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

“…was selectively associated with familiarity and activity in the hippocampus and posterior parahippocampal gyrus was selectively associated with recollection (Daselaar et al. 2006, Davachi et al. 2003, Kensinger & Corkin 2004, Ranganath et al. 2003, Uncapher & Rugg 2005, Weis et al. 2004b).”

“These studies have demonstrated that the amygdala is critical for the acquisition, storage, and expression of a conditioned fear response (Davis 1992, Kapp et al. 1992, LeDoux 1996, Maren 2001, but see also Cahill et al. 1999).”

“Simultaneously, amygdala-hippocampus activation was observed during the memory encoding of negative arousing words (Kensinger and Corkin, 2004).”

“…has been reported in a number of studies (Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000; Dolcos et al., 2004; Hamann, Ely, Grafton, & Kilts, 1999; Kensinger & Corkin, 2004; Sharot & Phelps, 2004), with the extent of functional connectivity at the time of learning being especially predictive of…”

“…the processing of emotional information, there are correlations between the strength of activity in the amygdala and in the hippocampus (e.g., Kensinger & Corkin, 2004), and the strength of these correlations can correspond with the magnitude of the mnemonic boost for emotional information…”

“We have also suggested that the high (declining) end of the curvilinear component of the Yerkes-Dodson law is generated largely by a stress-induced suppression of PFC functioning (see also Kensinger and Corkin [446] for related discussion).”

“These observations are in accord with neuroimaging studies showing that the activity of the amygdala is associated with memory formation of arousing stimuli (Cahill et al., 1996; Canli et al., 2000), apparently independent of stimuli valence (Hamann et al., 1999; Kensinger and Corkin, 2004).”

“…activity in the amygdala when viewing negative emotional stimuli (Anderson et al. 2003; Canli et al. 2000; Critchley et al. 2000; Morris et al. 1998), and this activity is related to later memory for this material (Cahill et al. 1996; Canli et al. 2000; Dolcos et al. 2004; Kensinger & Corkin 2004).”

“In particular, activity in the amygdala during the successful encoding of emotional information is positively correlated with activity in the hippocampus (e.g., Dolcos et al., 2004; Kensinger & Corkin, 2004).”

“Although the enhancing effects of emotion on cognitive functions has been the focus of intensive research (Christianson, 1992; Dolcos et al., 2004b; Kensinger and Corkin, 2004; McGaugh, 2004; Phelps, 2004; Sharot et al., 2004; Dolcos et al., 2005, 2006), the detrimental effects of emotion on cognitive functions have r…”

“…emotional words (especially highly arousing negative words) are more memorable than are neutral words even when they are learned while distracted (Kensinger & Corkin, 2003, 2004); however, to our knowledge, previous studies have not examined whether divided-attention affects negative and…”

“…about if and how the amygdala processes valence or arousal information (e.g., Anders, Eippert, Weiskopf, & Veit, 2008; Barrett, Bliss-Moreau, Duncan, Rauch, & Wright, 2007; Berntson, Bechara, Damasio, Tranel, & Cacioppo, 2007; Kensinger & Corkin, 2004; Lewis, Critchley, Rotshtein, & Dolan, 2007).”

“Kensinger and Corkin (2004) [#45] asked participants to encode words either as the sole task, or while concurrently performing an auditory discrimination task.”

“The amygdala and hippocampus are both known to play critical roles in the consolidation of emotionally laden memories in healthy adults (Kensinger and Corkin, 2004; Hamann et al., 1999).”

“fMRI evidence has suggested that for non-arousing information, successful encoding may be tied to the implementation of prefrontal processes tied to semantic elaboration and self-referential processing – regions that are recruited when we try to understand the meaning of information or to consider how the information…”

“…with the IES model, the amygdala-hippocampal-prefrontal interaction model includes the hippocampus, which is also frequently found in emotion related studies using functional connectivity methods (Kensinger and Corkin, 2004; Smith et al., 2006), and takes the effects of environment into account.”

“Enhanced amygdala activity (a neurophysiological marker of arousal) is found during initial processing of taboo words, and is associated with enhanced attention and superior memory for taboo words (Kensinger and Corkin 2004).”

“An aim of the current study was to determine whether the dissociation between valence and arousal that has been observed in the chemosensory domain also holds for these abstract stimuli (for prior efforts in this area, see Dolcos and others 2004; Kensinger and Corkin 2004).”

“Both the amygdala and hippocampus are identified as regions of interest in PTSD due to their role in the processing and coordination of traumatic memories and perception (Rolls, 1996; Kensinger and Corkin, 2004) and in salience network (SN) processes.”

“, 2004) and, together with other research conducted in humans (Cahill et al., 1996; Kensinger and Corkin, 2004) and in animals (McGaugh et al.”

