Interaction between the Amygdala and the Medial Temporal Lobe Memory System Predicts Better Memory for Emotional Events

“(Brewer et al., 1998; Davachi and Wagner, 2002; Kirch- MTL regions. hoff et al., 2000; Otten et al., 2001; Otten and Rugg, 2001; Strange et al., 2002; Wagner et al., 1998;”

“…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).”

“Enhanced retention was seen with intra-amygdaloid injections of bicuculline (Dickinson et al. 1993), and agonists of -adrenergic (Ferry and McGaugh 1999; Hatfield and McGaugh 1999) and muscarinic (Salinas et al. 1997) receptors.”

“Other human imaging studies suggest that interactions between the amygdala and the anterior hippocampus are crucial for emotional memory formation (Dolcos et al., 2004; Richardson et al., 2004).”

“In one of these studies (Dolcos et al., 2004), however, when participants were re-exposed to these same stimuli during recognition testing manymonths later, a change in the profile of activation occurred (Dolcos et al.”

“…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).”

“…cingulate cortex, Ht: hypothalamus, PAG: periaqueductal gray matter, Str: striatum, MC: motor cortices. amygdalar modulation of hippocampal function in Dolcos et al., 2004b; a similar modulation by VMPFC is probable due to its profuse outputs to the hippocampal complex: Cavada et al., 2000).”

“Amygdala recruitment during emotional arousal is proposed to modulate other medial temporal lobe (MTL) structures to facilitate encoding and consolidation (McGaugh 2000; Dolcos et al. 2004).”

“2001b, 2004), and studies of emotion and memory have linked amygdala activation at encoding with subsequent EEM (e.g., Canli et al. 2000, 2002; Cahill et al. 2001, 2004b; Dolcos et al. 2004; Kensinger and Corkin, 2004).”

“Similarly, in humans, the anterior hippocampus has been reliably associated with the successful encoding of motivationally relevant memoranda compared with neutral memoranda (Dolcos et al., 2004; Adcock et al., 2006; Murty et al., 2010; Poppenk et al., 2013).”

“This strategy was chosen in order to minimise differences in voluntary attention, which may complicate the interpretation of subsequent memory effects (compare Dolcos et al., 2004a).”

“Animal studies (e.g., Nakao et al. 2004) and recent functional MRI studies (e.g., Dolcos et al. 2004; Strange and Dolan 2004) further reported a modulating role for hippocampus in processing of emotional memory interacting with amygdala.”

“Overall, cross-species evidence strongly supports the notion that the amygdala influences hippocampal storage by providing information about the emotional context (Dolcos et al., 2004; McGaugh, 2004).”

“…regions, in successful encoding of emotionally arousing information (e.g., Hamann et al., 1999; Canli et al., 2000; Kilpatrick and Cahill, 2003; Dolcos et al., 2004b; Kensinger and Corkin, 2004; Richardson et al., 2004; Kensinger and Schacter, 2006a; Sergerie et al., 2006; Ritchey et al.,…”

“…that emotional arousal will have different effects on these distinct memory systems (Jacobs and Nadel, 1985, 1998; Brewin et al., 2010), also see (Dolcos et al., 2004; Sharot et al., 2004; Phelps and LeDoux, 2005; LaBar and Cabeza, 2006; Smith et al., 2006; Ritchey et al., 2011; Yonelinas and…”

“This process is subserved by medial temporal lobe structures and results in better encoding and retrieval (Dolcos et al., 2004).”

“…projection provided by SPM5. both hippocampus and amygdala may indicate that the interaction with friends induces spontaneously more retrieval of emotionally salient memories (Berntsen and Hall, 2004; Dolcos et al., 2004, 2005; Fink et al., 1996; Greenberg et al., 2005; Sugiura et al., 2006).”

“The emotional enhancement reflects primarily a modulating influence of the amygdala on hippocampal memory function (Akirav and RichterLevin 2002; Dolcos et al. 2004; Phelps 2004).”

