A causal role for the precuneus in network-wide theta and gamma oscillatory activity during complex memory retrieval

Melissa Hebscher, Jed A Meltzer, Asaf Gilboa, Melissa Hebscher, Jed A Meltzer, Asaf Gilboa

Abstract

Complex memory of personal events is thought to depend on coordinated reinstatement of cortical representations by the medial temporal lobes (MTL). MTL-cortical theta and gamma coupling is believed to mediate such coordination, but which cortical structures are critical for retrieval and how they influence oscillatory coupling is unclear. We used magnetoencephalography (MEG) combined with continuous theta burst stimulation (cTBS) to (i) clarify the roles of theta and gamma oscillations in network-wide communication during naturalistic memory retrieval, and (ii) understand the causal relationship between cortical network nodes and oscillatory communication. Retrieval was associated with MTL-posterior neocortical theta phase coupling and theta-gamma phase-amplitude coupling relative to a rest period. Precuneus cTBS altered MTL-neocortical communication by modulating theta and gamma oscillatory coupling. These findings provide a mechanistic account for MTL-cortical communication and demonstrate that the precuneus is a critical cortical node of oscillatory activity, coordinating cross-regional interactions that drive remembering.

Keywords: episodic memory; human; medial temporal lobe; neural oscillations; neuroscience; precuneus; theta burst stimulation.

Conflict of interest statement

MH, JM, AG No competing interests declared

© 2019, Hebscher et al.

Figures

Figure 1.. Autobiographical memory paradigm.
Figure 1.. Autobiographical memory paradigm.
Participants were cued with familiar words (locations, people, objects), and told to recall a past event in relation to this word. Construction was terminated when participants indicated they had an event in mind via button press.
Figure 2.. Exploratory between-subjects analysis showing that…
Figure 2.. Exploratory between-subjects analysis showing that precuneus stimulation leads to (A) reduced vividness ratings and (B) reduced ease of recall compared to vertex stimulation when considering only the first session for each participant.
Asterisks indicate a significant difference between precuneus and vertex stimulation (p

Figure 2—figure supplement 1.. Exploratory between-subjects analysis…

Figure 2—figure supplement 1.. Exploratory between-subjects analysis showing non-significant differences between precuneus and vertex stimulation…

Figure 2—figure supplement 1.. Exploratory between-subjects analysis showing non-significant differences between precuneus and vertex stimulation for (A) vividness and (B) ease of recall, when considering only the second session for each participant.

Figure 3.. Theta activity during autobiographical memory…

Figure 3.. Theta activity during autobiographical memory retrieval for vertex stimulation sessions.

( A )…

Figure 3.. Theta activity during autobiographical memory retrieval for vertex stimulation sessions.
(A) Theta power increases during AM retrieval relative to rest. (B) Increased theta phase coupling during AM retrieval using a right MTL seed (blue box). Theta power and phase coupling images displayed at p<0.005, cluster corrected. (C) Comodulogram showing theta-gamma phase-amplitude coupling between right MTL theta phase and left precuneus gamma amplitude. Black dotted lines on comodulogram shows areas of significantly different phase-amplitude coupling between memory and rest. Comodulogram displayed at p<0.05, cluster corrected.

Figure 4.. Effects of cTBS on theta…

Figure 4.. Effects of cTBS on theta activity during memory elaboration relative to rest.

(…

Figure 4.. Effects of cTBS on theta activity during memory elaboration relative to rest.
(A) Precuneus stimulation led to decreased theta phase coupling between a right MTL seed (blue box) and the left occipital lobe. Images displayed at p<0.005, cluster corrected. (B) Comodulograms showing theta-gamma phase-amplitude coupling separately for vertex (left) and precuneus (right) stimulation sessions, between right MTL theta phase and left precuneus gamma amplitude. Black dotted lines show areas of significantly different phase-amplitude coupling between memory and rest. (C) Comparison between comodulograms in (B), showing precuneus compared to vertex stimulation during memory retrieval, between right MTL theta phase and left precuneus gamma amplitude. Black dotted lines show areas of significantly different phase-amplitude coupling between precuneus and vertex stimulation. Comodulograms displayed at p<0.05, cluster corrected.