“…that overall the memory-enhancing effect of emotion is driven by the intensity of emotional events, rather than by their valence, although there is evidence that valence is also a contributing factor (Kensinger & Corkin, 2004; Mickley Steinmetz & Kensinger, 2009; Shaw, Brierley, & David, 2005).”

“…to support processes such as attention, attention-based learning, arousal, and the enhancement of memory formation, all of which have been shown to involve the amygdala (Holland and Gallagher, 1999, 2006; Kensinger and Corkin, 2004; McGaugh, 2004; Oya et al., 2005; Phelps and LeDoux, 2005).”

“film clips predicts subsequent retention (Cahill et al. 1996; Canli and others 2000; Kensinger and Corkin 2004), which is associated with functional interactions between the amygdala”

“Such a system is beneficial for shifting processing under stress away from slower, more deliberative processes that depend on the PFC (Gabrieli, Poldrack, & Desmond, 1998) and toward more automatic, reflexive processes that depend on subcortical areas like the amygdala (Kensinger & Corkin, 2004).”

“A recent model by Kensinger and Corkin (2004) describes the distinction between an arousal-dependent amygdalar-hippocampal and a valence-dependent prefrontal cortex-hippocampal network, supporting the idea of different neural pathways for valence and arousal.”

“This region has also been identified as showing greater ESA for emotional than neutral memory (Dolcos et al., 2004a; Kensinger & Corkin, 2004), which has been interpreted as indexing enhanced elaboration of emotional stimuli.”

“, 2003 ; Kensinger and Corkin , 2004 ) .”

“…& Yurgelun-Todd, 2004), intensity (Anders et al., 2004; Glascher & Adolphs, 2003; Kensinger & Corkin, 2004; Kensinger & Schacter, 2006; Small et al., 2003), or a combination of both valence and intensity (Anders et al., 2004; Kensinger & Corkin, 2004; Winston, Gottfried, Kilner, & Dolan, 2005).”

“merely unpleasant (Kensinger and Corkin 2004; Buchanan et al. 2006b).”

“Furthermore, both valence and arousal have been shown to have independent influences on memories for autobiographical events (Ford et al. 2012; Kensinger and Corkin 2004).”

“For example, although successful encoding activated the hippocampus regardless of emotion, the amygdala was activated only by successful encoding of arousing words (Kensinger & Corkin, 2004).”

“Evidence for amygdala–hippocampal interactions during affect processing has been provided by human neuroimaging studies which have shown concurrent, and in some cases correlated (Dolcos et al., 2004; Kensinger and Corkin, 2004), activation of the amygdala and hippocampus during the successful encoding of emotional inf…”

“…connectivity while valence-related enhancement was associated with interactions between medial temporal and prefrontal cortices (Kensinger, 2004; Kensinger and Corkin, 2004; LaBar and Cabeza, 2006), recent studies suggest that these two neural systems can interact to promote memory (Mickley…”

“Elevations in norepinephrine and cortisol are known to facilitate the functioning of the amygdala, which is critical for emotional memory processing (Cahill and McGaugh 1998; McGaugh 2000; Kensinger and Corkin 2004; Phelps 2004).”

“When activation in these regions was analyzed according to whether these items were subsequently remembered or forgotten, activation in the left inferior and dorsolateral prefrontal cortex was found to be correlated with memory for emotional items (Dolcos et al., 2004a; Kensinger & Corkin, 2004 ).”

“Kety (1970) suggested, four decades ago, that emotionally arousing experiences would activate the locus coeruleus (LC), producing release of norepinephrine in a variety of cortical and subcortical brain regions, to enhance synaptic plasticity and memory.”

“However, contrary to findings using ERPs or event related fMRI (e.g., Dolcos et al. 2004a, 2004b; Kensinger & Corkin, 2004), there was neither a main effect of subsequent memory nor an interaction with emotional valence.”

“…as well as non-clinical studies about the encoding and consolidation of deliberate (voluntary) memories (e.g. Wagner et al. 1998; Canli et al. 2000; Kensinger & Corkin, 2004 ; McGaugh, 2004 ; Francati et al. 2007; Roozendaal et al. 2008; Hughes & Shin, 2011), we predicted that encoding of…”

“However, ignoring the important debates has significant limitations, because a functional AC application can never be completely divorced from underlying emotion theory.”

“that the left prefrontal cortex contributes to superior encoding for emotional stimuli (Dolcos et al. 2004a; Kensinger and Corkin 2004).”

“It has also been suggested that neural systems associated with the encoding of emotional information may differ for emotional and nonemotional information ( Kensinger & Corkin, 2004 ).”

“Additional evidence for a pivotal role of the amygdala in emotional memory enhancement comes from several recent neuroimaging studies in healthy subjects (Alkire, Haier, Fallon, & Cahill, 1998; Cahill et al., 1996; Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000; Kensinger & Corkin, 2004 ).”

