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

“It is also supported by imaging studies, which suggest distinct neural systems for the processing of valence and arousal (Anders et al., 2004; Lewis et al., 2007; Kensinger and Corkin, 2004).”

“…as olfactory (Anderson et al., 2003), gustatory (Small et al., 2003), picture (Anders et al., 2004; Grimm et al., 2006; Nielen et al., 2009), word (Kensinger and Corkin, 2004; Lewis et al., 2007; Nielen et al., 2009; Posner et al., 2009), and face (Gerber et al., 2008), as well as emotional…”

“More recently, Kensinger and Corkin (2004) investigated brain structures and pathways involved in processing emotional words using functional magnetic resonance imaging and behavioral methods.”

“That is, individuals do better at recognizing emotional elements within scenes than neutral elements, but they do worse at recognizing the contexts in which emotional versus neutral elements were presented (Kensinger & Corkin, 2004; Kensinger et al., 2007).”

“, 2008), valence and arousal seem to be processed with differential connectivity pattern toward the hippocampus: a fast pathway via amygdala in case of arousal, and slower and more controlled pathway via prefrontal cortex for valence (Kensinger and Corkin, 2004).”

“Namely, immediate memory benefits are thought to result from attentional mechanisms whereas delayed memory benefits are thought to result from postencoding consolidation (Kensinger and Corkin 2004; Talmi et al. 2008).”

“Using functional magnetic-resonance imaging, Kensinger and Corkin (2004) has shown that effects of stimulus valence on memory encoding seem to be mediated by a PFC-hippocampal network, whereas effects of arousal appear to be dependent on an amygdalar-hippocampal network.”

“…words, emotional words are more likely to be attended (Williams et al., 1996; Mogg et al., 1997; Anderson and Phelps, 2001), are better remembered (Kensinger and Corkin, 2004; Krolak-Salmon et al., 2004; Strange and Dolan, 2004; Vuilleumier et al., 2004; Kissler et al., 2006), and are also more…”

“…materials (Bradley, Greenwald, Petry, & Lang, 1992; Dolcos & Denkova, 2008; Dolcos, LaBar, & Cabeza, 2004; Hamann, Ely, Grafton, & Kilts, 1999; Kensinger & Corkin, 2004) and their intrinsic features (D'Argembeau & Van der Linden, 2004; Doerksen & Shimamura, 2001; Kensinger & Corkin, 2003a;…”

“There is some evidence for different representations for positive and negative valence (Canli, Desmond, Zhao, Glover, & Gabrieli, 1998; Kensinger & Corkin, 2004), which may differentially affect interference resolution processes.”

“Past fMRI studies in humans have shown that BOLD activity in the amygdala and the hippocampus is correlated during encoding (Kensinger and Corkin, 2004) and retrieval (Kensinger and Schacter, 2007) of emotional information.”

“…of the amygdala in encoding: It makes sense that amygdala connectivity would strengthen with increasing arousal if the amygdala plays a particularly important role in the encoding of negative, high-arousal stimuli (e.g., Adolphs et al., 1999; Kensinger & Corkin, 2004; Cahill and McGaugh, 1995 ).”

“Moreover, arousing stimuli are remembered better than less arousing stimuli (Bradley et al. 1992; Dunsmoor et al. 2015; Kensinger and Corkin 2004).”

“Emotionʼs influence over cognition can be separated into two broad categories: those resulting from arousal and those resulting from valence (Anderson et al., 2003; Kensinger & Corkin, 2004).”

“... and Stang’s proposal of an intensity principle is in agreement with neuropsychological studies showing that the amygdala plays a key role in the encoding of negative emotional stimuli (Cahill & McGaugh, 1990, 1998; Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000), as well as in the encoding of positive emotional sti…”

“The amygdala and hippocampus have been linked with a specific arousal-evoking pathway during the processing of emotional memories [ Kensinger and Corkin, 2004 ].”

“The MTL mechanism contributes to the memory-enhancing effect of emotion through direct/bottom-up neurohormonal interactions between the AMY and memory-related MTL regions, during encoding (e.g., Dolcos et al., 2004b; Kensinger and Corkin, 2004; Kensinger and Schacter, 2006a; Sergerie et al., 2006; Ritchey et al., 2008…”

“The notion that cognitive factors contribute to immediate EEM is not new (Cahill & McGaugh, 1998; Kensinger & Corkin, 2004), yet it is unknown which factors ting for immediate emotional memory enhancement.”

