calorie or unhealthy foods commonly leads to weight gain. Understanding people’s neural responses to high-calorie food cues might help to develop better interventions for preventing or reducing overeating and weight gain. In this review, we conducted a coordinate-based meta-analysis of functional magnetic resonance imaging studies of viewing high-calorie food cues in both normal-weight people and people with obesity. Electronic databases were searched for relevant articles, retrieving 59 eligible studies containing 2410 unique participants. The results of an activation likelihood estimation indicate large clusters in a range of structures, including the orbitofrontal cortex (OFC), amygdala, insula/frontal operculum, culmen, as well as the middle occipital gyrus, lingual gyrus, and fusiform gyrus. Conjunction analysis suggested that both normal-weight people and people with obesity activated OFC, supporting that the two groups share common neural substrates of reward processing when viewing high-calorie food cues. The contrast analyses did not show significant activations when comparing obesity with normal-weight. Together, these results provide new important evidence for the neural mechanism underlying high-calorie food cues processing, and new insights into common and distinct brain activations of viewing high-calorie food cues between people with obesity and normal-weight people.
... It is also consistent with recent findings related to stress. Like novelty-related memory enhancement, stress-related memory enhancement have been linked to processes akin to those hypothesized in tagand-capture theory (Bergado et al., 2011;McIntyre et al., 2012;Richter-Levin & Akirav, 2003). For example, spatial recognition memory in rats was promoted from STM to LTM by acute stress after weak but not after strong training (Lopes da Cunha et al., 2019), and stress-related increases of cortisol in humans only predicted memory for weakly-learned neutral words, but not for strongly-learned reward-predicting words (Quent, McCullough, Sazma, Wolf, & Yonelinas, 2018;see Dunsmoor, Murty, Davachi, & Phelps, 2015, for similar effects using Pavlovian fear conditioning). ...
Thesis
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The Predictive Interactive Multiple Memory Systems (PIMMS) framework has been used to explain how novelty, or more precisely “prediction error”, boosts memory encoding. In this thesis, I explored several other phenomena in the animal and human literature that PIMMS cannot yet explain but should. PIMMS predicts that unexpected information will be better encoded than expected information. However recent work has suggested that expected information can also be better remembered than less expected information. By using a range of expectancies for the location of objects with an immersive virtual reality (iVR) kitchen, I showed that memory is a “U-shaped” function of expectancy, with best memory for highly expected or highly unexpected locations relative to intermediate levels of expectancy. Using OSF-registered Bayesian inference, this U-shape was consistent across four experiments. While the advantage for highly unexpected locations is consistent with PIMMS, the advantage for highly expected locations is not. Importantly, the advantage for expected locations was not simply due to a guessing bias when the location was forgotten, suggesting that the advantage arises during encoding rather than just at retrieval. This U-shape is consistent with another framework - the SLIMM framework - which proposes that different brain regions support the two ends of the U-shape, such that the advantage for unexpected information should be associated with recollection of contextual information via a medial temporal lobe system (like in PIMMS), while the advantage for expected information should be associated with a feeling of familiarity based on rapid cortical consolidation enabled by a medial prefrontal cortex system. However, when I asked participants to indicate recollection or familiarity at retrieval, both ends of the U-shape continuum were associated with higher recollection, while there was no detectable effect of expectancy on familiarity. I consider why this SLIMM prediction may therefore be incorrect. Another finding in the literature concerns the effect of novelty on unrelated information shortly preceding or succeeding the novel experience. PIMMS says nothing about this penumbra effect, which has been related to plasticity-related proteins triggered by the novel experience (so-called “behavioural tagging”). Since participants report that their first iVR experience is highly novel, I submitted a Registered Report to test whether iVR affected memory for unrelated words that were encountered prior to entering the iVR room. In short, the finding was that there is no evidence that novelty improves memory performance for information learned before experiencing something novel. Possible reasons for the failure of finding an effect were discussed. A final limitation of PIMMS I considered was the effect of “boundaries” in continuous stimuli, which are known to affect memory for the temporal order of information. While boundaries might be generated by prediction errors, PIMMS is silent on how they affect temporal order memory. Using a movie featuring a series of rooms, I tested whether memory for the temporal order of objects encountered in those rooms is affected by doorways between rooms and/or by surprising/perceptual changes within a room. Unfortunately, I was unable to replicate a previous report where temporal order memory was worse for pairs of objects in different rooms (i.e., either side of a doorway) than objects in the same room, let alone either sides of a surprising/perceptual change within a room. Taken together, my findings and the literature demonstrate the multiple potential factors that determine how novelty affects memory encoding (and consolidation), which require a more comprehensive theoretical framework than currently available.
... However, building on an older literature on mood congruence and state dependence from the 1970s and 1980s, e. g., Weingartner et al. (1977), Isen et al. (1978), Blaney (1986), modern neurological foundations of mood and memory show that emotionally arousing events are remembered better. A key role is assigned to the amygdala, one of the oldest parts of our brain, which is also called the limbic brain (Dolan 2002;Richter-Levin and Akirav 2003;LaBar and Cabeza 2006). Since the emotional arousal created by stimuli are processed in the amygdala and affect memory, the amygdala and at least the hippocampus, if not other parts of the brain, appear to interact. ...
Article
Personal experiences of economic outcomes, from global financial crises to individual-level job losses, can shape individual beliefs, risk attitudes, and choices for years to come. A growing literature on experience effects shows that individuals act as if past outcomes that they experienced were overly likely to occur again, even if they are fully informed about the actual likelihood. This reaction to past experiences is long-lasting though it decays over time as individuals accumulate new experiences. Modern brain science helps understand these processes. Evidence on neural plasticity reveals that personal experiences and learning alter the strength of neural connections and fine-tune the brain structure to those past experiences (“use-dependent brain”). I show that experience effects help understand belief formation and decision-making in a wide range of economic applications, including inflation, home purchases, mortgage choices, and consumption expenditures. I argue that experience-based learning is broadly applicable to economic decision-making and discuss topics for future research in education, health, race, and gender economics.
... Thus, the emotionally charged experience of slipping may have increased the activation of one or more of these regions during adaptation and led to strengthening of synaptic connections in relevant sensorimotor areas where memory of the learned mapping was marked for consolidation. This idea resembles the emotional tagging hypothesis (McReynolds and McIntyre 2012;Richter-Levin and Akirav 2003), which attempts to explain how and why emotionally arousing events are better remembered. ...
Preprint
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Actions have consequences. Motor learning involves correcting actions that lead to movement errors and remembering these actions for future behavior. In most laboratory situations, movement errors have no physical consequences and simply indicate the progress of learning. Here we asked how experiencing a physical consequence when making a movement error affects motor learning. Two groups of participants adapted to a new, prism-induced mapping between visual input and motor output while performing a precision walking task. Importantly, one group experienced an unexpected slip perturbation when making foot-placement errors during adaptation. Because of our innate drive for safety, and the fact that balance is fundamental to movement, we hypothesized that this experience would enhance motor memory. Learning generalized to different walking tasks to a greater extent in the group who experienced the adverse physical consequence. This group also showed faster relearning one week later despite exposure to a competing mapping during initial learning—evidence of greater memory consolidation. The group differences in generalization and consolidation occurred even though they both experienced similar magnitude foot-placement errors and adapted at similar rates. Our results suggest the brain considers the potential physical consequences of movement error when learning and that balance-threatening consequences serve to enhance this process.
