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Aversive memory formation in humans involves an amygdala-hippocampus phase code.

التفاصيل البيبلوغرافية
العنوان: Aversive memory formation in humans involves an amygdala-hippocampus phase code.
المؤلفون: Costa M; Laboratory for Clinical Neuroscience, Center for Biomedical Technology, Universidad Politécnica de Madrid, IdISSC, Madrid, Spain. manuela.costa@ctb.upm.es., Lozano-Soldevilla D; Laboratory for Clinical Neuroscience, Center for Biomedical Technology, Universidad Politécnica de Madrid, IdISSC, Madrid, Spain., Gil-Nagel A; Epilepsy Unit, Department of Neurology, Hospital Ruber Internacional, Madrid, Spain.; Fundación Iniciativa Para las Neurociencias (FINCE), Madrid, Spain., Toledano R; Epilepsy Unit, Department of Neurology, Hospital Ruber Internacional, Madrid, Spain.; Hospital Universitario Ramón y Cajal, Servicio de Neurología, Madrid, Spain., Oehrn CR; Department of Neurological Surgery, University of California, San Francisco, CA, USA., Kunz L; Department of Biomedical Engineering, Columbia University, New York, NY, USA., Yebra M; Laboratory for Clinical Neuroscience, Center for Biomedical Technology, Universidad Politécnica de Madrid, IdISSC, Madrid, Spain.; Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA, 90048, USA., Mendez-Bertolo C; Laboratory for Clinical Neuroscience, Center for Biomedical Technology, Universidad Politécnica de Madrid, IdISSC, Madrid, Spain.; Departamento de Psicología. Facultad de Ciencias de la Educación, Universidad de Cádiz, and Instituto de Investigación Biomédica de Cádiz (INIBICA), Cádiz, Spain., Stieglitz L; Department of Neurosurgery, University Hospital Zurich, University of Zurich, Zurich, Switzerland., Sarnthein J; Department of Neurosurgery, University Hospital Zurich, University of Zurich, Zurich, Switzerland., Axmacher N; Department of Neuropsychology, Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum, Universitaetsstrasse 150, 44801, Bochum, Germany., Moratti S; Laboratory for Clinical Neuroscience, Center for Biomedical Technology, Universidad Politécnica de Madrid, IdISSC, Madrid, Spain.; Department of Experimental Psychology, Complutense University of Madrid, Madrid, Spain., Strange BA; Laboratory for Clinical Neuroscience, Center for Biomedical Technology, Universidad Politécnica de Madrid, IdISSC, Madrid, Spain. bryan.strange@upm.es.; Department of Neuroimaging, Reina Sofia Centre for Alzheimer's Research, Madrid, Spain. bryan.strange@upm.es.
المصدر: Nature communications [Nat Commun] 2022 Oct 27; Vol. 13 (1), pp. 6403. Date of Electronic Publication: 2022 Oct 27.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Nature Pub. Group Country of Publication: England NLM ID: 101528555 Publication Model: Electronic Cited Medium: Internet ISSN: 2041-1723 (Electronic) Linking ISSN: 20411723 NLM ISO Abbreviation: Nat Commun Subsets: MEDLINE
أسماء مطبوعة: Original Publication: [London] : Nature Pub. Group
مواضيع طبية MeSH: Memory*/physiology , Amygdala*/physiology, Humans ; Hippocampus/physiology ; Emotions/physiology ; Mental Recall/physiology
مستخلص: Memory for aversive events is central to survival but can become maladaptive in psychiatric disorders. Memory enhancement for emotional events is thought to depend on amygdala modulation of hippocampal activity. However, the neural dynamics of amygdala-hippocampal communication during emotional memory encoding remain unknown. Using simultaneous intracranial recordings from both structures in human patients, here we show that successful emotional memory encoding depends on the amygdala theta phase to which hippocampal gamma activity and neuronal firing couple. The phase difference between subsequently remembered vs. not-remembered emotional stimuli translates to a time period that enables lagged coherence between amygdala and downstream hippocampal gamma. These results reveal a mechanism whereby amygdala theta phase coordinates transient amygdala -hippocampal gamma coherence to facilitate aversive memory encoding. Pacing of lagged gamma coherence via amygdala theta phase may represent a general mechanism through which the amygdala relays emotional content to distant brain regions to modulate other aspects of cognition, such as attention and decision-making.
