Direct electrical stimulation of the amygdala enhances declarative memory in humans

Inman, Cory S.; Manns, Joseph R.; Bijanki, Kelly R.; Bass, David I.; Hamann, Stephan; Fasano, Rebecca E.; Kovach, Christopher K.; Gross, Robert E.

doi:10.1073/pnas.1714058114

Cited by 144 publications

(119 citation statements)

References 55 publications

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“…Our results are in line with previous studies showing that AMY activity at encoding increases the likelihood of remembering emotional, but not neutral items 48,49 , even without a conscious emotional experience 50 . However, the current study is the first to show that AMY differentially contributes to memory for two distinct negative emotions, even after controlling for arousal level 51 .…”

Section: Differences In Memory Modulation By Disgust and Fearsupporting

confidence: 93%

Distinct medial-temporal lobe mechanisms of encoding and amygdala-mediated memory reinstatement for disgust and fear

Riegel

Wierzba

Wypych

et al. 2019

Preprint

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Many associative memory traces are charged with emotion that can either impair or enhance subsequent retrieval. Various factors may influence such emotion effects, including the nature of associations and type of emotions. We show that long-term recognition memory of very close verbal associations was enhanced for emotionally charged material, and these effects differed between two negative emotion categories matched for arousal level. Specifically, memory was better for word pairs related to disgust than word pairs related to fear. Furthermore, these two emotions distinctively modulated neural processes during encoding and its relationship with retrieval, regardless of arousal evoked by word pairs. Amygdala and perirhinal cortex activity were associated with enhanced memory for disgust-related unitizations, whereas better memory for fear-related unitizations engaged parahippocampal cortex and hippocampus. Finally, the magnitude of amygdala activation during encoding was related to the subsequent fidelity of hippocampal activity patterns during retrieval. These results show that dissociable neural pathways and reinstatement mechanisms are involved in associative memory for different emotion categories and that arousal alone cannot fully explain emotional influences on associative memory.individually control for the effects of valence and arousal dimensions. Most importantly, this paradigm enabled us to compare the encoding-retrieval similarity of brain activation patterns elicited across two different emotion categories and determine which brain regions promoted this measure of neural reinstatement.We found a memory enhancement effect due to emotion. Moreover, word pairs related to disgust were remembered better than word pairs related to fear, and this effect could not be explained by differences in arousal. We found distinctive neural pathways preferentially engaged in encoding modulation by disgust or fear. Specifically, the left AMY and left PRC were more activated during successful encoding of disgust-related unitized word pairs, whereas right PHC and HC were more activated for fear-related unitized word pairs, even when the level of arousal was regressed out from the analysis. Moreover, during successful encoding of disgust-compared to fearrelated word pairs, we observed an increase in functional connectivity between AMY, PRC and PHC. Finally, for disgusting compared to fearful word pairs, the left AMY encoding activation was found to be critical for the level of trial-by-trial encodingretrieval similarity of brain activation patterns.Altogether, the results show that behavioural and neuronal mechanisms of long-term associative memory can be differently modulated by basic emotion categories, over and above of valence and arousal dimensions. For the first time, we revealed that due to AMY and PRC engagement, disgust as opposed to fear has a strong influence on reinstatement and recognition memory of unitized word pairs, which is in line with its distinctive and perhaps evolutionary-driven role in memorizing ...

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Section: Differences In Memory Modulation By Disgust and Fearsupporting

confidence: 93%

Distinct medial-temporal lobe mechanisms of encoding and amygdala-mediated memory reinstatement for disgust and fear

Riegel

Wierzba

Wypych

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…Results predominantly show that applying electrical stimulation to the hippocampus and entorhinal cortex impairs memory (11,15) (with some exceptions (10)), providing evidence for causal role of these regions in mnemonic processing. This makes DBS ideal for studying cognitive enhancement and causal roles of deep cortical structures associated with memory (7--14, 16) and sensory processes (17,18) as well as for developing neuromodulation strategies to treat memory and motors disorders (19).…”