... More specifically, when an emotional event occurs, there is an increased release of adrenal stress hormones that increase activity in the amygdala (McGaugh, 2004). The amygdala then increases the likelihood of consolidating the emotional memories by strengthening the activated synapses in the hippocampus (synaptic tagging and capture; Frey & Morris, 1998;Richter-Levin & Akirav, 2003). This ensures that early long-term potentiation (LTP) at the synapses persists into late LTP, leading to long-lasting memories. ...
Thesis
Emotional experiences are more likely to be remembered than more neutral, mundane ones. In young adults, negative information may be particularly memorable. Yet, an interesting change seems to happen in aging: As adults grow older, they may start remembering positive information more often than negative information. This positive memory bias in aging is commonly reported and is often explained in terms of changing time perspectives and motivation across the lifespan (i.e., Socioemotional Selectivity Theory). However, few studies have considered the basic interactions between memory and emotion that could influence this positivity bias. In this thesis, I examine whether certain factors partially independent of aging (i.e., semantic relatedness and distinctiveness, Study 1; mood, Studies 2-4), might influence the presence and magnitude of the positivity bias in memory. In Study 1, I explore the cognitive mechanisms required to produce the positivity bias and apply what is learned in this paper to investigate, in Studies 2-4, whether differences in mood could explain why the positivity bias occurs. In all studies, memory is measured using immediate free recall of positive, negative, and neutral pictures. In Study 1, I manipulate item interrelatedness (i.e., the extent of relatedness among pictures of a same category) and relative distinctiveness (i.e., the processing of a picture category at the same time as or in isolation from the others) to show that older adults’ emotional memory can be entirely explained by these two factors. The distinctive processing of positive pictures relative to other pictures is necessary for producing a positivity bias in older adults, which completely disappears when the distinctive processing of positive pictures is removed. Therefore, in subsequent studies I encourage the distinctive processing of items to increase the likelihood of observing a positivity bias and its possible interaction with mood. In Study 2, I test whether differences in mood predict differences in emotional memory bias in young and older adults using a video mood induction technique validated in a separate pilot study. In Studies 3 and 4, I further test the effect of mood on the positivity bias beyond any age-specific factors, by examining young adults only. This serves to reduce the likelihood of confounds that might exist between age groups (i.e., related to neurocognitive changes or decline), in order to study the true effects of mood on the positivity bias. In Study 3, I use a written priming task to experimentally manipulate mood and time perspective in young adults. In Study 4, I compare differences in naturally occurring moods and emotional memory in two separate young adult samples: university students and non-students. The experimental mood manipulations have minimal influence on the presence of a negativity bias in young adults (Studies 2 and 3), and influence to a small extent the memory advantage of positive over neutral material in older adults (Study 2). Non-student young adults show a similar preferential memory for positive material that is different from what is observed in university students, but this is not easily attributed to differences in mood (Study 4). In light of these results, I argue that the positivity effect in aging memory reflects a temporary contextual advantage for positive information that is not permanent or irreversible. Rather, it seems to depend in varying degrees on the context of study (i.e., relatedness and distinctiveness), mood, and the young-adult reference group. This has implications for how future research defines and studies the positivity effect in aging.
... Emotional triggers are expected to support learning and aid long-term memory. 38 Given the strong active learning nature of the AI approach in relation to traditional modes of learning chemistry, we realized that modifying the course to match online learning should result from a carefully thought-out process that would provide active online teaching. In the next section, we present the adaptation process we used for this course. ...
Article
Full-text available
Owing to the COVID-19 pandemic, all teachers’ training courses scheduled for summer 2020 had to transition to online formats. For the arts-integrating course “Teaching Chemistry by a Creative Approach”, this shift jeopardized the course’s essence, since learning by this approach is based on creative, hands-on, and active learning. Here we describe how the course format and contents evolved from a planned face-to-face format to an adapted, successful online learning experience. Two main goals were considered during the adaptation process: (1) making available to teachers the theoretical and practical backgrounds necessary to internalize the arts-integrating approach through creative, active learning strategies, and (2) providing teachers with actual tools through which they can rethink and develop their own teaching materials to suit remote teaching by incorporating supporting neuropedagogical aspects. Evaluating the immediate and follow-up questionnaires, as well as the assessment of teachers’ course assignments, suggests that the online course successfully preserved the essence and the main objectives of the original course, that the course was useful for remote teaching, and that it seems to have had an impact on teachers’ practices. We attribute this impact to the well-thought-out process of adapting the course to promote creative, active online teaching and learning. In addition to modifying the course’s format, this process expanded the arts-integrating approach to acknowledge the inherent difficulties in learning chemistry, existing also while learning online. We propose this process as a model to be used by educators to rethink and adapt their own practices to improve distance chemistry teaching and learning.
... If so, cannabis may dampen the impact of stress-and drug-related cues in opiate-dependent patients, and facilitate fear extinction in PTSD patient populations. emotion, chemically mediated by the catecholamine neurotransmitters DA and NE, facilitate learning and memory formation (Christianson, 1992;McGaugh, 2000;Richter-Levin & Akirav, 2003). The complexity of these disorders is amplified by sexually divergent responses to stress (Figure 2). ...
Article
Emotional arousal is one of several factors that determines the strength of a memory and how efficiently it may be retrieved. The systems at play are multifaceted; on one hand, the dopaminergic mesocorticolimbic system evaluates the rewarding or reinforcing potential of a stimulus, while on the other, the noradrenergic stress response system evaluates the risk of threat, commanding attention, and engaging emotional and physical behavioral responses. Sex‐specific patterns in the anatomy and function of the arousal system suggest that sexually divergent therapeutic approaches may be advantageous for neurological disorders involving arousal, learning, and memory. From the lens of the triple network model of psychopathology, we argue that post‐traumatic stress disorder and opiate substance use disorder arise from maladaptive learning responses that are perpetuated by hyperarousal of the salience network. We present evidence that catecholamine‐modulated learning and stress responsive circuitry exerts substantial influence over the salience network and its dysfunction in stress‐related psychiatric disorders, and between the sexes. We discuss the therapeutic potential of targeting the endogenous cannabinoid system; a ubiquitous neuromodulator that influences learning, memory, and responsivity to stress by influencing catecholamine, excitatory, and inhibitory synaptic transmission. Relevant preclinical data in male and female rodents are integrated with clinical data in men and women in an effort to understand how ideal treatment modalities between the sexes may be different.
... This effect depends on protein synthesis at the exposure time to the new stimulus [62]. Likewise, the "emotional marking" concept has been suggested by results of electrophysiological studies linking hippocampal plasticity with emotional arousal, amygdala activation and memory enhancement [63,64]. Synaptic plasticity in the hippocampus is related to long-term memory only if it is associated with amygdala activity. ...
Article
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A growing body of neurobiological and anatomic data continues to provide an increasingly detailed understanding of the role of amygdala in cognitive and motor control. We review evidence from past studies showing that the amygdala, which for many years was considered a black box, plays important roles in many neurobiological processes. The amygdala has key connections with the cortical areas, responsible for information processing that subserve emotion (fear, anxiety), learning, motor control, cognition, decision-making and social interaction. We conducted a review of current literature with 169 studies that met inclusion criteria to synthesize findings on amygdala and their influence on the neurobiological aspects. The findings demonstate converging evidence that the amygdala plays a pivotal role in motor, cognitive and emotional functions.
... One possible explanation for enhanced memory performance for arousing information is the concept of emotional tagging. Emotional tagging suggests that encoding of emotionally arousing information activates mechanisms governed by the amygdala and other key memory regions, which results in long term plasticity in those synapses marked by the tag (Morris, 2006;Richter-Levin & Akirav, 2003;Wang & Morris, 2010). One study suggested that elevated basal cortisol before learning, along with arousal imparted by negatively-valenced stimuli, may help to create these tags. ...