“Only a handful of studies to date have studied the simultaneous influence of arousal and valence on brain activity, and they have produced inconsistent results (Anders et al., 2004; Kensinger & Corkin, 2004; Small et al., 2003).”

“…have demonstrated that the enhancing effects of arousal on memory can occur just minutes after an event has occurred (Dolcos, LaBar, & Cabeza, 2004; Kensinger & Corkin, 2004; Talmi &McGarry, 2012; Mickley Steinmetz et al., 2012) and can be associated with greater activation of the amygdala,…”

“Since cognitive processes and affect regulation are subserved by overlapping neurobiological substrates, regions such as the prefrontal cortex contribute both to executive function/cognitive flexibility and mood regulation [41], while the anterior cingulate and the hippocampus play a role in emotional salience of expe…”

“Previous work has documented that emotional words derive their enhanced memorability from some combination of emotional arousal and semantic cohesion (Maratos et al., 2000; Talmi and Moscovitch, 2004). Talmi and Moscovitch (2004) varied the semantic cohesion and emotional arousal of to-be-remembered words and found th…”

“Amygdala activation at encoding correlates with subsequent memory for emotionally arousing items (Cahill et al., 1996; Hamann et al., 1999; Canli et al., 2000; Dolcos et al., 2004a; Kensinger and Corkin, 2004).”

“…similarly emphasize the role of arousal in emotional memory, but additionally propose that valence can facilitate memory in the absence of arousal (Kensinger & Corkin, 2003, 2004; LaBar & Cabeza, 2006), or that valence influences memory for perceptual details of the stimulus (Kensinger, 2009;…”

“Although this finding might suggest that distinct processes support the vivid remembering of emotional as compared with nonemotional items, it does appear that the amygdala exerts many of its r effects through interactions with the hippocampus proper (Packard, Cahill, & McGaugh, 1994)—a key player in the recollection…”

“Healthy young adults show a correspondence between amygdala activation and memory for arousing information but no link between amygdala activation and memory for nonarousing information (Kensinger & Corkin, 2004).”

“, 2006) measured an entirely different dimension of mood: activation rather than valence (Kensinger and Corkin, 2004).”

“A similar approach has been used in previous neuroimaging studies of emotion, often yielding activation in the VLPFC (35), particularly in the left hemisphere (36, 37).”

“The two main alternatives were arousal theory (see, e.g., Cahill & van Stegeren, 2003; Hamann, Ely, Grafton, & Kilts, 1999; Kensinger, & Corkin, 2004; Le Doux, 1996, pp. 206–208; Maratos, Allan, & Rugg, 2000; and Phelps et al., 1998) and the priority-binding assumption of binding theory (see, e.g., MacKay et al., 2004…”

“With evidence from functional neuroimaging studies (Dolcos et al., 2004; Kensinger and Corkin, 2004; Kilpatrick and Cahill, 2003; Richardson et al., 2004) suggesting that encoding of emotional episodes involves a functional coupling between the amygdala and hippocampus, it has been suggested that…”

“With BOLD-fMRI, such findings were extended to trial-by-trial variation in success of memory formation (Cahill, Uncapher, Kilpatrick, Alkire, & Turner, 2004; Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000; Kensinger & Corkin, 2004).”

“Across conditions, T1 words were matched for word length (5.13, 5.42, 5.74 and 5.21 letters for neutral, negative, positive, and taboo words respectively) and word frequency 3 (17.83, 23.72, 29.00 and 27.14 per million, respectively, Fs < 1; (Kuçera & Francis, 1967).”

“…effect of emotion is associated with increased activity in and interactions between emotion-based systems, involving AMY, and memory-based systems, involving medial-temporal lobe (MTL) and PFC regions (Dolcos et al., 2004; Kensinger and Corkin, 2004; see also Dolcos et al., 2011, 2012 for reviews).”

“…memory enhancements depend on two diVerent neural networks, with successful retrieval of negative arousing words supported by left amygdala and hippocampus and successful retrieval of negative nonarousing words supported by left inferior prefrontal cortex and hippocampus (Kensinger & Corkin, 2004).”

“…have shown that increased amygdala activation during stimulus viewing is strongly associated with enhanced memory for emotional scenes (Cahill et al. 1995, 1996; Hamann et al. 1999; Canli et al. 2000; Kilpatrick and Cahill 2003; Dolcos et al. 2004; Kensinger and Corkin 2004; Sharot et al. 2004).”

“Note that by collapsing across all event types, the resulting statistical map, and the ROIs extracted from it, was unbiased with respect to subsequent memory performance (Kensinger and Corkin, 2004).”

“2007), and (3) because EEM is more pronounced under low attention (Kensinger and Corkin 2004; Talmi et al. 2007), as replicated in the present study.”