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26.03.2020 | Original Article - Functional Neurosurgery - Epilepsy

Amygdalar and hippocampal beta rhythm synchrony during human fear memory retrieval

verfasst von: Di Wang, Zhaoyang Huang, Liankun Ren, Jing Liu, Xueyuan Wang, Tao Yu, Minjing Hu, Xueming Wang, Jialin Du, Duanyu Ni, Xi Zhang, Runshi Gao, Liang Qiao, Yuping Wang

Erschienen in: Acta Neurochirurgica | Ausgabe 10/2020

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Abstract

Background

Fear, as one of the basic emotions, is crucial in helping humans to perceive hazards and adapt to social activities. Clinically, fear memory is also involved in a wide spectrum of psychiatric disorders. A better understanding of the neural mechanisms of fear thereby has both neuroscientific and clinical significance. In recent years, data from animal models have demonstrated the key role of the amygdala-hippocampal circuit in the development of fear. However, the neural processing of fear memory remains unclear in humans, which is mainly due to the limitation of indirect measure of neural activity.

Methods

Herein, we investigated fear memory by direct intracranial recordings from 8 intractable epilepsy patients with depth electrodes in both the hippocampus and ipsilateral amygdala. All the patients were subjected to a well-established Pavlovian fear memory paradigm consisted of the familiarization task, conditioning task, and retrieval task, respectively. Simultaneous local field potentials from the hippocampus and amygdala were recorded during different stages. The oscillatory activities from the amygdala and hippocampus were analyzed during fear memory retrieval compared with neutral stages.

Results

Consistent with previous rodent studies, our results showed that the amygdala was involved in fear memory retrieval rather than neutral memory retrieval, while the hippocampus was involved both in fear memory retrieval and neutral memory retrieval. In particular, we found that there was an enhanced synchronized activity between the amygdala and hippocampus at beta frequencies (14–30 Hz), which suggested that enhanced synchronized activity at beta frequencies between the amygdala and hippocampus play a pivotal role during retrieval of fear memory in human.

Conclusions

Thus, our observation that the amygdala-hippocampal system contributing to fear memory retrieval in human with frequency-depended specificity has provided new insights into the mechanism of fear and have potential clinical relevance.

Antzoulatos EG, Miller EK (2014) Increases in functional connectivity between prefrontal cortex and striatum during category learning. Neuron 83:216–225. https://doi.org/10.1016/j.neuron.2014.05.005CrossRefPubMedPubMedCentral

Botterill JJ, Fournier NM, Guskjolen AJ, Lussier AL, Marks WN, Kalynchuk LE (2014) Amygdala kindling disrupts trace and delay fear conditioning with parallel changes in Fos protein expression throughout the limbic brain. Neuroscience 265:158–171. https://doi.org/10.1016/j.neuroscience.2014.01.040CrossRefPubMed

Bruns A (2004) Fourier-, Hilbert- and wavelet-based signal analysis: are they really different approaches? J Neurosci Methods 137:321–332. https://doi.org/10.1016/j.jneumeth.2004.03.002CrossRefPubMed

Buschman TJ, Denovellis EL, Diogo C, Bullock D, Miller EK (2012) Synchronous oscillatory neural ensembles for rules in the prefrontal cortex. Neuron 76:838–846. https://doi.org/10.1016/j.neuron.2012.09.029CrossRefPubMedPubMedCentral

Chan D, Kent EC, Berry DI, Huybers P (2019) Correcting datasets leads to more homogeneous early-twentieth-century sea surface warming. Nature 571:393–397. https://doi.org/10.1038/s41586-019-1349-2CrossRefPubMed

Claerbout JF (1985) Fundamentals of geophysical data processing with applications to petroleum prospecting. Blackwell, Oxford, pp 59–62

de Voogd LD, Fernández G, Hermans EJ (2016) Awake reactivation of emotional memory traces through hippocampal–neocortical interactions. Neuroimage 134:563–572. https://doi.org/10.1016/j.neuroimage.2016.04.026CrossRefPubMed

de Voogd LD, Klumpers F, Fernandez G, Hermans EJ (2017) Intrinsic functional connectivity between amygdala and hippocampus during rest predicts enhanced memory under stress. Psychoneuroendocrinology 75:192–202. https://doi.org/10.1016/j.psyneuen.2016.11.002CrossRefPubMed

Desmedt A, Marighetto A, Piazza P-V (2015) Abnormal fear memory as a model for posttraumatic stress disorder. Biol Psychiatry 78:290–297. https://doi.org/10.1016/j.biopsych.2015.06.017CrossRefPubMed

10.

Desmedt A, Marighetto A, Richter-Levin G, Calandreau L (2015) Adaptive emotional memory: the key hippocampal-amygdalar interaction. Stress 18:297–308CrossRefPubMed

11.

Dolcos F, LaBar KS, Cabeza R (2005) Remembering one year later: role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. Proc Natl Acad Sci U S A 102:2626–2631. https://doi.org/10.1073/pnas.0409848102CrossRefPubMedPubMedCentral

12.