Article
Research has shown that remembering emotional information can occur at the expense of surrounding neutral background information; this emotional memory trade-off occurs similarly in both younger and older adults. We investigated how levels of cortisol, a hormone that acts on the central nervous system, impact emotional memory with age. Younger and older adult participants incidentally encoded emotional (positive, negative, or neutral) items placed on neutral backgrounds and later completed recognition tests for both the items and the backgrounds. Cortisol was measured at multiple time points to assess basal cortisol. Results are reported for prelearning levels, as findings were comparable across time points. Results revealed that higher levels of cortisol predicted a lower memory trade-off effect for older adults compared to younger adults and that this age difference in the role of cortisol tended to be strongest for memory for negative items (rather than for backgrounds or neutral items). No such interaction emerged for the positive trade-off effect. These results suggest that cortisol levels play a different role in supporting emotional memory across the life span, with lower levels of cortisol potentially more adaptive for memory for negative emotional information and higher levels indicating potential impairment with age. (PsycINFO Database Record (c) 2019 APA, all rights reserved).
Article
We investigated how affective states influence expository text comprehension and whether text valence moderates the effects (i.e., mood congruency). In Experiment 1 participants were randomly assigned to a happy or sad affective state (elicited via films) before reading a positive or negative version of a scientific text on animal adaptations. Participants (n = 79) in the sad (film) group had higher scores on deep-reasoning (d = .312) but not surface-level questions on a subsequent multiple-choice comprehension assessment; there was also no evidence for mood congruence. Using a neutral version of the same text, in Experiment 2 participants (n = 52) in a fearful condition performed better on surface-level comprehension questions (d = .594) compared with a sad condition, but the groups were on par for deep-reasoning questions. Experiment 3 (n = 595) did not replicate the findings from Experiment 2 (no comprehension differences between the sad and fear groups) and there were no differences between the fear and happy groups. However, the sad group outperformed the happy group on deep-reasoning questions (d = .210), thereby replicating Experiment 1. The overall findings were confirmed after pooling the data from the three experiments to increase power.
Article
The aim of the current study was to investigate the involvement of GABA neurotransmission in the CA1 region and endocannabinoid system in the basolateral amygdala (BLA) on morphine-induced memory impairment. We hypothesized that possible functional interaction between the GABAergic and cannabinoid systems in these brain regions would modulate morphine response in memory processing. Step-through type inhibitory avoidance paradigm was used for evaluating memory consolidation in adult male Wistar rats. Our results indicated that post-training systemic injection of morphine (3 and 5 mg/kg, i.p.) impaired memory retrieval. The microinjection of a GABA-A receptor agonist, muscimol (0.01-0.03 µg/rat) into the CA1 region increased the response of an ineffective dose of morphine (0.5 mg/kg, i.p.) and induced memory impairment, suggesting a synergistic interaction between morphine and muscimol. Interestingly, the activation of the BLA CB1 receptors by the microinjection of WIN55,212-2 (0.05-0.1 µg/rat) increased the effect of ineffective doses of muscimol (0.01 µg/rat; intra-CA1) and morphine (0.5 mg/kg, i.p.), inducing amnesia. The obtained results also showed that microinjection of AM251, a cannabinoid CB1 receptor antagonist, (1-2 μg/rat) into the BLA reversed the synergistic effect of muscimol and morphine, improving memory consolidation. It should be noted that the intra-CA1 microinjection of muscimol, intra-BLA microinjection of WIN55,212-2 or AM251 alone could not affect memory consolidation. Accordingly, it can be concluded that there may be a synergistic interaction between the CA1 GABAergic system and the BLA endocannabinoid neurotransmission with respect to the modulation of morphine-induced memory impairment.
Conference Paper
The concept of scientific paradox and the possibility to reveal and resolve these paradoxes by means of artificial intelligence are discussed. The cognitive architecture designed under the Natural-Constructive Approach for modeling the cognitive process is presented. This approach is aimed to interpret and reproduce the human-like cognitive features including uncertainty, individuality, intuitive and logical thinking, and the role of emotions in cognitive process. It is shown that this architecture involves, in particular, the high-level symbolic information that could be associated with concept of “science”. The scientific paradox is treated as impossibility to merge different representations of the same object. It is shown that these paradoxes could be resolved within the proposed architecture by decomposition of the high-level symbols into low-level of corresponding “images”, with subsequent revision of the object’s memorization procedure. This process should be accompanied by positive emotion manifestation (Eureka!).
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Cambridge Core - Cognition - The Cambridge Handbook of Cognitive Aging - edited by Ayanna K. Thomas
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This paper explores two ways that emotions can facilitate knowledge. First, emotions can play an evidential role with respect to belief formation. Second, emotions can be knowledge-conducive without being evidential by securing the safety of belief.
Article
International relations (IR) has witnessed an emerging interest in neuroscience, particularly for its relevance to a now widespread scholarship on emotions. Contributing to this scholarship, this paper draws on the subfields of affective neuroscience and neuropsychology, which remain largely unexplored in IR. Firstly, the paper draws on affective neuroscience in illuminating affect's defining role in consciousness and omnipresence in social behavior, challenging the continuing elision of emotions in mainstream approaches. Secondly, it applies theories of depth neuropsychology, which suggest a neural predisposition originating in the brain's higher cortical regions to attenuate emotional arousal and limit affective consciousness. This predisposition works to preserve individuals’ self-coherence, countering implicit assumptions about rationality and motivation within IR theory. Thirdly, it outlines three key implications for IR theory. It argues that affective neuroscience and neuropsychology offer a route toward deep theorizing of ontologies and motivations. It also leads to a reassessment of the social regulation of emotions, particularly as observed in institutions, including the state. It also suggests a productive engagement with constructivist and poststructuralist approaches by addressing the agency of the body in social relations. The paper concludes by sketching the potential for a therapeutically-attuned approach to IR.
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Previous research points to an association between retrieval-related activity in the medial prefrontal cortex (mPFC) and preservation of emotional information compared to co-occurring neutral information following sleep. Although the role of the mPFC in emotional memory likely begins at encoding, little research has examined how mPFC activity during encoding interacts with consolidation processes to enhance emotional memory. This issue was addressed in the present study using transcranial magnetic stimulation in conjunction with an emotional memory paradigm. Healthy young adults encoded negative and neutral scenes while undergoing concurrent TMS with a modified short intermittent theta burst stimulation (sTBS) protocol. Participants received stimulation to either the mPFC or an active control site (motor cortex) during the encoding phase. Recognition memory for scene components (objects and backgrounds) was assessed after a short (30-minute) and a long delay (24-hour, including a night of sleep) to obtain measures of specific and gist-based memory processes. The results demonstrated that, relative to control stimulation, sTBS to the mPFC enhanced memory for negative objects on the long delay test (collapsed across specific and gist-based memory measures). mPFC stimulation had no discernable effect on memory for objects on the short delay test nor on the background images at either test. These results suggest that mPFC activity occurring during encoding interacts with consolidation processes to preferentially preserve negatively salient information.SIGNIFICANCE STATEMENT:Understanding how emotional information is remembered over time is critical to understanding memory in the real world. The present study used noninvasive brain stimulation (repetitive transcranial magnetic stimulation, rTMS) to investigate the interplay between mPFC activity that occurs during memory encoding and its subsequent interactions with consolidation processes. rTMS delivered to the mPFC during encoding enhanced memory for negatively valenced pictures on a test following a 24-hr delay, with no such effect on a test occurring shortly after the encoding phase. These results are consistent with the hypothesis that emotional aspects of memories are differentially subjected to consolidation processes, and that the mPFC might contribute to this "tag-and-capture" mechanism during the initial formation of such memories.
