Bidirectional propagation of low frequency oscillations over the human hippocampal surface.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
12 05 2021
12 05 2021
Historique:
received:
24
05
2020
accepted:
01
04
2021
entrez:
13
5
2021
pubmed:
14
5
2021
medline:
29
5
2021
Statut:
epublish
Résumé
The hippocampus is diversely interconnected with other brain systems along its axis. Cycles of theta-frequency activity are believed to propagate from the septal to temporal pole, yet it is unclear how this one-way route supports the flexible cognitive capacities of this structure. We leveraged novel thin-film microgrid arrays conformed to the human hippocampal surface to track neural activity two-dimensionally in vivo. All oscillation frequencies identified between 1-15 Hz propagated across the tissue. Moreover, they dynamically shifted between two roughly opposite directions oblique to the long axis. This predominant propagation axis was mirrored across participants, hemispheres, and consciousness states. Directionality was modulated in a participant who performed a behavioral task, and it could be predicted by wave amplitude topography over the hippocampal surface. Our results show that propagation directions may thus represent distinct meso-scale network computations, operating along versatile spatiotemporal processing routes across the hippocampal body.
Identifiants
pubmed: 33980852
doi: 10.1038/s41467-021-22850-5
pii: 10.1038/s41467-021-22850-5
pmc: PMC8115072
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
2764Subventions
Organisme : NINDS NIH HHS
ID : K23 NS110920
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC012379
Pays : United States
Organisme : NINDS NIH HHS
ID : R25 NS070680
Pays : United States
Organisme : NINDS NIH HHS
ID : R00 NS065120
Pays : United States
Références
Moser, M. B. & Moser, E. I. Functional differentiation in the hippocampus. Hippocampus 8, 608–619 (1998).
pubmed: 9882018
doi: 10.1002/(SICI)1098-1063(1998)8:6<608::AID-HIPO3>3.0.CO;2-7
Fanselow, M. S. & Dong, H.-W. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65, 7–19 (2010).
pubmed: 20152109
pmcid: 2822727
doi: 10.1016/j.neuron.2009.11.031
Dong, H.-W., Swanson, L. W., Chen, L., Fanselow, M. S. & Toga, A. W. Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc. Natl Acad. Sci. USA 106, 11794–11799 (2009).
pubmed: 19561297
doi: 10.1073/pnas.0812608106
pmcid: 2710698
Vogel, J. W. et al. A molecular gradient along the longitudinal axis of the human hippocampus informs large-scale behavioral systems. Nat. Commun. 11, 960 (2020).
pubmed: 32075960
pmcid: 7031290
doi: 10.1038/s41467-020-14518-3
Strange, B. A., Witter, M. P., Lein, E. S. & Moser, E. I. Functional organization of the hippocampal longitudinal axis. Nat. Rev. Neurosci. 15, 655–669 (2014).
pubmed: 25234264
doi: 10.1038/nrn3785
Poppenk, J., Evensmoen, H. R., Moscovitch, M. & Nadel, L. Long-axis specialization of the human hippocampus. Trends Cogn. Sci. (Regul. Ed.) 17, 230–240 (2013).
doi: 10.1016/j.tics.2013.03.005
Kjelstrup, K. B. et al. Finite scale of spatial representation in the hippocampus. Science 321, 140–143 (2008).
pubmed: 18599792
doi: 10.1126/science.1157086
Brunec, I. K. et al. Multiple scales of representation along the hippocampal anteroposterior axis in humans. Curr. Biol. 28, 2129–2135.e6 (2018).
pubmed: 29937352
doi: 10.1016/j.cub.2018.05.016
Wittner, L., Henze, D. A., Záborszky, L. & Buzsáki, G. Three-dimensional reconstruction of the axon arbor of a CA3 pyramidal cell recorded and filled in vivo. Brain Struct. Funct. 212, 75–83 (2007).
pubmed: 17717699
pmcid: 2662726
doi: 10.1007/s00429-007-0148-y
Buzsáki, G. & Tingley, D. Space and time: the hippocampus as a sequence generator. Trends Cogn. Sci. (Regul. Ed.) 22, 853–869 (2018).
doi: 10.1016/j.tics.2018.07.006
Muller, L., Chavane, F., Reynolds, J. & Sejnowski, T. J. Cortical travelling waves: mechanisms and computational principles. Nat. Rev. Neurosci. 19, 255–268 (2018).
pubmed: 29563572
pmcid: 5933075
doi: 10.1038/nrn.2018.20
Zhang, H. & Jacobs, J. Traveling theta waves in the human hippocampus. J. Neurosci. 35, 12477–12487 (2015).
pubmed: 26354915
pmcid: 4563037
doi: 10.1523/JNEUROSCI.5102-14.2015
Zhang, H., Watrous, A. J., Patel, A. & Jacobs, J. Theta and alpha oscillations are traveling waves in the human neocortex. Neuron 98, 1269–1281.e4 (2018).