Figure 4—figure supplement 1.. Phase-amplitude coupling using…

Figure 4—figure supplement 1.. Phase-amplitude coupling using a broader amplitude frequency range reveals that effects…

Figure 4—figure supplement 1.. Phase-amplitude coupling using a broader amplitude frequency range reveals that effects are specific to high gamma.
Comodulograms show PAC for (A) vertex and (B) precuneus stimulation sessions, and (C) comparison between precuneus and vertex stimulation sessions. Comodulograms displayed at p<0.05, cluster corrected.
Figure 2—figure supplement 1.. Exploratory between-subjects analysis…
Figure 2—figure supplement 1.. Exploratory between-subjects analysis showing non-significant differences between precuneus and vertex stimulation for (A) vividness and (B) ease of recall, when considering only the second session for each participant.
Figure 3.. Theta activity during autobiographical memory…
Figure 3.. Theta activity during autobiographical memory retrieval for vertex stimulation sessions.
(A) Theta power increases during AM retrieval relative to rest. (B) Increased theta phase coupling during AM retrieval using a right MTL seed (blue box). Theta power and phase coupling images displayed at p<0.005, cluster corrected. (C) Comodulogram showing theta-gamma phase-amplitude coupling between right MTL theta phase and left precuneus gamma amplitude. Black dotted lines on comodulogram shows areas of significantly different phase-amplitude coupling between memory and rest. Comodulogram displayed at p<0.05, cluster corrected.
Figure 4.. Effects of cTBS on theta…
Figure 4.. Effects of cTBS on theta activity during memory elaboration relative to rest.
(A) Precuneus stimulation led to decreased theta phase coupling between a right MTL seed (blue box) and the left occipital lobe. Images displayed at p<0.005, cluster corrected. (B) Comodulograms showing theta-gamma phase-amplitude coupling separately for vertex (left) and precuneus (right) stimulation sessions, between right MTL theta phase and left precuneus gamma amplitude. Black dotted lines show areas of significantly different phase-amplitude coupling between memory and rest. (C) Comparison between comodulograms in (B), showing precuneus compared to vertex stimulation during memory retrieval, between right MTL theta phase and left precuneus gamma amplitude. Black dotted lines show areas of significantly different phase-amplitude coupling between precuneus and vertex stimulation. Comodulograms displayed at p<0.05, cluster corrected.
Figure 4—figure supplement 1.. Phase-amplitude coupling using…
Figure 4—figure supplement 1.. Phase-amplitude coupling using a broader amplitude frequency range reveals that effects are specific to high gamma.
Comodulograms show PAC for (A) vertex and (B) precuneus stimulation sessions, and (C) comparison between precuneus and vertex stimulation sessions. Comodulograms displayed at p<0.05, cluster corrected.