Article
The basolateral complex of the amygdala (BLA) is capable of modulating memory and is thought to do so via projections to regions such as the hippocampus. The present study used optogenetic stimulation of glutamatergic projection neurons in the BLA as rats learned object-context associations during a well-studied hippocampus-dependent memory task. Relative to a control condition, optogenetic BLA stimulation resulted in the accelerated acquisition of when stimulation was delivered following correct choices but not when it was delivered during the intertrial interval. These results extend prior examples of amygdala-mediated memory enhancement to a canonical example of hippocampus-dependent memory and provide an opportunity for future dissection of amygdalar modulation of object-context associative memory. (PsycInfo Database Record (c) 2021 APA, all rights reserved).
Article
Emotional events are often remembered better than neutral events, a benefit that many studies have hypothesized to depend on the amygdala's interactions with memory systems. These studies have indicated that the amygdala can modulate memory-consolidation processes in other brain regions such as the hippocampus and perirhinal cortex. Indeed, rodent studies have demonstrated that direct activation of the amygdala can enhance memory consolidation even during nonemotional events. However, the premise that the amygdala causally enhances declarative memory has not been directly tested in humans. Here we tested whether brief electrical stimulation to the amygdala could enhance declarative memory for specific images of neutral objects without eliciting a subjective emotional response. Fourteen epilepsy patients undergoing monitoring of seizures via intracranial depth electrodes viewed a series of neutral object images, half of which were immediately followed by brief, low-amplitude electrical stimulation to the amygdala. Amygdala stimulation elicited no subjective emotional response but led to reliably improved memory compared with control images when patients were given a recognition-memory test the next day. Neuronal oscillations in the amygdala, hippocampus, and perirhinal cortex during this next-day memory test indicated that a neural correlate of the memory enhancement was increased theta and gamma oscillatory interactions between these regions, consistent with the idea that the amygdala prioritizes consolidation by engaging other memory regions. These results show that the amygdala can initiate endogenous memory prioritization processes in the absence of emotional input, addressing a fundamental question and opening a path to future therapies.
Article
Purpose: Moderate-intensity aerobic exercise (MAE) has been shown to elicit improvements in cognition and subsequent academic performance among preadolescents. Aerobic exercise has also shown to increase cortisol release in response to increasing exercise intensity. However, it is unknown if increased cortisol levels following exercise are related to acute improvements in executive function following a bout of MAE in preadolescents. The purpose of this study was to examine the potential effects of increased cortisol release after acute MAE on attention and working memory among preadolescents. Methods: Eleven preadolescents [6 males, 5 females] volunteered to participate in this study (age=9.45±1.03). Participants were randomized in a counterbalanced fashion to 30 minutes of rest or 30 minutes of treadmill MAE (60-70% HR max). Immediately pre-post each condition, participants completed a cognitive battery consisting of tests of attention (Flanker Test) and working memory (List Sorting Working Memory Test), as well as salivary samples for the analysis of cortisol. Linear Regression models were used to assess significance of covariates. Generalized linear models were used to assess significance of changes in each dependent variable against time, condition, time*condition and change in cortisol. Tukey’s HSD post-hoc tests for multiple comparisons were used to assess the effect of condition on working memory, attention, and salivary cortisol. Results: There was a significant effect of condition on working memory (F=3.16, p =0.04), with no change from pre-post rest (p=0.93) and improving from pre-post exercise (p=0.04). There was no effect of condition on attention or salivary cortisol, most likely due to a small sample size. Multiple linear regression models showed a significant effect of age (p=0.03) and change in cortisol (p=0.007) on working memory. Conclusion: Exercise had a positive effect on working memory, however, we were unable to relate this improvement to changes in salivary cortisol due to a lack of statistical power. This study could provide insight into the physiological effects of increased cortisol release on cognition, specifically in regard to working memory. However, more data are needed to achieve sufficient statistical power to detect these relationships.
Article
The outcomes of many business decisions do not live up to expectations or possibilities. A literature review of neuroscience and psychological factors that affect decision making has been undertaken, highlighting many reasons why it is hard for people to be good decision makers, particularly in complex and uncertain situations such as oil and gas projects. One way to diminish the impact of these human factors is to use the structured methodology and tools of Decision Analysis, which have been developed and used over 50 years, for making good decisions. Interviews with senior personnel from oil and gas operating companies, followed up by a larger-scale survey, were conducted to determine whether or how Decision Analysis and Decision Quality are used and why they are used in particular ways. The results showed that Decision Analysis and Decision Quality are not used as often as the participants think they should be; some 90% of respondents believed that they should be used for key project decisions, but only ~50% said that they are used. Six propositions were tested for why Decision Analysis and Decision Quality are not used more, and the following three were deemed to be supported: • Decision Analysis and Decision Quality are not well understood. • There is reliance on experience and judgment for decision-making. • Projects are schedule-driven. Further research is proposed to determine the underlying causes, and tackle those, with the aim being to improve business outcomes by determining how to influence decision makers to use Decision Analysis and Decision Quality more effectively.
Article
Stress is known to have a critical impact on memory processes. In the present work, we focus on the effects of an acute stress event closely associated to an unrelated learning task. Here we show that acute stress (elevated platform session, EP) experienced one hour after a weak spatial object recognition training (SOR), which only induces a short‐term memory (STM), promoted the formation of SOR‐long term memory (SOR‐LTM) in rats. The effect induced by stress was dependent on the activation of glucocorticoid‐ and mineralocorticoid‐receptors, brain‐derived neurotrophic factor (BDNF) and protein synthesis in the dorsal hippocampus. In contrast, EP after a strong SOR impaired SOR‐LTM probably by interfering with the use of necessary resources. Moreover, we show that the EP session before training induced anterograde interference, which it was not reversed by a subsequent exposure to an open field. Our findings provide novel insights into the impact of stress on LTM formation in rodents and they are discussed under the behavioral analogue of the synaptic tagging and capture hypothesis. This article is protected by copyright. All rights reserved.
Article
The power of episodic memories is that they bring a past moment into the present, providing opportunities for us to recall details of the experiences, reframe or update the memory, and use the retrieved information to guide our decisions. In these regards, negative and positive memories can be especially powerful: Life’s highs and lows are disproportionately represented in memory, and when they are retrieved, they often impact our current mood and thoughts and influence various forms of behavior. Research rooted in neuroscience and cognitive psychology has historically focused on memory for negative emotional content. Yet the study of autobiographical memories has highlighted the importance of positive emotional memories, and more recently, cognitive neuroscience methods have begun to clarify why positive memories may show powerful relations to mental wellbeing. Here, we review the models that have been proposed to explain why emotional memories are long-lasting (durable) and likely to be retrieved (accessible), describing how in overlapping—but distinctly separable—ways, positive and negative memories can be easier to retrieve, and more likely to influence behavior. We end by identifying potential implications of this literature for broader topics related to mental wellbeing, education, and workplace environments.
