Two routes to emotional memory: Distinct neural processes for valence and arousal

“…of emotional memory have correspondingly focused on encoding (e.g., Cahill et al., 1996; Canli et al., 2000, 2002; Dolcos & Cabeza, 2002; Dolcos et al., 2004b; Hamann et al., 1999; Kensinger & Corkin, 2004; Kilpatrick & Cahill, 2003; Richardson et al., 2004; Sergerie, Lepage, & Armony, 2005).”

“Early affective processing may be influenced by arousal such that memory for arousing stimuli produces activation in the amygdala and hippocampus, whereas memory for nonarousing stimuli yields activation only in the hippocampus (Kensinger & Corkin, 2004).”

“, [48,49]) or self-relevant ([5], reviewed in [7]) even when attention is divided ([40,50], for an exception see [51]).”

“…how the brain responds to each dimension. fMRI studies have shown that processing of valence and arousal are supported by distinct brain networks (Kensinger & Corkin, 2004) and have varying temporal representations (Bayer, Sommer, & Schacht, 2010; Citron, Weekes, & Ferstl, 2013; Olofsson,…”

“The role of amygdala on emotional memory may depend on the degree of arousal of emotional stimuli [21, 22].”

“The arousal level of stimuli has been reported to affect cognition in memory and attention, possibly through the amygdala function of amygdala (Kensinger and Corkin, 2004; Anderson et al., 2006).”

“1 It is particularly important to equate words in terms of arousal because negative st imuli are often rated as more arousing than positive or neutral stimuli (Garavan, Pendergrass, Ross, Stein, & Risinger, 2001 ), and there may be different neural pathways for valence and arousal (Kensinger & Corkin, 2004 ; See also…”

“For example, activity in frontal–hippocampal networks, associated with controlled encoding processes, predicts memory for less arousing events (Kensinger & Corkin, 2004).”

“This effect depends on a facilitation of hippocampus-dependent memory processes by the amygdala (Seidenbecher et al., 2003; Dolcos et al., 2004; Kensinger and Corkin, 2004; Phelps, 2004; Smith et al., 2006; Figure 1A) and is related to the action of glucocorticoids (Kim and Diamond, 2002; Sapolsky,…”

“Each affective state can have various arousal levels (a.k.a intensity)[24].”

“The results do converge with prior literature indicating that emotional arousal and valence have dissociable effects on discriminability [59,60] (see Kensinger, 2004 [13], for a review).”

“In these cases, contrasts testing either for memory across emotional and neutral stimuli (Kensinger and Corkin, 2004; Erk et al., 2010), for memory of the included neutral stimuli (Iidaka et al., 2003), or, in one case, for memory of emotional stimuli (Kensinger and Schacter, 2005) were considered.”

“Various studies have shown differential processing of emotional and neutral stimuli in general (Kensinger & Corkin, 2004) as well as differences in the efficiency of suppressing emotional and neutral thoughts (e.g., Depue et al., 2006; Hertel & Gerstle, 2003; Joormann et al., 2005; Murray et al.,…”

“This is consistent with evidence that the interaction between emotion and attention during encoding is partly dissociable from the influence of emotion on later memory (Kensinger & Corkin, 2004; Riggs, McQuiggan, Farb, Anderson, & Ryan, 2011; Talmi et al., 2007).”

“Consistent with previous research (Hamann, et al., 1999; Kensinger & Corkin, 2004), we found that people remembered highly arousing stimuli more than stimuli with low arousal, regardless of valence.”

“enhancement (Canli, Zhao, Brewer, Gabrieri, & Cahill, 2000; Dolcos, LaBar, & Cabeza, 2004; Hamann et al., 1999), is also known to be modulated by the arousal level of stimuli rather than valence (i.e., positive or negative; Anderson et al., 2003; Kensinger & Corkin, 2004 ).”

“Arousal appears to be the core aspect activating the amygdala, whereas valence properties of a stimulus are mainly processed in the prefrontal parts of the brain.(21,23) Elaborating on a wealth of animal studies, the role of stress hormones such as noradrenaline and cortisol on Imaging Stress Effects on Memory: A Revi…”

“…the relative contributions of each mechanism toward abnormal emotional DF in 1 Emotionally significant stimuli are often conferred an automatic memory advantage termed the emotional enhancement of memory (e.g., Anderson et al., 2006; Kensinger and Corkin, 2003, 2004; Sommer et al., 2008).”

“Consistent with Kensinger and Corkin’s [11] proposal, the guide’s emotional memory holds not only information about when, what and how an event happened, but also an ‘arousal’ tag and a ‘valence’ tag.”

“Memory misattributions can occur less often for items that contain emotional relevance than for those void of emotional content (Kensinger and Corkin, 2004a; Kensinger and Schacter, in press(b); Pesta et al., 2001), plausibly because emotional information is more likely to be remembered with…”

“In the inverse group comparison (HC > OCD), healthy controls in the shame-neutral condition show activation within a frontoparietal network that might reflect processes of self-referencing and affective regulation (Goldin et al., 2008; Kensinger and Corkin, 2004; Rizzolatti and Craighero, 2004).”