“Even when encodingrelated factors such as attention and rehearsal are equated, emotional stimuli are more likely to be remembered later (Harris & Pashler, 2005; Kensinger & Corkin, 2004; Sharot & Phelps, 2004).”

“Results from their fMRI experiment suggested that memory enhancement for valenced, non-arousing words relied on activation of a prefrontal cortex—hippocampal network, whereas memory enhancement for arousing words relied on activation of an amygdalar—hippocampal network (Kensinger and Corkin, 2003).”

“Activity in the amygdala and hippocampus did relate disproportionately to later memory for emotional compared to neutral information, and activity in the amygdala was particularly related to subsequent memory for arousing information (see also Anderson et al., 2006; Kensinger & Corkin, 2004 ).”

“Because recent studies have shown differential neural recruitment in the processing of these two factors (activity and connectivity between the medial-temporal lobe and the DLPFC) (Dolcos, LaBar, & Cabeza, 2004a; Kensinger & Corkin, 2004 ), investigating the effect of these factors independent of each other on age-rel…”

“…of emotion on memory has been demonstrated to operate on multiple memory processes, including encoding—the initial formation of a memory trace (Dolcos, LaBar, & Cabeza, 2004a; Kensinger & Corkin, 2004)—and consolidation—the strengthening of this memory trace over time (LaBar & Phelps, 1998).”

“Prior studies have indicated that interactions between the amygdala and the hippocampus are critical for emotionalmemoryenhancementeffects(e.g.,Dolcosetal.,2003; Kensinger & Corkin, 2004a; Richardson et al., 2004).”

“…linking AMY-HC engagement to a direct route contributing to the memory-enhancing effect of emotion (Dolcos et al., 2004a,b, 2011, 2012; Kensinger and Corkin, 2004) and with studies showing that emotional distraction is linked to increased activity in ventral-affective regions (e.g.,…”

“Murty and colleagues emphasize the central role of the medial temporal lobe (MTL) in emotional encoding (see also Dolcos, LaBar, and Cabeza 2004; Hamann 2001; Kensinger and Corkin 2004).”

“2), thus providing further support for the modulation hypothesis (see also Kensinger & Corkin, 2004; Kilpatrick & Cahill, 2003).”

“As hypothesized, and consistent with previous studies (Dolcos, LaBar, & Cabeza, 2004; Kensinger & Corkin, 2004; Richardson, Strange, & Dolan, 2004; Strange & Dolan, 2004), we observed a significant amygdala activation associated with the successful encoding of negative stimuli.”

“As previously mentioned, the left IFG has been associated with predicting later subsequent memory recall (Kensinger & Corkin, 2004).”

“The observation that positive and negative pictures have a similar effect on connection strength might be in line with earlier studies demonstrating that amygdala activation is associated with arousal common to both negative and positive events, but not valence itself (Anderson et al., 2003; Small et al., 2003; Kensin…”

“Kensinger and Corkin (2004) found that amygdala activity was generally stronger during the processing of negative than neutral words irrespective of their arousal.”

“It is well established that negative emotion can influence memory during both encoding (Dolcos, LaBar, & Cabeza, 2004; Kensinger & Corkin, 2004) and consolidation (LaBar & Cabeza, 2006; McGaugh, 2004).”

“prefrontal cortex-hippocampal networks [LaBar and Phelps 2002; Kensinger and Corkin 2004]).”

“…separate neural routes for valence and arousal, although with some inconsistencies in the results (Anders, Lotze, Erb, Grodd, & Birbaumer, 2004; Colibazzi et al., 2010; Gianotti et al., 2008; Kensinger & Corkin, 2004; Kensinger & Schacter, 2006; Lewis, Critchley, Rotshtein, & Dolan, 2007).”

“Consistent with previous research (e.g., Canli et al., 2000; Kensinger & Corkin, 2004 ), we find that encoding activation in the amygdala and hippocampus correlates with recognition memory for emotional stimuli.”