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In the present experiments, the modulatory influence of the basolateral amygdala on hippocampal-dependent memory processes was examined. Adult male Long-Evans rats were trained in a dally session in a win-shift radial maze task to obtain food from four randomly selected maze arms. After a delay period, they were returned to the maze with all the arms accessible and allowed to obtain four pellets from those arms that were not previously visited. Following criterion training with 5- and 15-min delay periods, the rats were given a drug test in which they received a posttraining intracerebral drug treatment immediately following the first four food- rewarded choices. In Experiment 1, the treatment consisted of an intrahippocampal or intra-amygdala injection (0.5 μl) of either a 2% solution of the local anesthetic lidocaine or saline. Four hours after injection, the rats were returned to the maze for a retention test. Posttraining intrahippocampal, but not intra-amygdala, injections of lidocaine impaired retention test choice accuracy. In Experiment 2, the rats unilaterally cannulated in two brain regions (the hippocampus and the basolateral amygdala) received posttraining intrahippocampal injections of glutamate or saline and concurrent intra-amygdala injections of lidocaine or saline. Intrahippocampal injection of glutamate (2.0 μg/0.5 μl) enhanced memory in the win-shift task when an 18-h delay was used. Concurrent posttraining intra-amygdala injections of lidocaine blocked the memory- enhancing effects of intrahippocampal glutamate administration. The findings suggest that, although a functional basolateral amygdala is not essential for normal memory in a hippocampal-dependent win-shift radial maze task, the basolateral amygdala is a necessary cofactor in the memory-enhancing effects of posttraining intrahippocampal injections of glutamate.
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'Consolidation' has been used to describe distinct but related processes. In considering the implications of our recent findings on the lability of reactivated fear memories, we view consolidation and reconsolidation in terms of molecular events taking place within neurons as opposed to interactions between brain regions. Our findings open up a new dimension in the study of memory consolidation. We argue that consolidation is not a one-time event, but instead is reiterated with subsequent activation of the memories.
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The authors examined whether perception of emotional stimuli is normal in amnesia and whether emotional arousal has the same enhancing effect on memory in amnesic patients as it has in healthy controls. Forty standardized color pictures were presented while participants rated each picture according to emotional intensity (arousal) and pleasantness (valence). An immediate free-recall test was given for the pictures, followed by a yes-no recognition test. Arousal and valence ratings were highly similar among the amnesic patients and controls. Emotional arousal (regardless of valence) enhanced both recall and recognition of the pictures, and this enhancement was proportional for amnesic patients and controls. Results suggest that emotional perception and the enhancing effect of emotional arousal on memory are intact in amnesia. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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These experiments examined the involvement of α1-adrenoceptors in the basolateral amygdala and their interaction with β-adrenoceptors in modulating memory storage. In Experiment 1, male Sprague–Dawley rats, implanted with bilateral cannulae in the basolateral amygdala, were trained in a one-trial inhibitory avoidance task and immediately after training, were given microinfusions (0.2 μl/side) of the selective α1-adrenoceptor antagonist, prazosin (0.1–1.0 μg). Retention was tested 48 h later. Prazosin induced a dose-dependent impairment in retention performance. In Experiment 2, animals received post-training intra-basolateral amygdala infusions of phenylephrine (a non-selective α-adrenoceptor agonist; 1.0–10.0 μg) alone or in combination with yohimbine (a selective α2-adrenoceptor antagonist; 0.2 μg) to examine the effects, on memory storage, of selective α1-adrenoceptor activation. Low doses of phenylephrine alone tended to impair retention performance, whereas the highest dose was non-effective. In contrast, phenylephrine infused together with yohimbine induced a dose-dependent enhancement of retention performance, suggesting that a selective activation of α1-adrenoceptors enhances memory formation. In Experiment 3, animals received intra-basolateral amygdala infusions of phenylephrine (1.0–10.0 μg) and yohimbine (0.2 μg) in combination with atenolol (a β1-adrenoceptor antagonist; 1.0 μg). Atenolol blocked the memory-enhancing effects induced by infusions of phenylephrine together with yohimbine. Considered together, these findings suggest that α1-adrenoceptors in the basolateral amygdala are implicated in mediating the effects of norepinephrine on memory storage and that their action depends on concurrent β-adrenoceptor activation.
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This article reviews recent studies of memory systems in humans and nonhuman primates. Three major conclusions from recent work are that (i) the capacity for nondeclarative (nonconscious) learning can now be studied in a broad array of tasks that assess classification learning, perceptuomotor skill learning, artificial grammar learning, and prototype abstraction; (ii) cortical areas adjacent to the hippocampal formation, including entorhinal, perirhinal, and parahippocampal cortices, are an essential part of the medial temporal lobe memory system that supports declarative (conscious) memory; and (iii) in humans, bilateral damage limited to the hippocampal formation is nevertheless sufficient to produce severe anterograde amnesia and temporally graded retrograde amnesia covering as much as 25 years.
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Electrophysiological studies have shown that single cells in the hippocampus respond during spatial learning and exploration1-4, some firing only when animals enter specific and restricted areas of a familiar environment. Deficits in spatial learning and memory are found after lesions of the hippocampus and its extrinsic fibre connections5,6 following damage to the medial septal nucleus which successfully disrupts the hippocampal theta rhythm7, and in senescent rats which also show a correlated reduction in synaptic enhancement on the perforant path input to the hippocampus8. We now report, using a novel behavioural procedure requiring search for a hidden goal, that, in addition to a spatial discrimination impairment, total hippocampal lesions also cause a profound and lasting placenavigational impairment that can be dissociated from correlated motor, motivational and reinforcement aspects of the procedure.
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Immediate post-training, stereotactically guided, intraparenchymal administration of pregnenolone sulfate (PS) into the amygdala, septum, mammillary bodies, or caudate nucleus and of PS, dehydroepiandrosterone sulfate, and corticosterone into the hippocampus was performed in mice that had been weakly trained in a foot-shock active avoidance paradigm. Intrahippocampal injection of PS resulted in memory enhancement (ME) at a lower dose than was found with dehydroepiandrosterone sulfate and corticosterone. Intraamygdally administered PS was approximately 10(4) times more potent on a molar basis in producing ME than when PS was injected into the hippocampus and approximately 10(5) times more potent than when injected into the septum or mammillary bodies. ME did not occur on injection of PS into the caudate nucleus over the range of doses tested in the other brain structures. The finding that fewer than 150 molecules of PS significantly enhanced post-training memory processes when injected into the amygdala establishes PS as the most potent memory enhancer yet reported and the amygdala as the most sensitive brain region for ME by any substance yet tested.
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The present study aimed at documenting the neurobiological substrate of taste-potentiated odor aversion (TPOA) in the rat. The role of several temporal lobe structures in discriminative TPOA learning was questioned. The effects of excitotoxic lesions (ibotenate) of the basolateral amygdaloid nucleus, the central amygdaloid nucleus, the caudate putamen nucleus, and aspirative lesion of the entorhinal cortex were studied. The results show that only basolateral amygdaloid nucleus (ABL) damage impaired TPOA. This effect was selective of TPOA, since it spared conditioned taste aversion (CTA) and olfactory perception. In order to find out which process in TPOA requires normal functioning of the ABL, the effects of microinjections of a GABAA agonist (muscimol) into the ABL at various stages of the experiment were examined. The results show that application of muscimol during the acquisition, before or after the presentation of the odor-taste stimulus, impaired TPOA without affecting CTA. Contrastingly, application of muscimol before the test impaired neither TPOA nor CTA. These results suggest that ABL is involved in the acquisition but not in the retrieval of TPOA. The efficacy of muscimol microinjected after the presentation of the odor-taste stimulus further suggests that the deficit is not due to a sensory impairment but rather to the disruption of a memory process, critical for TPOA.