(© 2022. The Author(s).)
References: Ressler, K. J. & Mayberg, H. S. Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic NIH Public Access Author Manuscript. Nat. Neurosci. 10, 1116–1124 (2007). (PMID: 17726478244403510.1038/nn1944)
Pitman, R. K. et al. Biological studies of post-traumatic stress disorder. Nat. Rev. Neurosci. 13, 769–787 (2012). (PMID: 23047775495115710.1038/nrn3339)
Bocchio, M., Nabavi, S. & Capogna, M. Synaptic plasticity, engrams, and network oscillations in amygdala circuits for storage and retrieval of emotional memories. Neuron, https://doi.org/10.1016/j.neuron.2017.03.022 (2017).
Paré, D. Role of the basolateral amygdala in memory consolidation. Prog. Neurobiol. 70, 409–420 (2003). (PMID: 1451169910.1016/S0301-0082(03)00104-7)
Kim, J. J. & Fanselow, M. S. Modality-specific retrograde amnesia of fear. Science 256, 675–677 (1992). (PMID: 158518310.1126/science.1585183)
Strange, B. A., Witter, M. P., Lein, E. S. & Moser, E. I. Functional organization of the hippocampal longitudinal axis. Nat. Rev. Neurosci. 15, 655–655 (2014). (PMID: 2523426410.1038/nrn3785)
Adolphs, R., Cahill, L., Schul, R. & Babinsky, R. Impaired declarative memory for emotional material following bilateral amygdala damage in humans. Learn. Mem. 4, 291–300 (1997). (PMID: 1045607010.1101/lm.4.3.291)
LaBar, K. S. & Cabeza, R. Cognitive neuroscience of emotional memory. Nat. Rev. Neurosci., https://doi.org/10.1038/nrn1825 (2006).
Strange, B. A., Hurlemann, R. & Dolan, R. J. An emotion-induced retrograde amnesia in humans is amygdala- and β-adrenergic-dependent. Proc. Natl. Acad. Sci., https://doi.org/10.1073/pnas.1635116100 (2003).
Dolcos, F., LaBar, K. S. & Cabeza, R. Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron, https://doi.org/10.1016/S0896-6273(04)00289-2 (2004).
Richardson, M. P., Strange, B. A. & Dolan, R. J. Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nat. Neurosci. 7, 278–285 (2004). (PMID: 1475836410.1038/nn1190)
Strange, B. A. & Dolan, R. J. β-Adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses. Proc. Natl. Acad. Sci. https://doi.org/10.1073/pnas.0404282101 (2004).
McGaugh, J. L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27, 1–28 (2004). (PMID: 1521732410.1146/annurev.neuro.27.070203.144157)
Phelps, E. A. & LeDoux, J. E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48, 175–187 (2005). (PMID: 1624239910.1016/j.neuron.2005.09.025)
Seidenbecher, T., Laxmi, T. R., Stork, O. & Pape, H.-C. Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301, 846–850 (2003). (PMID: 1290780610.1126/science.1085818)
Zheng, J. et al. Amygdala-hippocampal dynamics during salient information processing. Nat. Commun. 8, https://doi.org/10.1038/ncomms14413 (2017).
Yonelinas, A. P., Otten, L. J., Shaw, K. N. & Rugg, M. D. Separating the brain regions involved in recollection and familiarity in recognition memory. J. Neurosci. 25, 3002–3008 (2005). (PMID: 15772360672512910.1523/JNEUROSCI.5295-04.2005)
Ochsner, K. N. & Gross, J. J. The cognitive control of emotion. Trends Cogn Sci. 9, 242–249 (2005).