“…processing and expression of positive affect may be guided disproportionately by dorsolateral (rather than ventrolateral) prefrontal regions (e.g., Dolcos et al., 2004b; Kensinger & Schacter, 2006) and by left-lateralized prefrontal regions (for review, see Davidson & Irwin, 1999; for discussion,…”

“The right middle temporal gyrus has been found to be activated in both emotional processing and encoding tasks (Critchley et al., 2000; Dolcos et al., 2004; Olson et al., 2007), and the group results from the current study also indicate widespread activation in the temporal lobes associated with…”

“These previous studies have traditionally used encoding tasks consisting of simple valence ratings (e.g., Dolcos et al., 2004a, 2004b) or binary decisions about the content of the stimulus (e.g., Ritchey et al., 2008; Kensinger & Corkin, 2004).”

“In a general sample of recurrent involuntary memories, we therefore predict a high frequency of recent events (Rubin & Wenzel, 1996), emotionally intense (arousing) events (e.g., Dolcos, LaBar, & Cabeza, 2004, 2005; McGaugh, 2003; Thompson et al., 1996), emotionally positive events (Walker et al., 2003), and positive…”

“In humans, enhanced connectivity between amygdala and (para) hippocampal regions has been shown during formation (Dolcos et al. 2004) and retrieval (Smith et al.”

“…of traumatic memories (Kaspi et al., 1995; Harvey et al., 1998; McNally, 2006), have been linked to dysfunctions of the basic MTL-based mechanism (Hayes et al., 2011) identified in healthy participants as being responsible for the memory-enhancing effect of emotion (Dolcos et al., 2004b).”

“The acute stage of ayahuasca has been assimilated to a controlled exposure to autobiographical material (Domínguez-Clavé et al., 2016).”

“Evidence from functional neuroimaging studies in humans are actually consistent with this idea (Dolcos & Denkova, 2008; Dolcos et al., 2011; Dolcos et al., 2004b, 2005).”

“A left amygdala activation during encoding should also be observed in the case of emotional pictures, such as those used in previous studies (Dolcos et al., 2004), or other type of complex stimuli that may require cognitive and/or linguist processing (Hariri et al., 2002).”

“Furthermore, several studies in healthy humans have demonstrated coactivation of the amygdala and regions in the medial temporal lobe, such as the hippocampus, the entorhinal cortex, parahippocampal cortex, and perirhinal cortex (Hamann et al., 1999; Dolcos et al., 2004; Kensinger and Corkin, 2004; Ritchey et al., 200…”

“Emotionally arousing events are better remembered than emotionally neutral ones (Atienza & Cantero 2008; Canli et al. 2000; Dolcos et al. 2004; Kensinger 2004; Sharot et al. 2004).”

“Thus, it is possible that lower memory scores for negative faces in older adults could be due to less intense responses to these stimuli in the amygdala, which would reduce the influence of amygdala activity on other medial temporal lobe structures that is thought to underlie memory enhancement for negative emotional…”

“…a similar amygdala response as young adults when perceiving novel fearful faces compared to familiar neutral faces (Wright et al., 2008), and young adults may show frontal activation during encoding of emotional information (Dolcos et al., 2004; Kensinger and Corkin, 2004; Sergerie et al, 2005).”

“In controls , high confidence memory responses are typically more accurate for arousing vs. neutral material, an effect linked to amygdala activation at encoding (Canli et al., 2000; Dolcos et al., 2004).”

“Although previous functional neuroimaging studies have investigated the role of the amygdala on emotional facial expression (Breiter et al., 1996; Keightley, Chiew, Winocur, & Grady, 2007; Morris et al., 1996; Phillips et al., 1998; Winston, O’Doherty, & Dolan, 2003) or emotional memory ( Dolcos, LaBar, & Cabeza, 2004…”

“All participants gave informed consent to a protocol approved by the Institutional Review Board of Tohoku University School of Medicine.”