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Research in humans and monkeys has demonstrated a system of anatomically related structures in the medial temporal lobe that is important for memory function. This system is comprised of the hippocampal region (i.e., the dentate gyrus, hippocampus proper and subicular complex) and the entorhinal, perirhinal, and parahippocampal cortices. While the hippocampal region has long been thought to be important in memory, there are few systematic studies in primates of the effects on memory of damage limited to the hippocampal region. We have used magnetic resonance imaging techniques, together with a stereotaxic approach, to produce bilateral lesions limited to the hippocampal region (the H lesion). Damage to the adjacent perirhinal, entorhinal, and parahippocampal cortex was minimal. Monkeys with the H lesion exhibited significant and long-lasting impairment on the delayed non-matching to sample task. At the same time, on this and other amnesia-sensitive tasks, monkeys with the H lesion performed better overall than monkeys with lesions of the hippocampal region that also included damage to the adjacent entorhinal and parahippocampal cortices (the H+ lesion). These findings show that, first, the hippocampal region itself is essential for normal memory function; and second, the adjacent entorhinal and parahippocampal cortices, either alone or in combination, are also an essential component of the medial temporal lobe memory system.
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Platelet-activating factor (PAF; 1-O-alkyl-2-acetyl-sn-glycero-3-phosphocholine), which is thought to be a retrograde messenger in long-term potentiation (LTP), enhances glutamate release and LTP through an action on presynaptic nerve endings. The PAF antagonist BN 52021 blocks CA1 LTP in hippocampal slices, and, when infused into rat dorsal hippocampus pre- or posttraining, blocks retention of inhibitory avoidance. Here we report that memory is affected by pre- or posttraining infusion of the PAF analog 1-O-hexadecyl-2-N-methylcarbamoyl-sn-glycerol-3-phosphocholine (mc-PAF) into either rat dorsal hippocampus, amygdala, or entorhinal cortex. Male Wistar rats were implanted bilaterally with cannulae in these brain regions. After recovery from surgery, the animals were trained in step-down inhibitory avoidance or in a spatial habituation task and tested for retention 24 h later. mc-PAF (1.0 microgram per side) enhanced retention test performance of the two tasks when infused into the hippocampus before training without altering training session performance. In addition, mc-PAF enhanced retention test performance of the avoidance task when infused into (i) the hippocampus 0 but not 60 min after training; (ii) the amygdala immediately after training; and (iii) the entorhinal cortex 100 but not 0 or 300 min after training. In confirmation of previous findings, BN 52021 (0.5 microgram per side) was found to be amnestic for the avoidance task when infused into the hippocampus or the amygdala immediately but not 30 or more minutes after training or into the entorhinal cortex 100 but not 0 or 300 min after training. These findings support the hypothesis that memory involves PAF-regulated events, possibly LTP, generated at the time of training in hippocampus and amygdala and 100 min later in the entorhinal cortex.
Article
Mitogen-activated protein kinase (MAPK) is an integral component of cellular signaling during mitogenesis and differentiation of mitotic cells. Recently MAPK activation in post-mitotic cells has been implicated in hippocampal long-term potentiation (LTP), a potential cellular mechanism of learning and memory. Here we investigate the involvement of MAPK in learning and memory in behaving animals. MAPK activation increased in the rat hippocampus after an associative learning task, contextual fear conditioning. Two other protein kinases known to be activated during hippocampal LTP, protein kinase C and α-calcium/calmodulin protein kinase II, also were activated in the hippocampus after learning. Inhibition of the specific upstream activator of MAPK, MAPK kinase (MEK), blocked fear conditioning. Thus, classical conditioning in mammals activates MAPK, which is necessary for consolidation of the resultant learning.
Article
Case studies of patients with bilateral amygdala damage and functional imaging studies of normal individuals have demonstrated that the amygdala plays a critical role in encoding emotionally arousing stimuli into long-term declarative memory. However, several issues remain poorly understood: the separate roles of left and right amygdala, the time course over which the amygdala participates in memory consolidation, and the type of knowledge structures it helps consolidate. We investigated these questions in eight subjects with unilateral amygdala damage, using several different measures. For comparison, our main task used stimuli identical to those used previously to investigate emotional declarative memory in patients with bilateral amygdala damage. Contrasts with both brain-damaged and normal control groups showed that subjects with left amygdala damage were impaired in their memory for emotional stimuli, despite entirely normal memory for neutral stimuli (because of a number of caveats, the findings from subjects with right amygdala damage were less clear). Follow-up experiments suggested that the normal facilitation of memory for emotional stimuli may develop over an extended time course (>30 min), consistent with prior findings, and that the specific impairment we report may depend in part on the lexical nature of the task used (written questionnaire). We stress the complex and temporally extended nature of memory consolidation and suggest that the amygdala may influence specific components of this process.
Article
Although the biochemical mechanisms underlying learning and memory have not yet been fully elucidated, mounting evidence suggests that activation of protein kinases and phosphorylation of their downstream effectors plays a major role. Recent findings in our laboratory have shown a requirement for the mitogen-activated protein kinase (MAPK) cascade in hippocampal synaptic plasticity. Therefore, we used an inhibitor of MAPK activation, SL327, to test the role of the MAPK cascade in hippocampus-dependent learning in mice. SL327, which crosses the blood-brain barrier, was administered intraperitoneally at several concentrations to animals prior to cue and contextual fear conditioning. Administration of SL327 completely blocked contextual fear conditioning and significantly attenuated cue learning when measured 24 hr after training. To determine whether MAPK activation is required for spatial learning, we administered SL327 to mice prior to training in the Morris water maze. Animals treated with SL327 exhibited significant attenuation of water maze learning; they took significantly longer to find a hidden platform compared with vehicle-treated controls and also failed to use a selective search strategy during subsequent probe trials in which the platform was removed. These impairments cannot be attributed to nonspecific effects of the drug during the training phase; no deficit was seen in the visible platform task, and injection of SL327 following training produced no effect on the performance of these mice in the hidden platform task. These findings indicate that the MAPK cascade is required for spatial and contextual learning in mice.
Article
Abstract Theoretical arguments and empirical data are presented in favor of the hypothesis that the hippocampal system supports a declarative memory capacity in animals as well as humans. This view is advanced by identifying two prominent characteristics of human declarative memory and by operationalizing and evaluating them using both experimental lesion and single unit recording studies on animals. First, hippocampal processing is not selective to any particular category of learning materials; instead, it supports comparisons among all kinds of information in memory, resulting in a representation of critical relations between items. Conversely, individual representations are supported outside the hippocampal system. Second, hippocampal-dependent, relational memory representations involve a flexible organization that permits inferences from memory in novel situations. Conversely, hippocampal-independent individual representations can support only repetition of procedures acquired during original learning. Correspondences between the neuropsychological and neurophysiological findings presented serve to indicate how these properties of hippocampal representation support declarative memory across behavioral paradigms and across species.