pubmed: 29887341
pmcid: 6534129
doi: 10.1016/j.neuron.2018.05.019
Bahramisharif, A. et al. Propagating neocortical gamma bursts are coordinated by traveling alpha waves. J. Neurosci. 33, 18849–18854 (2013).
pubmed: 24285891
pmcid: 4262700
doi: 10.1523/JNEUROSCI.2455-13.2013
Lubenov, E. V. & Siapas, A. G. Hippocampal theta oscillations are travelling waves. Nature 459, 534–539 (2009).
pubmed: 19489117
doi: 10.1038/nature08010
Patel, J., Fujisawa, S., Berényi, A., Royer, S. & Buzsáki, G. Traveling theta waves along the entire septotemporal axis of the hippocampus. Neuron 75, 410–417 (2012).
pubmed: 22884325
pmcid: 3427387
doi: 10.1016/j.neuron.2012.07.015
Patel, J., Schomburg, E. W., Berényi, A., Fujisawa, S. & Buzsáki, G. Local generation and propagation of ripples along the septotemporal axis of the hippocampus. J. Neurosci. 33, 17029–17041 (2013).
pubmed: 24155307
pmcid: 3807028
doi: 10.1523/JNEUROSCI.2036-13.2013
Jackson, J. et al. Reversal of theta rhythm flow through intact hippocampal circuits. Nat. Neurosci. 17, 1362–1370 (2014).
pubmed: 25174002
doi: 10.1038/nn.3803
Rubino, D., Robbins, K. A. & Hatsopoulos, N. G. Propagating waves mediate information transfer in the motor cortex. Nat. Neurosci. 9, 1549–1557 (2006).
pubmed: 17115042
doi: 10.1038/nn1802
Stolk, A. et al. Electrocorticographic dissociation of alpha and beta rhythmic activity in the human sensorimotor system.eLife 8, e48065 (2019).
pubmed: 31596233
pmcid: 6785220
doi: 10.7554/eLife.48065
Smith, E. H. et al. The ictal wavefront is the spatiotemporal source of discharges during spontaneous human seizures. Nat. Commun. 7, 11098 (2016).
pubmed: 27020798
pmcid: 4820627
doi: 10.1038/ncomms11098
Takahashi, K., Saleh, M., Penn, R. D. & Hatsopoulos, N. G. Propagating waves in human motor cortex. Front Hum. Neurosci. 5, 40 (2011).
pubmed: 21629859
pmcid: 3084448
doi: 10.3389/fnhum.2011.00040
Martinet, L.-E. et al. Human seizures couple across spatial scales through travelling wave dynamics. Nat. Commun. 8, 14896 (2017).
pubmed: 28374740
pmcid: 5382286
doi: 10.1038/ncomms14896
Duvernoy, H. M., Cattin, F., Risold, P.-Y., Vannson, J. L. & Gaudron, M. The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI (Springer, 2013).
Delgado-González, J.C. et al. Quantitative measurements in the human hippocampus and related areas: correspondence between ex-vivo MRI and histological preparations.PLoS ONE 10, e0130314 (2015).
pubmed: 26098887
pmcid: 4476703
doi: 10.1371/journal.pone.0130314
Fell, J. et al. Medial temporal theta/alpha power enhancement precedes successful memory encoding: evidence based on intracranial EEG. J. Neurosci. 31, 5392–5397 (2011).
pubmed: 21471374
pmcid: 6622710
doi: 10.1523/JNEUROSCI.3668-10.2011
Jacobs, J. Hippocampal theta oscillations are slower in humans than in rodents: implications for models of spatial navigation and memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130304 (2014).
pubmed: 24366145
pmcid: 3866455
doi: 10.1098/rstb.2013.0304
Goyal, A. et al. Functionally distinct high and low theta oscillations in the human hippocampus. Nat. Commun. 11, 2469 (2020).
pubmed: 32424312
pmcid: 7235253
doi: 10.1038/s41467-020-15670-6
McKhann, G. M., Schoenfeld-McNeill, J., Born, D. E., Haglund, M. M. & Ojemann, G. A. Intraoperative hippocampal electrocorticography to predict the extent of hippocampal resection in temporal lobe epilepsy surgery. J. Neurosurg. 93, 44–52 (2000).
pubmed: 10883904
doi: 10.3171/jns.2000.93.1.0044
Muller, L. et al. Thin-film, high-density micro-electrocorticographic decoding of a human cortical gyrus. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2016, 1528–1531 (2016).
pmcid: 5789448
Cantero, J. L. et al. Sleep-dependent theta oscillations in the human hippocampus and neocortex. J. Neurosci. 23, 10897–10903 (2003).