“This result corroborates previous functional neuroimaging studies that reported a dissociated neural representation of the two dimensions (e.g., [2, 22 , 23]).”

“It is interesting that the apparent lack of influence of arousal on emotional face memory is in contrast to evidence that arousal plays a role in memory for emotional scenes (Canli et al., 2000) and words ( Kensinger & Corkin, 2004 ).”

“Memory distortion for emotional versus neutral information has been investigated previously with associate lists (Kensinger & Corkin, 2004a; Pesta et al., 2001).”

“…often associated with OFC (Lewis et al., 2007), ventral anterior (as well as posterior and subgenual) cingulate cortex (vACC; Maddock et al., 2003), inferior frontal (Briesemeister et al., 2014b) or a prefrontal cortex-amygdalar network (Kensinger and Corkin, 2004; Schlochtermeier et al., 2013).”

“…whether the memories of arousing stimuli over the short term are qualitatively different from memories of non-arousing stimuli in this group, which would implicate the amygdala (see Kensinger & Corkin 2003; Kensinger & Corkin, 2004 for a divided attention paradigm that may be suitable here).”

“It would also be consistent with the multiplicity of possible neuroanatomical pathways linking emotional and memory brain systems (Kensinger and Corkin, 2004; Schaefer et al., 2006).”

“, perception [15–18], spatial or temporal attention [19–21], and memory [22–26], until now no study has investigated whether effects of valence and arousal on cognitive processing are indeed dissociable.”

“Furthermore, valence can enhance memory for low-arousing items via prefrontal-based organizational strategies during retrieval that are independent of the amygdala and noradrenergic modulation (Kensinger and Corkin, 2004; Mickley Steinmetz and Kensinger, 2009).”

“Emotional arousal allows recruiting additional cognitive and attentional resource allocation (Anderson and Sobel, 2003), facilitating access to awareness (Vuilleumier and Schwartz, 2001) and enhancing encoding and memory through an automatic process mediated by the sub-cortical amygdalar–hippocampal route (Kensinger a…”

“In one study, Kensinger and Corkin (2004a) revealed that non-arousing items that were vividly remembered were associated with enhanced lateral prefrontal and hippocampal activity during encoding, consistent with the results revealed in a number of subsequentmemory neuroimaging studies (Paller &…”

“…emotionally arousing stimuli preferentially recruit attentional resources, such as in dual-task conditions, resulting in even greater memory advantages relative to neutral stimuli (Kensinger and Corkin, 2004; MacKay et al., 2004; Mather and Sutherland, 2011; Kang et al., 2014; Madan et al., 2017).”

“…(e.g., Öhman, Flykt, & Esteves, 2001), and we process emotional information faster and more fluently than non-emotional information (Kityama, 1990), even in the absence of full attention (Kensinger & Corkin, 2004; Talmi, Schimmack, et al., 2007; Talmi, Anderson, Riggs, Caplan, & Moscovitch, 2008).”

“Moreover, these substances indirectly act to modulate the activity of the amygdala, which itself modulates hippocampal memory consolidation processes (Adolphs, Tranel, & Buchanan, 2005; Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000; Kensinger & Corkin, 2004; McGaugh, 2004).”

“More recently, several imaging and electrophysiological studies have demonstrated that dissociable anatomical substrates are responsible for the effects induced by these two dimensions (Anderson et al., 2003; Arana et al., 2003; Kensinger & Corkin, 2004; Small et al., 2003; Yeung & Sanfey, 2004).”

“These include the hippocampus and various regions in prefrontal cortex (Hamann et al., 1999; Dolcos et al., 2004; Kensinger and Corkin, 2004).”

“…magnetic resonance imaging data suggest that memory enhancements due to valence are associated with increased activity in regions within the PFC, and memory enhancements due to arousal are associated with increased activity in the amygdala (Dolcos, LaBar, & Cabeza, 2004; Kensinger & Corkin, 2004).”

“The neurocognitive basis for the change in valence (and arousal) ratings remains to be clarified [26,47–49].”

“For example, these areas are active when reading emotional, relative to nonemotional words (Kensinger and Corkin 2004; Burnett et al., 2009), and damage to vmPFC and amygdala results in social-emotional processing impairments (Barrash et al.”