Article
Reports an error in the original article by L. R. Squire (Psychological Review, 1992[Apr], Vol 99[2], 195–231). The caption for Figure 7 was incorrect. The corrected caption is given. (The following abstract of this article originally appeared in record 1992-26428-001.) Considers the role of the hippocampus in memory function. A central thesis involving work with rats, monkeys, and humans (which has sometimes seemed to proceed independently in 3 separate literatures) is now largely in agreement about the function of the hippocampus and related structures. A biological perspective is presented that proposes multiple memory systems with different functions and distinct anatomical organizations. The hippocampus (together with anatomically related structures) is essential for a specific kind of memory, here termed declarative memory (similar terms include explicit and relational). Declarative memory is contrasted with a heterogeneous collection of nondeclarative (implicit) memory abilities that do not require the hippocampus (skills and habits, simple conditioning, and the phenomenon of priming). The hippocampus is needed temporarily to bind together distributed sites in the neocortex that together represent a whole memory. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Article
These experiments examined the involvement of the amygdaloid complex as a site of interaction of adrenergic and muscarinic cholinergic influences on memory storage. Male Sprague–Dawley rats (60 days old; 250–300 g) were given a single training trial in an inhibitory avoidance task and a retention test trial 48 h later. Immediately after training buffer control or drug solutions (0.5 μl) were infused into the amygdala and, in the first experiment only, other drugs were administered intraperitoneally (ip). The first experiment examined the effects of post-training systemic injections of the muscarinic agonist oxotremorine (100.0 μg/kg) administered alone or together with intraamygdala injections of either the muscarinic antagonist atropine (1.0 μg) or the β-noradrenergic antagonist propranolol (0.3 μg). Oxotremorine enhanced retention and atropine, but not propranolol, attenuated the effects of oxotremorine. In the second experiment intraamygdala infusions of the β-noradrenergic agonist clenbuterol (10.0 ng) were administered either alone or together with atropine (1.0 μg). Clenbuterol enhanced retention and atropine blocked the effects of clenbuterol. In the third experiment intraamygdala infusions of oxotremorine (3, 10, 30, or 100 ng) were administered either alone or together with propranolol (0.3 μg). Oxotremorine (3.0 and 10.0 ng) enhanced retention and propranolol did not block the effects of oxotremorine. These findings are consistent with the view that memory storage is regulated by an interaction of β-noradrenergic and cholinergic influences and suggest that the noradrenergic influences are mediated by the release of acetylcholine and activation of muscarinic cholinergic receptors within the amygdala.
Article
[ Howard Eichenbaum ][1] In this issue of Science , [ Vargha-Khadem et al .][2] report that three patients who had very specific loss of their hippocampi within the first few years of life showed a severe loss of episodic memory (our record of personal events), but that their semantic memory (our lifetime accumulation of universal factual knowledge) was intact. In his Perspective, Eichenbaum explains what these results mean for the classification of different types of memory and their correspondence with distinct regions of the brain. He outlines the emerging notion of the hippocampus as the area that facilitates associations of memories from different perceptual modalities (a face with a particular voice, for example). [1]: http://www.sciencemag.org#affiliation [2]: http://www.sciencemag.org/cgi/content/short/277/5324/376
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Substantial evidence from animal studies suggests that enhanced memory associated with emotional arousal results from an activation of beta-adrenergic stress hormone systems during and after an emotional experience. To examine this implication in human subjects, we investigated the effect of the beta-adrenergic receptor antagonist propranolol hydrochloride on long-term memory for an emotionally arousing short story, or a closely matched but more emotionally neutral story. We report here that propranolol significantly impaired memory of the emotionally arousing story but did not affect memory of the emotionally neutral story. The impairing effect of propranolol on memory of the emotional story was not due either to reduced emotional responsiveness or to nonspecific sedative or attentional effects. The results support the hypothesis that enhanced memory associated with emotional experiences involves activation of the beta-adrenergic system.
Article
35 male rats in 2 experiments were trained on several discrimination problems that should require a configural association solution: (1) 3 variations of the negative-patterning problem, A+, B+, AB–; (2) a conditional discrimination, AC+, B+, AB–, C–; and (3) an AC+, B+, AB– problem. These problems had similar or identical logical descriptions. Yet, results suggest that the subtle procedural differences between them influenced the processes that enabled the rats to withhold responding to the nonreinforced AB– compound. These results help to explain why damage to the hippocampal formation does not always impair performance on nonlinear discriminations. They do not, however, offer any support for R. J. Sutherland and J. W. Rudy's (see record 1989-38933-001) configural association system theory of how the hippocampal formation contributes to learning and memory. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Article
Discusses the role of the amygdaloid complex in conditioning of autonomic processes during emotional learning situations. Results from studies on animals and normal humans have implicated at the simplest, the activation of β-adrenergic receptors, and the amygdaloid complex in such learning. Recent experimental results with patients with brain-damage and Urbach-Weithe disease show selective impairment of memory for emotional material (e.g., L. Cahil, et al, 1995), have confirmed this hypothesis for conscious, long-term memory. However, these autonomic processes are not required for normal retention in non-emotionally arousing situations. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Article
the findings summarized in this chapter [suggest]: the amygdala may serve to modulate the storage of information at other brain sites / physiological systems activated by affective stimulation influence memory storage, at least in part, through effects mediated by the amygdala / viewed from this perspective, the amygdala may be part of a brain system that serves to ensure that memories of significant experiences are well retained the central hypothesis guiding the research summarized in this chapter is that memory storage is regulated by neuromodulatory systems activated by experiences role of endogenous systems in the modulation of memory storage / involvement of the amygdala in adrenergic influences on memory / involvement of the amygdala in the effects of opiate antagonists on memory / involvement of the amygdala in GABAergic influences on memory storage / interaction of neuromodulatory influences / effects of lesions affecting amygdala functioning / effects of NMDA [n-methyl-d-aspartic acid] antagonists / rats (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Article
Cell adhesion molecules (CAMs) of the immunoglobulin superfamily, NCAM and L1, as well as the post-translational addition of α-2,8-linked polysialic acid (PSA) homopolymers to NCAM (PSA–NCAM), have been implicated in the neural mechanisms underlying memory formation. Given that the degree of stress elicited by the training situation is one of the key factors that influence consolidation processes, this study questioned whether training rats under different stressor intensities (0.2, 0.4, or 1 mA shock intensity) in a contextual fear conditioning task might regulate subsequent expression of NCAM, PSA–NCAM and L1 in the hippocampus, as evaluated immediately after testing rats for conditioning at 12 and 24 h after training. Behavioural inhibition (evaluated as a ‘freezing’ index) at testing and post-testing plasma corticosterone levels were also assessed. The results showed that 12 h post-training, conditioned animals displayed reduced NCAM, but increased L1, expression. At this time point, the group trained at the highest shock intensity (1 mA) also presented decreased PSA–NCAM expression. Analyses performed 24 h post-training indicated that the 1 mA group exhibited increased NCAM and L1 expression, but decreased expression of PSA–NCAM levels. In addition, L1 values that presented a shock intensity-dependent U-shaped pattern were also increased in the group trained at the lowest shock condition (0.2 mA) and remained unchanged in the intermediate shock condition (0.4 mA). Freezing and corticosterone values at both testing times were positively related with shock intensity experienced at training. Therefore, our results show a complex regulation of CAMs of the immunoglobulin superfamily in the hippocampus that depends upon stressor intensity and time factors. In addition, the pattern of CAMs expression found in the 1 mA group (which is the one that shows higher post-training corticosterone levels and develops the stronger and longer-lasting levels of fear conditioning) supports the view that, after a first phase of synaptic de-adherence during consolidation, NCAM and L1 might participate in the stabilization of selected synapses underlying the establishment of long-term memory for contextual fear conditioning, and suggests that glucocorticoids might play a role in the observed regulation of CAMs.
Article
Male Sprague Dawley rats with stria terminalis (ST) or sham lesions were trained in an inhibitory avoidance task, injected immediately post-training with clenbuterol hydrochloride (0.03 mg/kg; IP), and tested for retention 48 h later. Clenbuterol enhanced retention of the sham-lesioned animals but did not affect retention of the ST-lesioned animals. Clenbuterol injected intra-amygdally immediately after training also enhanced retention of the inhibitory avoidance task. These results agree with other evidence suggesting the participation of-noradrenergic mechanisms in the amygdala in the modulation of memory storage.