pubmed: 14645485
pmcid: 6740994
doi: 10.1523/JNEUROSCI.23-34-10897.2003
Miller, J. et al. Lateralized hippocampal oscillations underlie distinct aspects of human spatial memory and navigation. Nat. Commun. 9, 2423 (2018).
pubmed: 29930307
pmcid: 6013427
doi: 10.1038/s41467-018-04847-9
Hamamé, C. M., Alario, F.-X., Llorens, A., Liégeois-Chauvel, C. & Trébuchon-Da Fonseca, A. High frequency gamma activity in the left hippocampus predicts visual object naming performance. Brain Lang. 135, 104–114 (2014).
pubmed: 25016093
doi: 10.1016/j.bandl.2014.05.007
Norman, Y. et al. Hippocampal sharp-wave ripples linked to visual episodic recollection in humans.Science 365, eaax1030 (2019).
pubmed: 31416934
doi: 10.1126/science.aax1030
Hamberger, M. J., Seidel, W. T., McKhann, G. M. & Goodman, R. R. Hippocampal removal affects visual but not auditory naming. Neurology 74, 1488–1493 (2010).
pubmed: 20335560
pmcid: 2875921
doi: 10.1212/WNL.0b013e3181dd40f0
Fisher, N. I. Statistical analysis of circular data. Cambridge Core /core/books/statistical-analysis-of-circular-data/324A46F3941A5CD641ED0B0910B2C33F https://doi.org/10.1017/CBO9780511564345 (1993).
Kleen, J. K. et al. Oscillation phase locking and late ERP components of intracranial hippocampal recordings correlate to patient performance in a working memory task. Front Hum. Neurosci. 10, 287 (2016).
pubmed: 27378885
pmcid: 4910536
doi: 10.3389/fnhum.2016.00287
Zhang, M., Shivacharan, R. S., Chiang, C.-C., Gonzalez-Reyes, L. E. & Durand, D. M. Propagating neural source revealed by doppler shift of population spiking frequency. J. Neurosci. 36, 3495–3505 (2016).
pubmed: 27013678
pmcid: 4804007
doi: 10.1523/JNEUROSCI.3525-15.2016
Eichenbaum, H. On the integration of space, time, and memory. Neuron 95, 1007–1018 (2017).
pubmed: 28858612
pmcid: 5662113
doi: 10.1016/j.neuron.2017.06.036
Ermentrout, G. B. & Kleinfeld, D. Traveling electrical waves in cortex: insights from phase dynamics and speculation on a computational role. Neuron 29, 33–44 (2001).
pubmed: 11182079
doi: 10.1016/S0896-6273(01)00178-7
Buzsáki, G. Theta oscillations in the hippocampus. Neuron 33, 325–340 (2002).
pubmed: 11832222
doi: 10.1016/S0896-6273(02)00586-X
Ólafsdóttir, H. F., Bush, D. & Barry, C. The role of hippocampal replay in memory and planning. Curr. Biol. 28, R37–R50 (2018).
pubmed: 29316421
pmcid: 5847173
doi: 10.1016/j.cub.2017.10.073
Diba, K. & Buzsáki, G. Forward and reverse hippocampal place-cell sequences during ripples. Nat. Neurosci. 10, 1241–1242 (2007).
pubmed: 17828259
pmcid: 2039924
doi: 10.1038/nn1961
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
Baud, M. O. et al. Unsupervised learning of spatiotemporal interictal discharges in focal epilepsy. Neurosurgery 83, 683–691 (2018).
pubmed: 29040672
doi: 10.1093/neuros/nyx480
He, B. J. Scale-free brain activity: past, present, and future. Trends Cogn. Sci. 18, 480–487 (2014).
pubmed: 24788139
pmcid: 4149861
doi: 10.1016/j.tics.2014.04.003
Donoghue, T., Dominguez, J. & Voytek, B. Electrophysiological frequency band ratio measures conflate periodic and aperiodic neural activity. eNeuro 7, ENEURO.0192-20.2020 (2020).
pubmed: 32978216
pmcid: 7768281
doi: 10.1523/ENEURO.0192-20.2020
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
Berens, P. CircStat: a MATLAB toolbox for circular statistics.J. Stat. Soft. 31, 1–21 (2009).
doi: 10.18637/jss.v031.i10
Ozarowska, A., Ilieva, M., Zehtindjiev, P., Akesson, S. & Muś, K. A new approach to evaluate multimodal orientation behaviour of migratory passerine birds recorded in circular orientation cages. J. Exp. Biol. 216, 4038–4046 (2013).
pubmed: 23868843
Rossion, B. & Pourtois, G. Revisiting Snodgrass and Vanderwart’s object pictorial set: the role of surface detail in basic-level object recognition. Perception 33, 217–236 (2004).
pubmed: 15109163
doi: 10.1068/p5117
Benjamini, Y. & Yekutieli, D. The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165–1188 (2001).
doi: 10.1214/aos/1013699998