Bessette-Symons, B. A. The robustness of false memory for emotional pictures. Memory 26, 171–188 (2018). (PMID: 2862510310.1080/09658211.2017.1339091)
Riberto, M., Paz, R., Pobric, G. & Talmi, D. The neural representations of emotional experiences are more similar than those of neutral experiences. J. Neurosci. 42, 2772–2785 (2022). (PMID: 35165174897342410.1523/JNEUROSCI.1490-21.2022)
Bierbrauer, A., Fellner, M.-C., Heinen, R., Wolf, O. T. & Axmacher, N. The memory trace of a stressful episode. Curr. Biol. 31, 5204–5213. e5208 (2021). (PMID: 3465335910.1016/j.cub.2021.09.044)
Gallo, D. A., Foster, K. T. & Johnson, E. L. Elevated false recollection of emotional pictures in young and older adults. Psychol. aging 24, 981 (2009). (PMID: 20025411292288310.1037/a0017545)
Paz, R. & Pare, D. Physiological basis for emotional modulation of memory circuits by the amygdala. Curr. Opin. Neurobiol. 23, 381–386 (2013). (PMID: 23394774365290610.1016/j.conb.2013.01.008)
Taub, A. H., Perets, R., Kahana, E. & Paz, R. Oscillations synchronize amygdala-to-prefrontal primate circuits during aversive learning. Neuron 97, 291–298.e293 (2018). (PMID: 2929055310.1016/j.neuron.2017.11.042)
Rutishauser, U., Ross, I. B., Mamelak, A. N. & Schuman, E. M. Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464, 903–907 (2010). (PMID: 2033607110.1038/nature08860)
Rutishauser, U., Reddy, L., Mormann, F. & Sarnthein, J. The architecture of human memory: insights from human single-neuron recordings. J. Neurosci. 41, 883–890 (2021). (PMID: 33257323788027210.1523/JNEUROSCI.1648-20.2020)
Fedele, T. et al. The relation between neuronal firing, local field potentials and hemodynamic activity in the human amygdala in response to aversive dynamic visual stimuli. NeuroImage 213, https://doi.org/10.1016/j.neuroimage.2020.116705 (2020).
Kucewicz, M. T. et al. Electrical stimulation modulates high γ activity and human memory performance. Eneuro 5, ENEURO.0369-17.2018 (2018).
Tort, A. B. L., Komorowski, R., Eichenbaum, H. & Kopell, N. Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. J. Neurophysiol. 104, 1195–1210 (2010). (PMID: 20463205294120610.1152/jn.00106.2010)
Fell, J. & Axmacher, N. The role of phase synchronization in memory processes. Nat. Rev. Neurosci. 12, 105–118 (2011). (PMID: 2124878910.1038/nrn2979)
Hasselmo, M. E., Bodelón, C. & Wyble, B. P. A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput. 14, 793–817 (2002). (PMID: 1193696210.1162/089976602317318965)
Lisman, J. The theta/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus 15, 913–922 (2005). (PMID: 1616103510.1002/hipo.20121)
Maris, E. & Oostenveld, R. Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Methods 164, 177–190 (2007). (PMID: 1751743810.1016/j.jneumeth.2007.03.024)
Sassenhagen, J. & Draschkow, D. Cluster‐based permutation tests of MEG/EEG data do not establish significance of effect latency or location. Psychophysiology 56, e13335 (2019). (PMID: 3065717610.1111/psyp.13335)
Bass, D. I., Partain, K. N. & Manns, J. R. Event-specific enhancement of memory via brief electrical stimulation to the basolateral complex of the amygdala in rats. Behav. Neurosci. 126, 204 (2012). (PMID: 2214146710.1037/a0026462)