References

    1. Addis DR, Wong AT, Schacter DL. Remembering the past and imagining the future: common and distinct neural substrates during event construction and elaboration. Neuropsychologia. 2007;45:1363–1377. doi: 10.1016/j.neuropsychologia.2006.10.016.
    1. Addis DR, Pan L, Vu MA, Laiser N, Schacter DL. Constructive episodic simulation of the future and the past: distinct subsystems of a core brain network mediate imagining and remembering. Neuropsychologia. 2009;47:2222–2238. doi: 10.1016/j.neuropsychologia.2008.10.026.
    1. Arnold KM, McDermott KB, Szpunar KK. Imagining the near and far future: the role of location familiarity. Memory & Cognition. 2011;39:954–967. doi: 10.3758/s13421-011-0076-1.
    1. Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J. Cross-frequency coupling supports multi-item working memory in the human hippocampus. PNAS. 2010;107:3228–3233. doi: 10.1073/pnas.0911531107.
    1. Battaglia FP, Benchenane K, Sirota A, Pennartz CM, Wiener SI. The hippocampus: hub of brain network communication for memory. Trends in Cognitive Sciences. 2011;15:310–318. doi: 10.1016/j.tics.2011.05.008.
    1. Bonnì S, Veniero D, Mastropasqua C, Ponzo V, Caltagirone C, Bozzali M, Koch G. TMS evidence for a selective role of the precuneus in source memory retrieval. Behavioural Brain Research. 2015;282:70–75. doi: 10.1016/j.bbr.2014.12.032.
    1. Bonnici HM, Cheke LG, Green DAE, FitzGerald THMB, Simons JS. Specifying a causal role for angular gyrus in autobiographical memory. The Journal of Neuroscience. 2018;38:10438–10443. doi: 10.1523/JNEUROSCI.1239-18.2018.
    1. Burgess N, Becker S, King JA, O'Keefe J. Memory for events and their spatial context: models and experiments. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences. 2001a;356:1493–1503. doi: 10.1098/rstb.2001.0948.
    1. Burgess N, Maguire EA, Spiers HJ, O'Keefe J. A temporoparietal and prefrontal network for retrieving the spatial context of lifelike events. NeuroImage. 2001b;14:439–453. doi: 10.1006/nimg.2001.0806.
    1. Burke JF, Ramayya AG, Kahana MJ. Human intracranial high-frequency activity during memory processing: neural oscillations or stochastic volatility? Current Opinion in Neurobiology. 2015;31:104–110. doi: 10.1016/j.conb.2014.09.003.
    1. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS. High gamma power is Phase-Locked to theta oscillations in human neocortex . Science. 2007;313 doi: 10.1126/science.1128115.
    1. Cavanna AE, Trimble MR. The precuneus: a review of its functional anatomy and behavioural correlates. Brain. 2006;129:564–583. doi: 10.1093/brain/awl004.
    1. Chen HY, Gilmore AW, Nelson SM, McDermott KB. Are there multiple kinds of episodic memory? an fMRI investigation comparing autobiographical and recognition memory tasks. The Journal of Neuroscience. 2017;37:2764–2775. doi: 10.1523/JNEUROSCI.1534-16.2017.
    1. Cohen MX. Assessing transient cross-frequency coupling in EEG data. Journal of Neuroscience Methods. 2008;168:494–499. doi: 10.1016/j.jneumeth.2007.10.012.
    1. Colgin LL. Rhythms of the hippocampal network. Nature Reviews Neuroscience. 2016;17:239–249. doi: 10.1038/nrn.2016.21.
    1. Crone NE, Korzeniewska A, Franaszczuk PJ. Cortical γ responses: searching high and low. International Journal of Psychophysiology. 2011;79:9–15. doi: 10.1016/j.ijpsycho.2010.10.013.
    1. Eckart C, Fuentemilla L, Bauch EM, Bunzeck N. Dopaminergic stimulation facilitates working memory and differentially affects prefrontal low theta oscillations. NeuroImage. 2014;94:185–192. doi: 10.1016/j.neuroimage.2014.03.011.
    1. Fell J, Axmacher N. The role of phase synchronization in memory processes. Nature Reviews Neuroscience. 2011;12:105–118. doi: 10.1038/nrn2979.
    1. Foster BL, Kaveh A, Dastjerdi M, Miller KJ, Parvizi J. Human retrosplenial cortex displays transient theta phase locking with medial temporal cortex prior to activation during autobiographical memory retrieval. Journal of Neuroscience. 2013;33:10439–10446. doi: 10.1523/JNEUROSCI.0513-13.2013.
    1. Freton M, Lemogne C, Bergouignan L, Delaveau P, Lehéricy S, Fossati P. The eye of the self: precuneus volume and visual perspective during autobiographical memory retrieval. Brain Structure and Function. 2014;219:959–968. doi: 10.1007/s00429-013-0546-2.
    1. Fuentemilla L, Barnes GR, Düzel E, Levine B. Theta oscillations orchestrate medial temporal lobe and neocortex in remembering autobiographical memories. NeuroImage. 2014;85 Pt 2:730–737. doi: 10.1016/j.neuroimage.2013.08.029.