Article
These experiments examined the effects of posttraining intraamygdala administration of the muscarinic agonist, oxotremorine, and the β-noradrenergic antagonist, propranolol, on memory for reduction in reward magnitude. Male Sprague–Dawley rats (175–200 g) implanted with bilateral intraamygdala cannulae were food deprived (maintained at 80% of body weight) and trained to run a straight alley (six trials/day) for either ten 45-mg food pellets (high reward) or one 45-mg food pellet (low reward) for 10 days. In Experiment One, the animals in the high-reward group were then shifted to a one-pellet reward and immediately given intraamygdala infusions (0.5 μl/side) of either oxotremorine (10 ng) or phosphate buffer. Shifted training continued for 4 more days and no further injections were given. Shifted animals given the buffer solution displayed an increase in runway latencies but returned to preshift latencies by the fifth day of shifted training. In contrast, animals given oxotremorine exhibited increased latencies through the fifth day. In Experiment Two, rats were trained as in Experiment One but immediately following the shift received intraamygdala infusions of oxotremorine (10 ng), propranolol (0.3 μg), both, or phosphate buffer. Shifted vehicle-injected rats returned to preshift performance by the fifth day of shifted training. Shifted propranolol rats returned to preshift latencies by the third day of shifted training. In contrast, the shifted oxotremorine and the shifted oxotremorine/propranolol rats displayed longer latencies than unshifted controls through 5 days of shifted training. The findings indicate that the muscarinic cholinergic and β-noradrenergic systems within the amygdala interact in regulating memory and support the view that noradrenergic influences are mediated through cholinergic activation.
Article
Extensive evidence indicates that benzodiazepine receptors in the amygdala are involved in regulating memory consolidation. Recent findings indicate that many other drugs and hormones influence memory through selective activation of the basolateral amygdala nucleus (BLA). This experiment examined whether the memory-modulatory effect of flumazenil, a benzodiazepine receptor antagonist, selectively involves the BLA. Bilateral microinfusions of flumazenil (12 nmol in 0.2 μl) into the BLA of rats administered immediately after training in an inhibitory avoidance task significantly enhanced 48-h retention performance whereas infusions into the central nucleus were ineffective. These findings indicate that the BLA is selectively involved in mediating flumazenil's influence on memory storage and are thus consistent with extensive evidence indicating that the BLA is involved in regulating memory consolidation.
Article
These experiments examined the involvement of the intrinsic GABAergic system of the amygdaloid complex in the modulation of memory storage. Rats were chronically implanted with bilateral cannulae in the amygdala, trained in an inhibitory avoidance task, and given post-training bilateral intra-amygdala injections of either the GABA receptor antagonist bicuculline methiodide (BMI) (0.1-1.0 nmol) or the GABAA receptor agonist muscimol (0.001-0.1 nmol). As indicated by performance on a 48 h retention test, BMI enhanced retention of the inhibitory avoidance conditioning, while muscimol impaired retention. The memory-enhancement obtained with BMI (0.1 nmol) was produced by a dose lower than that necessary to induce convulsions. Post-training injections of BMI did not affect retention when injected into the caudate-putamen dorsal to the amygdala. These results suggest that the amygdaloid GABAergic system is involved in the modulation of memory storage.
Article
This article reviews findings of research examining the interaction of peripheral adrenergic systems with cholinergic, opioid peptidergic and GABAergic systems in modulating memory storage. It is well established that retention is enhanced by posttraining systemic or intra-amygdala injections of adrenergic agonists, opiate antagonists and GABAergic antagonists. These influences appear to be mediated by activation of NE receptors within the amygdala, as intra-amygdala injections of β-adrenergic antagonists block the memory-modulating effects of hormones and drugs affecting these systems. Furthermore, these influences also appear to involve, at a subsequent step, activation of a cholinergic system: atropine blocks the memory-enhancing effects of adrenergic agonists and opiate and GABAergic antagonists and oxotremorine attenuate the memory-impairing effects of opiate agonists and GABAergic agonists. These findings suggest that the amygdala integrates the memory-modulating effects of neuromodulatory systems activated by learning experiences.
Article
Flashbulb Memories are memories for the circumstances in which one first learned of a very surprising and consequential (or emotionally arousing) event. Hearing the news that President John Kennedy had been shot is the prototype case. Almost everyone can remember, with an almost perceptual clarity, where he was when he heard, what he was doing at the time, who told him, what was the immediate aftermath, how he felt about it, and also one or more totally idiosyncratic and often trivial concomitants. The present paper reports a questionnaire inquiry into the determinants of such memories by asking about other assassinations, highly newsworthy events, and personally significant events. It is shown that while the Kennedy assassination created an extraordinarily powerful and widely shared flashbulb memory, it is not the only event that has created such memories. The principal two determinants appear to be a high level of surprise, a high level of consequentiality, or perhaps emotional arousal (assessed by both rating scales and ethnic group membership). If these two variables do not attain sufficiently high levels, no flashbulb memory occurs. If they do attain high levels, they seem, most directly, to affect the frequency of rehearsal, covert and overt, which, in turn, affects the degree of elaboration in the narrative of the memory that can be elicited experimentally. Parallels are made explicit between the behavioral theory and a less elaborated, speculative neuro-physiological theory of which R. B. Livingston (1967) is the proponent Finally, an argument is made that a permanent memory for incidental concomitants of a surprising and consequential (in the sense of biologically significant) event would have high selection value and so could account for the evolution of an innate base for such a memory mechanism.
Article
The expression of innate reproductive, defensive, and ingestive behaviors appears to be controlled by three sets of medial hypothalamic nuclei, which are modulated by cognitive influences from the cerebral hemispheres, including especially the amygdala and hippocampal formation. PHAL analysis of the rat amygdala indicates that a majority of its cell groups project topographically (a) to hypothalamic behavior systems via direct inputs, and (b) to partly overlapping sets of hypothalamic behavior control systems through inputs to ventral hippocampal functional domains that in turn project to the medial hypothalamus directly, and by way of the lateral septal nucleus. Amygdalar cell groups are in a position to help bias or prioritize the temporal order of instinctive behavior expression controlled by the medial hypothalamus, and the memory of associated events that include an emotional or affective component.
Article
The present study examined the effects, in male Sprague–Dawley rats, of microinfusion of drugs affecting glucocorticoid receptors (GRs or Type II) administered into either the basolateral (BLA) or central nucleus of the amygdala (CEA) on memory for training in an inhibitory avoidance and water-maze escape task. The specific GR agonist RU 28362 (1.0 or 3.0 ng) infused into the BLA immediately after training in a one-trial inhibitory avoidance task dose-dependently enhanced 48-h retention, whereas infusion of the GR agonist into the CEA did not affect retention. Additionally, pretraining microinfusions of the specific GR antagonist RU 38486 (0.3, 1.0, or 3.0 ng) into the BLA, but not infusions into the CEA, impaired memory for escape training to find a submerged platform in a water maze. These findings indicate that glucocorticoids affect memory storage, at least in part, by binding directly to GRs in the BLA and provide further evidence for the view that the BLA is an important brain region in integrating hormonal and neurotransmitter influences on memory storage.
Article
In the present study, we investigated the effect of immediate post-training bilateral infusion of spermidine, a polyamine agonist, into the amygdala on inhibitory avoidance learning of rats. Bilateral microinjection of spermidine (0.02–20 nmol) caused an increase in test step-down latencies at high concentrations. Administration of arcaine (0.002–0.2 nmol), an antagonist of the NMDA receptor polyamine binding site, decreased test step-down latencies. On the other hand, co-administration of arcaine and spermidine completely reversed the spermidine-induced increase of test step-down latencies. These results provide evidence that polyamines may be involved in learning and memory modulation in the amygdala.