Section: Introductionmentioning

confidence: 99%

Stimulation of the posterior cingulate impairs episodic memory encoding

Natu

Lin

Burks

et al. 2018

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Significance Statement (120/120 words)Cognitive impairment and memory loss are critical public health challenges. Deep brain stimulation (DBS) is a promising tool for developing strategies to ameliorate memory disorders by targeting brain regions involved in mnemonic processing. Using DBS, our study sheds light on the lesser--known role of the posterior cingulate cortex (PCC) in memory encoding. Stimulating the PCC during encoding impairs subsequent recall memory. The degree of impairment is predicted by stimulation--induced hippocampal gamma oscillations and functional connectivity between PCC and hippocampus. Our findings provide the first causal evidence implicating PCC in memory encoding and highlight the PCC as a favorable target for neuromodulation strategies, using a--priori connectivity measures to predict stimulation effects. This has significant implications for developing therapies for memory diseases. Abstract (250/250)Neuroimaging experiments implicate the posterior cingulate cortex (PCC) in episodic memory processing, making it a potential target for responsive neuromodulation strategies outside of the hippocampal network. However, causal evidence for the role PCC plays in memory encoding is lacking. In patients undergoing seizure mapping, we investigated functional properties of the PCC using deep brain stimulation (DBS) and stereotactic electroencephalography (stereo EEG). These techniques allow precise targeting of deep cortical structures including the PCC, and simultaneous acquisition of oscillatory recordings from neighboring regions such as the hippocampus. We used a free recall experiment in which PCC was stimulated during item encoding period of half of the study lists, while no stimulation was 2 applied during encoding period of the remaining lists. We evaluated if stimulation affected memory and/or modulated hippocampal activity. Results revealed four main findings. (i) Stimulation during encoding impaired memory for early items on the study lists. (ii) Stimulation increased hippocampal gamma band power. (iii) Stimulation--induced gamma power predicted memory impairment. (iv) Functional connectivity between the hippocampus and PCC predicted the degree of stimulation effect on memory. Our findings offer the first causal evidence implicating the PCC in episodic memory encoding.Importantly, results highlight that stimulation targeted outside of the temporal lobe can modulate hippocampal activity with implications on behavior. Furthermore, a--priori measures of connectivity between brain regions within a functional network can be informative in predicting behavioral effects of stimulation. Our findings have significant implications for developing therapies to treat diseases of memory loss and cognitive impairment using DBS.

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“…the subject perceived faces more positively when stimulation was applied as compared when it was off (Bijanki et al 2014). Second, Inman et al reported in fourteen patients that stimulation of the amygdala during perception of neutral stimuli enhanced subsequent delayed memory for the stimuli (Inman et al 2018). The investigators postulated that stimulation induced interactions between the amygdala, hippocampus, and entorhinal cortex.…”

Section: Introductionmentioning

confidence: 99%

Modulation of emotion perception and memory via sub-threshold amygdala stimulation in humans

Song

et al. 2019

Preprint

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A common human experience is noticing that emotional life events are more vividly remembered than dull ones. Studies show that the amygdala plays a central role in such emotionally driven enhancement of memory. With this in mind, we investigated the effect of electrical brain stimulation of the left human amygdala on performance on an emotional perception and emotional memory task. We randomly applied sub-threshold 50 Hz stimulation to the left amygdala in 10 patients (5 female and 5 male) with intracranial electrodes during the encoding portion of an emotional valence perception and emotional memory task. We found that amygdala stimulation did not affect reported valence for neutral stimuli (non-stimulated group average valence 5.34, stimulated 5.38, p=0.68) but it did affect positively (non-stimulated group average valence 7.31, stimulated 6.70, p=0.004) and negatively (non-stimulated group average valence 2.79, stimulated 3.55, p=0.0002) valenced stimuli in effect reporting both valence categories as more neutral. Furthermore, we found that stimulation did not significantly disrupt memory for neutral stimuli (68% vs. 61% correctly remembered p=0.48) or positive stimuli (87% vs. 70% correct, trend towards significant difference p=0.09) but did for negative stimuli (83% vs. 67% correct, p=0.03). These results suggest that electrical brain stimulation by our parameters likely reversibly inhibits amygdala function disrupting neural networks responsible for emotional perception and memory. This effect may have clinical implications in treatment of certain neuropsychiatric disorders, such as emotional dysregulation and post-traumatic stress disorder. Statement of significanceThe current study builds and expands on extensive prior research into the function of the human amygdala. It provides the first systematic description in humans of a cognitive change brought both studies, amygdala stimulation produced effects on emotional valence and memory without inducing subjective emotional states in these patients.Building upon prior work cited above, the objective in this study was to further investigate the effects of amygdala stimulation on performance on an emotional perception and emotional memory task. Our central hypothesis -as gained from previous studies discussed above -was that stimulation of the amygdala would lead to changes in the perceived emotional intensity of stimuli and in turn lead to an effect on delayed recognition, i.e. emotional memory. Materials and Methods.Patients. Consecutive patients at Dartmouth-Hitchcock Medical Center undergoing intracranial EEG evaluation for epilepsy surgery were recruited for to participate in the study. We included both female and male patients who were willing to participate in research, who were able to consent, who had electrodes which localized to the left amygdala on preliminary co-registration, and who had pre-surgical FSIQ greater than 70.Electrodes. Electrodes used for the study were either Ad-Tech SEEG electrodes 0.86 mm diameter with 10 contacts per electrode or...

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Direct electrical stimulation of the amygdala enhances declarative memory in humans

Cited by 144 publications

References 55 publications

Distinct medial-temporal lobe mechanisms of encoding and amygdala-mediated memory reinstatement for disgust and fear

Distinct medial-temporal lobe mechanisms of encoding and amygdala-mediated memory reinstatement for disgust and fear

Stimulation of the posterior cingulate impairs episodic memory encoding

Modulation of emotion perception and memory via sub-threshold amygdala stimulation in humans

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