Aversive memory formation in humans involves an amygdala-hippocampus phase code.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
27 10 2022
27 10 2022
Historique:
received:
09
12
2021
accepted:
05
10
2022
entrez:
27
10
2022
pubmed:
28
10
2022
medline:
1
11
2022
Statut:
epublish
Résumé
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.
Identifiants
pubmed: 36302909
doi: 10.1038/s41467-022-33828-2
pii: 10.1038/s41467-022-33828-2
pmc: PMC9613775
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
6403Informations de copyright
© 2022. The Author(s).
Références
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).
pubmed: 17726478
pmcid: 2444035
doi: 10.1038/nn1944
Pitman, R. K. et al. Biological studies of post-traumatic stress disorder. Nat. Rev. Neurosci. 13, 769–787 (2012).
pubmed: 23047775
pmcid: 4951157
doi: 10.1038/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).
pubmed: 14511699
doi: 10.1016/S0301-0082(03)00104-7
Kim, J. J. & Fanselow, M. S. Modality-specific retrograde amnesia of fear. Science 256, 675–677 (1992).
pubmed: 1585183
doi: 10.1126/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).
pubmed: 25234264
doi: 10.1038/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).
pubmed: 10456070
doi: 10.1101/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).
pubmed: 14758364
doi: 10.1038/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).
pubmed: 15217324
doi: 10.1146/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).
pubmed: 16242399
doi: 10.1016/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).
pubmed: 12907806
doi: 10.1126/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).
pubmed: 15772360
pmcid: 6725129
doi: 10.1523/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).
pubmed: 28625103
doi: 10.1080/09658211.2017.1339091
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).
pubmed: 35165174
pmcid: 8973424
doi: 10.1523/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).
pubmed: 34653359
doi: 10.1016/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).
pubmed: 20025411
pmcid: 2922883
doi: 10.1037/a0017545
Paz, R. & Pare, D. Physiological basis for emotional modulation of memory circuits by the amygdala. Curr. Opin. Neurobiol. 23, 381–386 (2013).
pubmed: 23394774
pmcid: 3652906
doi: 10.1016/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).
pubmed: 29290553
doi: 10.1016/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).
pubmed: 20336071
doi: 10.1038/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).
pubmed: 33257323
pmcid: 7880272
doi: 10.1523/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).
pubmed: 20463205
pmcid: 2941206
doi: 10.1152/jn.00106.2010
Fell, J. & Axmacher, N. The role of phase synchronization in memory processes. Nat. Rev. Neurosci. 12, 105–118 (2011).
pubmed: 21248789
doi: 10.1038/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).
pubmed: 11936962
doi: 10.1162/089976602317318965
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).
pubmed: 16161035
doi: 10.1002/hipo.20121
Maris, E. & Oostenveld, R. Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Methods 164, 177–190 (2007).
pubmed: 17517438
doi: 10.1016/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).
pubmed: 30657176
doi: 10.1111/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).
pubmed: 22141467
doi: 10.1037/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).
pubmed: 24211699
doi: 10.1016/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).
doi: 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).
pubmed: 26030426
pmcid: 4451623
doi: 10.1037/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).
pubmed: 29255054
doi: 10.1073/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).
pubmed: 25316340
doi: 10.1093/cercor/bhu232
Sederberg, P. B. et al. Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cereb. Cortex 17, 1190–1196 (2007).
pubmed: 16831858
doi: 10.1093/cercor/bhl030
Titiz, A. S. et al. Theta-burst microstimulation in the human entorhinal area improves memory specificity. Elife 6, e29515 (2017).
pubmed: 29063831
pmcid: 5655155
doi: 10.7554/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).
pubmed: 26106097
doi: 10.1093/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).
pubmed: 8421494
doi: 10.1038/361031a0
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).
pubmed: 7576649
doi: 10.1016/0896-6273(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).
pubmed: 14684874
pmcid: 6740943
doi: 10.1523/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).
pubmed: 21435370
doi: 10.1016/j.pneurobio.2011.03.004
Roozendaal, B. & McGaugh, J. L. Memory modulation. Behav. Neurosci. 125, 797 (2011).
pubmed: 22122145
pmcid: 3236701
doi: 10.1037/a0026187
Dolan, R. J. Emotion, cognition, and behavior. Science 298, 1191–1194 (2002).
pubmed: 12424363
doi: 10.1126/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).
pubmed: 27773570
pmcid: 5106371
doi: 10.1016/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).
pubmed: 24650595
doi: 10.1016/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).
pubmed: 26942748
pmcid: 7117962
doi: 10.1162/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).
pubmed: 23159599
pmcid: 3528834
doi: 10.1016/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).
pubmed: 26834583
pmcid: 4718991
doi: 10.3389/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).
pubmed: 20599418
doi: 10.1016/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).
pubmed: 18599267
pmcid: 2585694
doi: 10.1016/j.neunet.2008.05.007
Seth, A. K. A MATLAB toolbox for Granger causal connectivity analysis. J. Neurosci. Methods 186, 262–273 (2010).
pubmed: 19961876
doi: 10.1016/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).
doi: 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).
pubmed: 6185292
doi: 10.1016/0013-4694(83)90141-4
Oehrn, C. R. et al. Neural communication patterns underlying conflict detection, resolution, and adaptation. J. Neurosci. 34, 10438–10452 (2014).
pubmed: 25080602
pmcid: 6608272
doi: 10.1523/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).
doi: 10.1214/aoms/1177729694
VanRullen, R. How to evaluate phase differences between trial groups in ongoing electrophysiological signals. Front. Neurosci. 10, 426–426 (2016).
pubmed: 27683543
pmcid: 5021700
doi: 10.3389/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).
pubmed: 20133762
pmcid: 2840289
doi: 10.1073/pnas.0911531107
de Cheveigné, A. & Nelken, I. Filters: when, why, and how (not) to use them. Neuron 102, 280–293 (2019).
pubmed: 30998899
doi: 10.1016/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).
pubmed: 25128257
doi: 10.1016/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).
pubmed: 29995603
pmcid: 6230803
doi: 10.1152/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).
pubmed: 30244883
doi: 10.1016/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).
pubmed: 17409248
pmcid: 6672400
doi: 10.1523/JNEUROSCI.4636-06.2007
Berens, P. CircStat: a MATLAB toolbox for circular statistics. J. Stat. Softw. 31, 1–21 (2009).
doi: 10.18637/jss.v031.i10