Duits P, Cath DC, Lissek S, Hox JJ, Hamm AO, Engelhard IM, van den Hout MA, Baas JM (2015) Updated meta-analysis of classical fear conditioning in the anxiety disorders. Depress Anxiety 32:239–253. https://doi.org/10.1002/da.22353CrossRefPubMed

13.

Dymond S, Dunsmoor JE, Vervliet B, Roche B, Hermans D (2015) Fear generalization in humans: systematic review and implications for anxiety disorder research. Behav Ther 46:561–582. https://doi.org/10.1016/j.beth.2014.10.001CrossRefPubMed

14.

Edwards M, Stewart E, Palermo R, Lah S (2017) Facial emotion perception in patients with epilepsy: a systematic review with meta-analysis. Neurosci Biobehav Rev 83:212–225. https://doi.org/10.1016/j.neubiorev.2017.10.013CrossRefPubMed

15.

Faltermeier R, Proescholdt MA, Bele S, Brawanski A (2015) Windowed multitaper correlation analysis of multimodal brain monitoring parameters. Computational and mathematical methods in medicine 2015:124325. https://doi.org/10.1155/2015/124325CrossRefPubMedPubMedCentral

16.

Ghosh S, Laxmi TR, Chattarji S (2013) Functional connectivity from the amygdala to the hippocampus grows stronger after stress. J Neurosci 33:7234–7244. https://doi.org/10.1523/jneurosci.0638-13.2013CrossRefPubMedPubMedCentral

17.

Hamann SB, Ely TD, Grafton ST, Kilts CD (1999) Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nat Neurosci 2:289–293. https://doi.org/10.1038/6404CrossRefPubMed

18.

Hauner KK, Howard JD, Zelano C, Gottfried JA (2013) Stimulus-specific enhancement of fear extinction during slow-wave sleep. Nat Neurosci 16:1553–1555. https://doi.org/10.1038/nn.3527CrossRefPubMedPubMedCentral

19.

Holland AC, Kensinger EA (2010) Emotion and autobiographical memory. Phys Life Rev 7:88–131. https://doi.org/10.1016/j.plrev.2010.01.006CrossRefPubMedPubMedCentral

20.

Honkanen R, Rouhinen S, Wang SH, Palva JM, Palva S (2015) Gamma oscillations underlie the maintenance of feature-specific information and the contents of visual working memory. Cereb Cortex 25:3788–3801. https://doi.org/10.1093/cercor/bhu263CrossRefPubMed

21.

Horn A, Kuhn AA (2015) Lead-DBS: a toolbox for deep brain stimulation electrode localizations and visualizations. Neuroimage 107:127–135. https://doi.org/10.1016/j.neuroimage.2014.12.002CrossRefPubMed

22.

Janak PH, Tye KM (2015) From circuits to behaviour in the amygdala. Nature 517:284–292. https://doi.org/10.1038/nature14188CrossRefPubMedPubMedCentral

23.

Ji J, Maren S (2007) Hippocampal involvement in contextual modulation of fear extinction. Hippocampus 17:749–758. https://doi.org/10.1002/hipo.20331CrossRefPubMed

24.

Kilpatrick L, Cahill L (2003) Amygdala modulation of parahippocampal and frontal regions during emotionally influenced memory storage. Neuroimage 20:2091–2099. https://doi.org/10.1016/S1053-8119(03)00478-6CrossRefPubMed

25.

Kirkby LA, Luongo FJ, Lee MB, Nahum M, Van Vleet TM, Rao VR, Dawes HE, Chang EF, Sohal VS (2018) An amygdala-hippocampus subnetwork that encodes variation in human mood. Cell 175:1688–1700. https://doi.org/10.1016/j.cell.2018.10.005CrossRefPubMed

26.

Kornblith S, Buschman TJ, Miller EK (2016) Stimulus load and oscillatory activity in higher cortex. Cereb Cortex 26:3772–3784. https://doi.org/10.1093/cercor/bhv182CrossRefPubMedPubMedCentral

27.

LeDoux J (2012) Rethinking the emotional brain. Neuron 73:653–676. https://doi.org/10.1016/j.neuron.2012.02.004CrossRefPubMedPubMedCentral

28.

LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184CrossRefPubMed

29.

Lesting J, Geiger M, Narayanan RT, Pape HC, Seidenbecher T (2011) Impaired extinction of fear and maintained amygdala-hippocampal theta synchrony in a mouse model of temporal lobe epilepsy. Epilepsia 52:337–346. https://doi.org/10.1111/j.1528-1167.2010.02758.xCrossRefPubMed

30.

Li W, Howard JD, Parrish TB, Gottfried JA (2008) Aversive learning enhances perceptual and cortical discrimination of indiscriminable odor cues. Science 319:1842–1845. https://doi.org/10.1126/science.1152837CrossRefPubMedPubMedCentral

31.