“…possible explanation for the observed activity is that the socially appropriate conditions represent emotionally charged personally-relevant autobiographical events which tend to activate the hippocampus (Burgess et al., 2001; Dolcos et al., 2004; Maguire et al., 2000; Maguire and Mummery, 1999).”

“Of particular interest is the AG's involvement in processing of emotionally relevant stimuli and encoding of emotionally salient memories (Dolcos et al., 2004; Kensinger, 2009; LeDoux and Schiller, 2009; Murty et al., 2010; Sergerie et al., 2008; Shafer et al., 2012; Shafer and Dolcos, 2012).”

“Human imaging studies have revealed that during encoding, activation in the amygdala is predictive of emotional memory performance later on (Canli et al., 2000; Dolcos et al., 2004).”

“Critically, mixed-effects models revealed that valence significantly 141 predicted changes to memory-related HFA, and that this pattern varied with depression severity and brain region 142 (χ(15) = 40.”

“Our results mirror those from previous fMRI studies on negative emotions that also implicate temporal (51), prefrontal (53–56), frontal polar (57, 58), and parietal regions (54).”

“…hemisphere laterality and, to limit the number of comparisons, reduced the original 12 channels into six bi-lateral regions of interest by combining each channel with its corresponding channel on the opposite hemisphere, similar to techniques used in the fMRI literature (e.g., Dolcos et al. 2004).”

“This selectivity of memory is partly due to immediate effects of emotional arousal on attentional, sensory, and mnemonic processes (Davis and Whalen, 2001; Dolcos et al., 2004; Labar and Cabeza, 2006; Visser et al., 2013), but is further strengthened by preferential consolidation (McGaugh, 2000).”

“Moreover, work using PET and fMRI approaches has reported that, during emotionally influenced learning, amygdala activity not only correlates with enhanced memory but also with activity in hippocampal regions (Kilpatrick and Cahill, 2003; Dolcos et al., 2004, 2005).”

“The lack of difference between positive and negative memory estimates is therefore consistent with previous evidence suggesting that arousal, not valence, is the key factor determining why emotional items are often better remembered than neutral items (Dolcos et al., 2004; Dolcos et al., 2004; Dolcos et al., 2004, Ken…”

“Furthermore, amygdala–parahippocampal interactions have previously been associated with declarative memory encoding for emotionally arousing stim- uli and contexts (Dolcos et al., 2004; Alvarez et al., 2008; Ritchey et al., 2008; Rudy, 2009).”

“In both tests, participants were required to write to the utmost detail all the characteristics of the pictures they could remember, so that an outsider would be able to identify the pictures as distinctively recognizable with the information provided [Dolcos et al., 2004].”

“Lastly, abnormal hippocampal function (Corcoran and Maren, 2001) and reduced connectivity to the amygdala (Dolcos et al., 2004; McGaugh, 2004) may be associated impairments in contextual memory processing and the ability to inhibit intrusive memories (Shin et al., 2004a), although fi ndings have…”

“…in- teractions in memory processes in humans have mostly used long-term and working memory paradigms involving emotional stimuli (Canli et al., 2000; Dolcos et al., 2004; Richardson et al., 2004; LoPresti et al., 2008), suggesting that the amygdala is primarily involved in emotional processing.”

“…a voxel that is independently signiWcant in each and both contrasts (i.e., the joint probability) can be estimated by multiplying the probabilities for each contrast: .0707 £ .0707 D p < .005 (Allan et al., 2000; Cabeza et al., 2002; Dolcos et al., 2004; Liu et al., 2003; Nitschke et al., 2006).”

“The anterior hippocampus has been found to be especially important for emotional memory (Dolcos et al., 2004; Murty et al., 2010), associated with gist-like, or coarse, global, representations (Adolphs et al.”

“Moreover, emotionally arousing stimuli exert their beneficial effect on episodic memory by enhancing activity in both the amygdala and the medial temporal lobe memory system in the human brain (Dolcos et al., 2004).”