Bass, D. I., Nizam, Z. G., Partain, K. N., Wang, A. & Manns, J. R. Amygdala-mediated enhancement of memory for specific events depends on the hippocampus. Neurobiol. Learn. Mem. 107, 37–41 (2014). (PMID: 2421169910.1016/j.nlm.2013.10.020)
Ahlgrim, N. S. & Manns, J. R. Optogenetic stimulation of the basolateral amygdala increased theta-modulated gamma oscillations in the hippocampus. Front. Behav. Neurosci. 13, 1–13 (2019). (PMID: 10.3389/fnbeh.2019.00087)
Bass, D. I. & Manns, J. R. Memory-enhancing amygdala stimulation elicits gamma synchrony in the Hippocampus. Behav. Neurosci. 129, 244–256 (2015). (PMID: 26030426445162310.1037/bne0000052)
Inman, C. S. et al. Direct electrical stimulation of the amygdala enhances declarative memory in humans. Proc. Natl. Acad. Sci. USA 115, 98–103 (2018). (PMID: 2925505410.1073/pnas.1714058114)
Lega, B., Burke, J., Jacobs, J. & Kahana, M. J. Slow-theta-to-gamma phase-amplitude coupling in human hippocampus supports the formation of new episodic memories. Cereb. Cortex 26, 268–278 (2016). (PMID: 2531634010.1093/cercor/bhu232)
Sederberg, P. B. et al. Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cereb. Cortex 17, 1190–1196 (2007). (PMID: 1683185810.1093/cercor/bhl030)
Titiz, A. S. et al. Theta-burst microstimulation in the human entorhinal area improves memory specificity. Elife 6, e29515 (2017). (PMID: 29063831565515510.7554/eLife.29515)
Miller, J. P. et al. Visual-spatial memory may be enhanced with theta burst deep brain stimulation of the fornix: a preliminary investigation with four cases. Brain 138, 1833–1842 (2015). (PMID: 2610609710.1093/brain/awv095)
Langevin, J.-P. et al. Deep brain stimulation of the basolateral amygdala for treatment-refractory posttraumatic stress disorder. Biological Psychiatry, https://doi.org/10.1016/j.biopsych.2015.09.003 (2016).
Bliss, T. V. & Collingridge, G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31–39 (1993). (PMID: 842149410.1038/361031a0)
Huerta, P. T. & Lisman, J. E. Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron 15, 1053–1063 (1995). (PMID: 757664910.1016/0896-6273(95)90094-2)
Hyman, J. M., Wyble, B. P., Goyal, V., Rossi, C. A. & Hasselmo, M. E. Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J. Neurosci. 23, 11725–11731 (2003). (PMID: 14684874674094310.1523/JNEUROSCI.23-37-11725.2003)
Bergado, J. A., Lucas, M. & Richter-Levin, G. Emotional tagging—a simple hypothesis in a complex reality. Prog. Neurobiol. 94, 64–76 (2011). (PMID: 2143537010.1016/j.pneurobio.2011.03.004)
Roozendaal, B. & McGaugh, J. L. Memory modulation. Behav. Neurosci. 125, 797 (2011). (PMID: 22122145323670110.1037/a0026187)
Dolan, R. J. Emotion, cognition, and behavior. Science 298, 1191–1194 (2002). (PMID: 1242436310.1126/science.1076358)
Méndez-Bértolo, C. et al. A fast pathway for fear in human amygdala. Nat. Neurosci. https://doi.org/10.1038/nn.4324 (2016).
Jha, A., Diehl, B., Scott, C., McEvoy, A. W. & Nachev, P. Reversed procrastination by focal disruption of medial frontal cortex. Curr. Biol. 26, 2893–2898 (2016). (PMID: 27773570510637110.1016/j.cub.2016.08.016)
Lang, P. J. International affective picture system (IAPS): Affective ratings of pictures and instruction manual. Technical report (2005).
Tulving, E. Elements of episodic memory. (1985).
Oostenveld, R., Fries, P., Maris, E. & Schoffelen, J. M. FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci. 2011, https://doi.org/10.1155/2011/156869 (2011).