“Functional imaging studies have indicated that increased activation of both the amygdala and orbitofrontal cortex is present during emotional memory tasks (e.g. Kensinger and Corkin, 2004; Kensinger and Schacter, 2005).”

“Additionally, Kensinger and Corkin (2004) have demonstrated that the intensity of a verbal stimulus determines both the amygdala response and the subsequent memory of that stimulus whereas memory for less intense, negatively valenced words was associated with prefrontal activity during encoding.”

“Indeed, in many areas of cognitive neuroscience, BA 47 is discussed as being a part of the ventrolateral prefrontal cortex (vlPFC; Badre & Wagner, 2007) or the inferior frontal gyrus (Kensinger & Corkin, 2004), as opposed to the OFC.”

“Possibly, attention to emotion is mediated by the amygdala, whereas its connections to the thalamus may mediate these attentional effects in preparation for action (Kensinger & Corkin, 2004).”

“High arousal, rather than valence, particularly drives amygdala activity in American samples (Kensinger and Corkin, 2004); it is possible that the connectivity between the amygdala and the hippocampus or frontal regions differs for East Asians who could prioritize low arousal information more than Americans.”

“ORIGINAL RESEARCH ARTICLE published: 28 July 2014 doi: 10.3389/fpsyg.2014.00681 The role of arousal in the spontaneous regulation of emotions in healthy aging: a fMRI investigation”

“…want to take this into account when selecting stimulus items, if the goal is to dissociate effects of valence from effects of arousal (e.g., Anderson et al., 2003; Cunningham, Raye, & Johnson, 2004; Dolcos, LaBar, & Cabeza, 2004; Kensinger & Corkin, 2004; Lewis et al., 2007; Small et al., 2003).”

“2006) and human fMRI studies of emotional memory (Kensinger and Corkin 2004; Phelps 2004; Richardson et al. 2004; Dolcos et al. 2005; LaBar and Cabeza 2006).”

“The hippocampus has been linked with specific arousal-evoking pathways during the processing of emotional autobiographical memories [Kensinger and Corkin, 2004].”

“Moreover, memory processes involving emotional material have been frequently found to implicate the recruitment of a different network of neural structures, including the amygdala and the parahippocampal area (Kensinger & Corkin, 2004; Murray & Kensinger, 2013).”

“…might vary on the arousal scale, with anger and fear usually described as high arousing emotions, and sadness as a low arousing emotion (e.g., Kensinger and Corkin 2004; Kensinger 2004), previous studies have shown that this difference might not necessarily be reflected in GSR patterns…”

“Arousal was manipulated in this study given the evidence of distinct neural networks involved in processing arousing vs. valenced information (Kensinger and Corkin, 2004) and differential effects of low vs. high arousal valenced information (Leclerc and Kensinger, 2008).”

“This is in line with reports of an enhancing effect of emotional stimuli on memory performance (for review, see Hamann, 2001; Phelps, 2006), which is explained by a modulating effect of the amygdala on sensory systems (Davis & Whalen, 2001; Kensinger & Corkin, 2004; Vuilleumier, 2005).”

“Although a number of studies have reported amygdala activation during the processing of verbal stimuli (Hamann & Mao, 2002; Herbert et al., 2009; Kensinger & Corkin, 2004; Kensinger & Schacter, 2006b; for a review, see Baas, Aleman, & Kahn, 2004), there is considerable evidence that amygdala…”

“Whereas arousal is thought to reflect the degree of physiological response generated during retrieval, valence considers the positivity or the negativity of the event (Conway, 2013; Conway et al., 1994; Kensinger & Corkin, 2004).”

“This brain structure is mainly implicated in the relatively automatic facilitation of memory processes in other brain regions during memory encoding (Kensinger and Corkin, 2004; Kilpatrick and Cahill, 2003; McGaugh, 2004).”

“…language-dependent processing (Markowitsch, 1998; Phelps, 2006), the right amygdala has been shown to subserve a system of automatic detection of emotional stimuli (Kensinger and Corkin, 2004; Costafreda et al., 2008), which can be triggered by recognition tasks (Clark-Foos and Marsh, 2008).”