“This emotional enhancement effect (Kensinger, 2006) has been suggested to be primarily driven by amygdalamodulated consolidation processes in the medial temporal lobe (Kensinger et al., 2002; Kensinger and Corkin, 2004; Ritchey et al., 2008).”

“It is well established that emotionally negative stimuli such as International Affective Picture System (IAPS) pictures [24] or faces with negative expressions are better remembered than neutral items [29–32].”

“Yet the EEM is often pronounced immediately after study (e.g. Harris and Pashler, 2005; Kensinger and Corkin, 2004), before synaptic consolidation has been completed (Alberini and Kandel, 2015); a finding for which the modulation model cannot account.”

“Studies that increase processing load during encoding could investigate whether testosterone preserves memory for males when elaborative encoding strategies are compromised, for example with divided attention procedures (e.g., Kensinger and Corkin, 2004).”

“In general, valence refers to a pleasant-to-unpleasant state and arousal refers to a low-to-high state of excitement (Kensinger and Corkin, 2004).”

“We opted not to use a bipolar valence scale because such scales have an inherent ambiguity built into them; they conflate changes in valence with changes in arousal (Kensinger and Corkin, 2004).”

“Research using fMRI has found that words such as “rape” and “slaughter”, which are not swear words, produce activation of the amygdala, a part of the brain strongly linked to emotion processing (Kensinger & Corkin, 2004).”

“For example, it has been suggested that higher arousal has more impact on automatic processes whereas valence influences controlled processes in memory (Kensinger and Corkin, 2004).”

“amygdala and hippocampus are known to play critical roles in the consolidation of emotionally laden memories in healthy adults (Kensinger and Corkin, 2004).”

“This is consistent with a prevailing concept that during emotional memory formation, the amygdala communicates Ex emotional itemevoked arousal to the hippocampus, thus rendering it susceptible to valence transfer from the PFC (Dolcos et al. 2004b ; Kensinger, 2004; Kensinger & Corkin, 2004).”

“As previous studies demonstrated that both, negative and positive events evoke emotional brain activation in areas such as the amygdala and the hippocampus (Kensinger and Corkin, 2004; Kensinger and Schacter, 2006; Lewis et al., 2007), we decided to present a variety of pictures which carry positive and negative emoti…”

“These attentional effects may be more important for positive arousing stimuli than for negative arousing stimuli (Kensinger & Corkin, 2004; Talmi, Schimmack, Paterson, & Moscovitch, 2007).”

“…in an amygdalarhippocampal pathway, while recall of non-arousing words is related to a more executively controlled hippocampal-frontal pathway (Kensinger & Corkin, 2004) and several studies have indicated that the memory of nonarousing or more common words is less dependent upon arousal than…”

“Kensinger and Corkin (2004) report the hemodynamic correlates of processes that predicted whether neutral, negative, and nonarousing or negative and arousing words were later remembered.”

“…enhancement effects in memory have mostly failed to make the distinction between emotionally positive and emotionally negative stimuli (e.g., Kensinger and Corkin, 2004; Talmi and Moscovitch, 2004) despite evidence showing that valence (how positive or negative an item is) affects…”

“Moreover, such age-related positivity effects in memory have shown to be specific to lowarousing emotional stimuli (Kensinger, 2008), which engage more controlled as opposed to automatic processes commonly involved in processing highly arousing stimuli (Kensinger and Corkin, 2004).”

“…and parahippocampal gyrus), striatum, medial and dorsolateral prefrontal cortices , and amygdala (Delgado et al., 2008; Depue et al., 2007; Kensinger and Corkin, 2004; Kilpatrick and Cahill, 2003; LeDoux, 1996; McGaugh et al., 1996; Peper et al., 2006; Phelps, 2006; Phelps and LeDoux,…”

“…studies have indicated that both the EME for the E items and the ERA affecting the E-1 items depend on the beta-adrenergic modulation of amygdala activity during encoding and on hippocampal activation during retrieval (Strange & Dolan, 2004; Strange et al., 2003; see also Kensinger & Corkin, 2004).”

“Changes in arousal level and valence—the affective signed value associated with a stimulus or context—are crucial for the manifestation of motivational states 30 , and are therefore likely to have an important role in regulating interactions with the environment.”

“The amygdala is the primary brain structure for processing fear, and it has been linked to behavioral inhibition (Haas, Canli, Haas, & Canli, 2008; Kensinger & Corkin, 2004; Morgan & Morgan, 2006), suggesting neural substrates implicated in the functioning of the amygdala are also potential…”

“…in Behavioral Neuroscience www.frontiersin.org August 2013 | Volume 7 | Article 109 | 1 and memory MTL systems during encoding (Dolcos et al., 2004; Kensinger and Corkin, 2004; Kensinger and Schacter, 2006; Sergerie et al., 2006), consolidation (Ritchey et al., 2008), and retrieval (Hamann et al.,…”

“These patients appear to access other cognitive resources that enhance emotional episodic memory, most likely by recruiting mPFC–hippocampal routes that code emotional valence (Kensinger 2004; Kensinger and Corkin 2004).”