Lundqvist M, Rose J, Herman P, Brincat SL, Buschman TJ, Miller EK (2016) Gamma and beta bursts underlie working memory. Neuron 90:152–164. https://doi.org/10.1016/j.neuron.2016.02.028CrossRefPubMedPubMedCentral

32.

McGaugh JL (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27:1–28. https://doi.org/10.1146/annurev.neuro.27.070203.144157CrossRefPubMed

33.

Michalareas G, Vezoli J, van Pelt S, Schoffelen JM, Kennedy H, Fries P (2016) Alpha-beta and gamma rhythms subserve feedback and feedforward influences among human visual cortical areas. Neuron 89:384–397. https://doi.org/10.1016/j.neuron.2015.12.018CrossRefPubMedPubMedCentral

34.

Moita MA, Rosis S, Zhou Y, LeDoux JE, Blair HT (2003) Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37:485–497CrossRefPubMed

35.

Murray RJ, Brosch T, Sander D (2014) The functional profile of the human amygdala in affective processing: insights from intracranial recordings. Cortex 60:10–33. https://doi.org/10.1016/j.cortex.2014.06.010CrossRefPubMed

36.

Paré D, Collins DR, Pelletier JG (2002) Amygdala oscillations and the consolidation of emotional memories. Trends Cogn Sci 6:306–314CrossRefPubMed

37.

Rabinak CA, Mori S, Lyons M, Milad MR, Phan KL (2017) Acquisition of CS-US contingencies during Pavlovian fear conditioning and extinction in social anxiety disorder and posttraumatic stress disorder. J Affect Disord 207:76–85. https://doi.org/10.1016/j.jad.2016.09.018CrossRefPubMed

38.

Richter-Levin G (2016) The amygdala, the hippocampus, and emotional modulation of memory. Neuroscientist 10:31–39. https://doi.org/10.1177/1073858403259955CrossRef

39.

Ritchey M, Dolcos F, Cabeza R (2008) Role of amygdala connectivity in the persistence of emotional memories over time: an event-related FMRI investigation. Cereb Cortex 18:2494–2504. https://doi.org/10.1093/cercor/bhm262CrossRefPubMedPubMedCentral

40.

Seidenbecher T, Laxmi TR, Stork O, Pape HC (2003) Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301:846–850. https://doi.org/10.1126/science.1085818CrossRefPubMed

41.

Staresina BP, Michelmann S, Bonnefond M, Jensen O, Axmacher N, Fell J (2016) Hippocampal pattern completion is linked to gamma power increases and alpha power decreases during recollection. Elife 5. https://doi.org/10.7554/eLife.17397

42.

Tinoco-Gonzalez D, Fullana MA, Torrents-Rodas D, Bonillo A, Vervliet B, Blasco MJ, Farre M, Torrubia R (2015) Conditioned fear acquisition and generalization in generalized anxiety disorder. Behav Ther 46:627–639. https://doi.org/10.1016/j.beth.2014.12.004CrossRefPubMed

43.

Tort ABL, Komorowski RW, Manns JR, Kopell NJ, Eichenbaum H (2009) Theta-gamma coupling increases during the learning of item-context associations. Proc Natl Acad Sci 106:20942–20947. https://doi.org/10.1073/pnas.0911331106CrossRefPubMedPubMedCentral

44.

van Vugt MK, Sederberg PB, Kahana MJ (2007) Comparison of spectral analysis methods for characterizing brain oscillations. J Neurosci Methods 162:49–63. https://doi.org/10.1016/j.jneumeth.2006.12.004CrossRefPubMed

45.

Waldhauser GT, Johansson M, Hanslmayr S (2012) Alpha/beta oscillations indicate inhibition of interfering visual memories. J Neurosci 32:1953–1961. https://doi.org/10.1523/jneurosci.4201-11.2012CrossRefPubMedPubMedCentral

46.

Zheng J, Anderson KL, Leal SL, Shestyuk A, Gulsen G, Mnatsakanyan L, Vadera S, Hsu FP, Yassa MA, Knight RT, Lin JJ (2017) Amygdala-hippocampal dynamics during salient information processing. Nat Commun 8:14413. https://doi.org/10.1038/ncomms14413CrossRefPubMedPubMedCentral

Titel: Amygdalar and hippocampal beta rhythm synchrony during human fear memory retrieval
verfasst von: Di Wang
Zhaoyang Huang
Liankun Ren
Jing Liu
Xueyuan Wang
Tao Yu
Minjing Hu
Xueming Wang
Jialin Du
Duanyu Ni
Xi Zhang
Runshi Gao
Liang Qiao
Yuping Wang
Publikationsdatum: 26.03.2020
Verlag: Springer Vienna
Erschienen in: Acta Neurochirurgica / Ausgabe 10/2020
Print ISSN: 0001-6268
Elektronische ISSN: 0942-0940
DOI: https://doi.org/10.1007/s00701-020-04276-y

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Amygdalar and hippocampal beta rhythm synchrony during human fear memory retrieval