    1. Gilboa A. Autobiographical and episodic memory--one and the same? evidence from prefrontal activation in neuroimaging studies. Neuropsychologia. 2004;42:1336–1349. doi: 10.1016/j.neuropsychologia.2004.02.014.
    1. Hassabis D, Maguire EA. The construction system of the brain. Philosophical Transactions of the Royal Society B: Biological Sciences. 2009;364:1263–1271. doi: 10.1098/rstb.2008.0296.
    1. Hebscher M, Levine B, Gilboa A. The precuneus and hippocampus contribute to individual differences in the unfolding of spatial representations during episodic autobiographical memory. Neuropsychologia. 2018;110:123–133. doi: 10.1016/j.neuropsychologia.2017.03.029.
    1. Hebscher M, Gilboa A. A boost of confidence: the role of the ventromedial prefrontal cortex in memory, decision-making, and schemas. Neuropsychologia. 2016;90:46–58. doi: 10.1016/j.neuropsychologia.2016.05.003.
    1. Iriye H, Jacques PLS. Construction and elaboration of autobiographical memories from multiple visual perspectives heather. BioRxiv. 2018;44 doi: 10.1101/317594.
    1. Kaplan R, Bush D, Bonnefond M, Bandettini PA, Barnes GR, Doeller CF, Burgess N. Medial prefrontal theta phase coupling during spatial memory retrieval. Hippocampus. 2014;24:656–665. doi: 10.1002/hipo.22255.
    1. Kaplan R, Bush D, Bisby JA, Horner AJ, Meyer SS, Burgess N. Medial Prefrontal–Medial Temporal Theta Phase Coupling in Dynamic Spatial Imagery. Journal of Cognitive Neuroscience. 2017;3:1–13. doi: 10.1162/jocn_a_01064.
    1. Kim H. Neural activity that predicts subsequent memory and forgetting: a meta-analysis of 74 fMRI studies. NeuroImage. 2011;54:2446–2461. doi: 10.1016/j.neuroimage.2010.09.045.
    1. Koch G, Bonnì S, Pellicciari MC, Casula EP, Mancini M, Esposito R, Ponzo V, Picazio S, Di Lorenzo F, Serra L, Motta C, Maiella M, Marra C, Cercignani M, Martorana A, Caltagirone C, Bozzali M. Transcranial magnetic stimulation of the precuneus enhances memory and neural activity in prodromal alzheimer's disease. NeuroImage. 2018;169:302–311. doi: 10.1016/j.neuroimage.2017.12.048.
    1. McClelland JL, McNaughton BL, O'Reilly RC. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychological Review. 1995;102:419–457. doi: 10.1037/0033-295X.102.3.419.
    1. McCormick C, Ciaramelli E, De Luca F, Maguire EA. Comparing and contrasting the cognitive effects of hippocampal and ventromedial prefrontal cortex damage: a review of human lesion studies. Neuroscience. 2018;374:295–318. doi: 10.1016/j.neuroscience.2017.07.066.
    1. McDermott KB, Szpunar KK, Christ SE. Laboratory-based and autobiographical retrieval tasks differ substantially in their neural substrates. Neuropsychologia. 2009;47:2290–2298. doi: 10.1016/j.neuropsychologia.2008.12.025.
    1. Nadel L, Moscovitch M. Memory consolidation, retrograde amnesia and the hippocampal complex. Current Opinion in Neurobiology. 1997;7:217–227. doi: 10.1016/S0959-4388(97)80010-4.
    1. Neuling T, Rach S, Wagner S, Wolters CH, Herrmann CS. Good vibrations: oscillatory phase shapes perception. NeuroImage. 2012;63:771–778. doi: 10.1016/j.neuroimage.2012.07.024.
    1. Nilakantan AS, Bridge DJ, Gagnon EP, VanHaerents SA, Voss JL. Stimulation of the posterior Cortical-Hippocampal network enhances precision of memory recollection. Current Biology. 2017;27:465–470. doi: 10.1016/j.cub.2016.12.042.
    1. Olsen RK, Rondina R, Riggs L, Meltzer JA, Ryan JD. Hippocampal and neocortical oscillatory contributions to visuospatial binding and comparison. Journal of Experimental Psychology: General. 2013;142:1335–1345. doi: 10.1037/a0034043.
    1. Payne L, Kounios J. Coherent oscillatory networks supporting short-term memory retention. Brain Research. 2009;1247:126–132. doi: 10.1016/j.brainres.2008.09.095.
    1. Pu Y, Cheyne DO, Cornwell BR, Johnson BW. Non-invasive investigation of human hippocampal rhythms using magnetoencephalography: a review. Frontiers in Neuroscience. 2018;12:1–16. doi: 10.3389/fnins.2018.00273.
    1. Robin J, Wynn J, Moscovitch M. The spatial scaffold: the effects of spatial context on memory for events. Journal of Experimental Psychology: Learning Memory. 2015 doi: 10.1037/xlm0000167.
    1. Rolls ET. Hippocampo-cortical and cortico-cortical backprojections. Hippocampus. 2000;10:380–388. doi: 10.1002/1098-1063(2000)10:4<380::AID-HIPO4>;2-0.
    1. Rosenbaum RS, Moscovitch M, Foster JK, Schnyer DM, Gao F, Kovacevic N, Verfaellie M, Black SE, Levine B. Patterns of autobiographical memory loss in medial-temporal lobe amnesic patients. Journal of Cognitive Neuroscience. 2008;20:1490–1506. doi: 10.1162/jocn.2008.20105.