“This result provides a novel contribution to studies on the role of the amygdala in emotional memory, which have previously shown that amygdala activation at encoding mediates the relationship between emotionally arousing stimuli and increased memory encoding or retrieval for those stimuli (Cahill et al., 1996; LaBar…”

“…intensity (i.e., arousal; Anderson et al., 2003; Small et al., 2003; Glascher and Adolphs, 2003; Anders et al., 2004; Cunningham et al., 2004; Kensinger and Corkin, 2004; Kensinger and Schacter, 2006; Lewis et al., 2007; Gerber et al., 2008) or a combination of both valence and intensity…”

“Thus, this research should be seen as promoting the idea that two mechanisms support the emotional enhancement of memory (see Kensinger & Corkin, 2004; Schmidt & Saari, 2007): increased attention and/or increased discriminability (i.e., distinctiveness).”

“The memory advantage for emotional versus neutral stimuli is larger when attention is divided during encoding compared to full attention (Kensinger & Corkin, 2004; Kern et al., 2005; Maddox et al., 2012) because divided attention reduces memory for neutral stimuli more than emotional stimuli.”

“Other regions involved in episodic memory retrieval of emotional imagery include the medial temporal lobe (Hamann 2001; Kensinger and Corkin, 2004) and the ventral striatum (Klucken, Tabbert, and Schweckendick et al. 2009b).”

“The caudal hippocampus is believed to be extensively connected to the amygdala and work together to process affective memories, specifically associated with negative emotions [83,84]; to modulate function of other neural structures in the reward pathway, and to mediate anxiety and depressive behaviors, and perhaps alc…”

“This enhanced activity is suggested to modulate memory consolidation (Dolcos et al., 2004b), resulting in better memory performance for emotionally arousing material relative to neutral (Dolcos, Denkova, & Dolcos, 2012; Dolcos et al., 2004b; Kensinger & Corkin, 2004).”

“Furthermore, this area has been associated with emotional memory coding and especially when modulated by arousal [64–66].”

“Some of these pathways may initially bypass the amygdala and indirectly contribute to emotional memory (Kensinger and Corkin, 2004; Sergerie et al., 2005).”

“…studies have found that arousal-related responses are unaffected by diverted attention and do not rely on conscious awareness or evaluation of the stimulus, whereas valence responses are controlled and dependent on attentional resources (Cunningham, Raye, & Johnson, 2004; Kensinger & Corkin, 2004).”

“…temporal lobe (including the hippocampus and parahippocampal gyrus) (McGaugh et al. 1996; LeDoux 1996; Kilpatrick and Cahill 2003; Richter-Levin 2004; Kensinger and Corkin 2004; Phelps and LeDoux 2005; Phelps 2006; Peper et al. 2006; Depue et al. 2007) and to interact with the prefrontal cortex…”

“While this approach is valuable in that it mirrors how emotions develop and evolve in response to unfolding events, it is unknown whether the model would generalize to brief, momentary stimuli such as affective images [ 24,30] or sounds [3,4,25] that are also known to modulate emotional arousal.”

“Although the literature distinguishes between high-arousal and low-arousal emotions (e.g., Kensinger, 2004; Kensinger & Corkin, 2004), applying SC as the only method of investigating emotion might not be sufficient to answer the question of which emotion, and of what valence, the participant…”

“Neuroimaging studies support this assumption by showing that amygdala activity varies according to the level of arousal evoked by a stimulus (Kensinger and Corkin, 2004; Sabatinelli et al., 2005; Kensinger and Schacter, 2006; Kryklywy et al., 2013).”

“The orthogonality of these two dimensions is also supported by neuroimaging results (Kensinger and Corkin, 2004; Posner et al., 2009): the valence-specific network was associated with the insula, the arousal-specific network with the medial prefrontal cortex and posterior cingulate, while both…”

“Fear, anger and happiness are usually referred to as high-arousing emotions, while sadness is described as a low-arousing emotion (e.g. Kensinger & Corkin, 2004; Kensinger, 2004).”

“While they are not completely independent, valence and arousal have been found to be dissociable in terms of the physiological responses they produce (Colibazzi et al., 2010), as well as their impact on other cognitive processes like memory (Kensinger & Corkin, 2004).”

“There were a bunch of studies demonstrating that valence (ranging from negative to positive) and arousal (ranging from calming to exciting) exerted divergent effects on cognitive processing and that they differentiated in related neural substrates (Mourão-Miranda et al., 2003; Anders et al., 2004; Kensinger, 2004; Ken…”

“Memory for arousing emotional words is supported by automatic AMY activation, whereas memory for negative but nonarousing words was associated with increased activity in the PFC–HC network (Kensinger and Corkin, 2004).”

“For example, Kensinger and Corkin (2004) tested memory after 10 minutes, and Dolcos et al. (2004a) after 45 minutes.”

“Other investigators conducting structural and functional neuroimaging studies of depression have focused on the amygdala, given its critical involvement in the perception and memory of emotional information (Kensinger and Corkin 2004; Adolphs 2008; Pessoa and Adolphs 2010).”