Hamamé, C. M. et al. Functional selectivity in the human occipitotemporal cortex during natural vision: Evidence from combined intracranial EEG and eye-tracking. Neuroimage 95, 276–286 (2014). (PMID: 2465059510.1016/j.neuroimage.2014.03.025)
Shirhatti, V., Borthakur, A. & Ray, S. Effect of reference scheme on power and phase of the local field potential. Neural Comput. 28, 882–913 (2016). (PMID: 26942748711796210.1162/NECO_a_00827)
Spaak, E., Bonnefond, M., Maier, A., Leopold, D. A. & Jensen, O. Layer-specific entrainment of gamma-band neural activity by the alpha rhythm in monkey visual cortex. Curr. Biol. 22, 2313–2318 (2012). (PMID: 23159599352883410.1016/j.cub.2012.10.020)
Trongnetrpunya, A. et al. Assessing granger causality in electrophysiological data: removing the adverse effects of common signals via bipolar derivations. Front. Syst. Neurosci. 9, 189–189 (2016). (PMID: 26834583471899110.3389/fnsys.2015.00189)
Jacobs, J., Kobayashi, K. & Gotman, J. High-frequency changes during interictal spikes detected by time-frequency analysis. Clin. Neurophysiol. 122, 32–42 (2011). (PMID: 2059941810.1016/j.clinph.2010.05.033)
Cui, J., Xu, L., Bressler, S. L., Ding, M. & Liang, H. BSMART: A Matlab/C toolbox for analysis of multichannel neural time series. Neural Netw. 21, 1094–1104 (2008). (PMID: 18599267258569410.1016/j.neunet.2008.05.007)
Seth, A. K. A MATLAB toolbox for Granger causal connectivity analysis. J. Neurosci. Methods 186, 262–273 (2010). (PMID: 1996187610.1016/j.jneumeth.2009.11.020)
Kwiatkowski, D., Phillips, P. C. B., Schmidt, P. & Shin, Y. Testing the null hypothesis of stationarity against the alternative of a unit root. How sure are we that economic time series have a unit root? J. Econ. 54, 159–178 (1992). (PMID: 10.1016/0304-4076(92)90104-Y)
Buser, P. & Bancaud, J. Unilateral connections between amygdala and hippocampus in man. A study of epileptic patients with depth electrodes. Electroencephalogr. Clin. Neurophysiol. 55, 1–12 (1983). (PMID: 618529210.1016/0013-4694(83)90141-4)
Oehrn, C. R. et al. Neural communication patterns underlying conflict detection, resolution, and adaptation. J. Neurosci. 34, 10438–10452 (2014). (PMID: 25080602660827210.1523/JNEUROSCI.3099-13.2014)
Tort, A. B. L. et al. Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. Proc. Natl. Acad. Sci., https://doi.org/10.1073/pnas.0810524105 (2008).
Kullback, S. L. A. On Information and Sufficiency. Ann. Math. Stat. 22, 79–86 (1951). (PMID: 10.1214/aoms/1177729694)
VanRullen, R. How to evaluate phase differences between trial groups in ongoing electrophysiological signals. Front. Neurosci. 10, 426–426 (2016). (PMID: 27683543502170010.3389/fnins.2016.00426)
Axmacher, N. et al. Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc. Natl. Acad. Sci. USA 107, 3228–3233 (2010). (PMID: 20133762284028910.1073/pnas.0911531107)
de Cheveigné, A. & Nelken, I. Filters: when, why, and how (not) to use them. Neuron 102, 280–293 (2019). (PMID: 3099889910.1016/j.neuron.2019.02.039)
Widmann, A., Schröger, E. & Maess, B. Digital filter design for electrophysiological data–a practical approach. J. Neurosci. methods 250, 34–46 (2015). (PMID: 2512825710.1016/j.jneumeth.2014.08.002)
Chaure, F. J., Rey, H. G. & Quian Quiroga, R. A novel and fully automatic spike-sorting implementation with variable number of features. J. Neurophysiol. 120, 1859–1871 (2018). (PMID: 29995603623080310.1152/jn.00339.2018)
Kutter, E. F., Bostroem, J., Elger, C. E., Mormann, F. & Nieder, A. Single neurons in the human brain encode numbers. Neuron 100, 753–761. e754 (2018). (PMID: 3024488310.1016/j.neuron.2018.08.036)
Jacobs, J., Kahana, M. J., Ekstrom, A. D. & Fried, I. Brain oscillations control timing of single-neuron activity in humans. J. Neurosci. 27, 3839–3844 (2007). (PMID: 17409248667240010.1523/JNEUROSCI.4636-06.2007)
Berens, P. CircStat: a MATLAB toolbox for circular statistics. J. Stat. Softw. 31, 1–21 (2009). (PMID: 10.18637/jss.v031.i10)
تواريخ الأحداث: Date Created: 20221027 Date Completed: 20221031 Latest Revision: 20221223
رمز التحديث: 20231215
مُعرف محوري في PubMed: PMC9613775
DOI: 10.1038/s41467-022-33828-2
PMID: 36302909
قاعدة البيانات: MEDLINE
الوصف
تدمد:2041-1723
DOI:10.1038/s41467-022-33828-2