    1. Rossi S, Hallett M, Rossini PM, Pascual-Leone A, Safety of TMS Consensus Group Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical Neurophysiology. 2009;120:2008–2039. doi: 10.1016/j.clinph.2009.08.016.
    1. Rugg MD, Vilberg KL. Brain networks underlying episodic memory retrieval. Current Opinion in Neurobiology. 2013;23:255–260. doi: 10.1016/j.conb.2012.11.005.
    1. Sauseng P, Klimesch W, Heise KF, Gruber WR, Holz E, Karim AA, Glennon M, Gerloff C, Birbaumer N, Hummel FC. Brain oscillatory substrates of visual short-term memory capacity. Current Biology. 2009;19:1846–1852. doi: 10.1016/j.cub.2009.08.062.
    1. Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery & Psychiatry. 1957;20:11–21. doi: 10.1136/jnnp.20.1.11.
    1. Seymour RA, Rippon G, Kessler K. The detection of phase amplitude coupling during sensory processing. Frontiers in Neuroscience. 2017;11:1–22. doi: 10.3389/fnins.2017.00487.
    1. Shimamura T, Shiroishi M, Weyand S, Tsujimoto H, Winter G, Katritch V, Abagyan R, Cherezov V, Liu W, Han GW, Kobayashi T, Stevens RC, Iwata S. Structure of the human histamine H1 receptor complex with doxepin. Nature. 2011;475:65–70. doi: 10.1038/nature10236.
    1. Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsáki G. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron. 2008;60:683–697. doi: 10.1016/j.neuron.2008.09.014.
    1. St Jacques PL, Szpunar KK, Schacter DL. Shifting visual perspective during retrieval shapes autobiographical memories. NeuroImage. 2017;148:103–114. doi: 10.1016/j.neuroimage.2016.12.028.
    1. Stam CJ, Nolte G, Daffertshofer A. Phase lag index: assessment of functional connectivity from multi channel EEG and MEG with diminished bias from common sources. Human Brain Mapping. 2007;28:1178–1193. doi: 10.1002/hbm.20346.
    1. Staudigl T, Hanslmayr S. Theta oscillations at encoding mediate the context-dependent nature of human episodic memory. Current Biology. 2013;23:1101–1106. doi: 10.1016/j.cub.2013.04.074.
    1. Steinvorth S, Wang C, Ulbert I, Schomer D, Halgren E. Human entorhinal gamma and theta oscillations selective for remote autobiographical memory. Hippocampus. 2010;20:166–173. doi: 10.1002/hipo.20597.
    1. Svoboda E, McKinnon MC, Levine B. The functional neuroanatomy of autobiographical memory: a meta-analysis. Neuropsychologia. 2006;44:2189–2208. doi: 10.1016/j.neuropsychologia.2006.05.023.
    1. Thakral PP, Madore KP, Schacter DL. A role for the left angular gyrus in episodic simulation and memory. The Journal of Neuroscience. 2017;37:8142–8149. doi: 10.1523/JNEUROSCI.1319-17.2017.
    1. van der Meij R, Kahana M, Maris E. Phase-Amplitude coupling in human electrocorticography is spatially distributed and phase diverse. Journal of Neuroscience. 2012;32:111–123. doi: 10.1523/JNEUROSCI.4816-11.2012.
    1. Vinck M, Oostenveld R, van Wingerden M, Battaglia F, Pennartz CM. An improved index of phase-synchronization for electrophysiological data in the presence of volume-conduction, noise and sample-size bias. NeuroImage. 2011;55:1548–1565. doi: 10.1016/j.neuroimage.2011.01.055.
    1. Vrba J, Robinson SE. Signal processing in magnetoencephalography. Methods. 2001;25:249–271. doi: 10.1006/meth.2001.1238.
    1. Wang JX, Rogers LM, Gross EZ, Ryals AJ, Dokucu ME, Brandstatt KL, Hermiller MS, Voss JL. Targeted enhancement of cortical-hippocampal brain networks and associative memory. Science. 2014;345:1054–1057. doi: 10.1126/science.1252900.
    1. Wang JX, Voss JL. Long-lasting enhancements of memory and hippocampal-cortical functional connectivity following multiple-day targeted noninvasive stimulation. Hippocampus. 2015;25:877–883. doi: 10.1002/hipo.22416.
    1. Wikenheiser AM, Redish AD. Hippocampal theta sequences reflect current goals. Nature Neuroscience. 2015;18:289–294. doi: 10.1038/nn.3909.
    1. Wu SW, Shahana N, Huddleston DA, Gilbert DL. Effects of 30hz θ burst transcranial magnetic stimulation on the primary motor cortex. Journal of Neuroscience Methods. 2012;208:161–164. doi: 10.1016/j.jneumeth.2012.05.014.
    1. Yazar Y, Bergström ZM, Simons JS. Continuous theta burst stimulation of angular gyrus reduces subjective recollection. PLOS ONE. 2014;9:e110414. doi: 10.1371/journal.pone.0110414.
    1. Zaehle T, Rach S, Herrmann CS. Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PLOS ONE. 2010;5:e13766. doi: 10.1371/journal.pone.0013766.

Source: PubMed

Patrocinadores y Colaboradores

Condiciones médicas

Intervenciones de drogas

3
Suscribir