Medial Prefrontal Theta Phase Coupling During Spatial Memory Retrieval

Overview

Journal Hippocampus

Publisher Wiley

Date 2014 Feb 6

PMID 24497013

Citations 61

Authors

Raphael Kaplan

Daniel Bush

Mathilde Bonnefond

Peter A Bandettini

Gareth R Barnes

Christian F Doeller

Neil Burgess

Affiliations

Soon will be listed here.

Abstract

Memory retrieval is believed to involve a disparate network of areas, including medial prefrontal and medial temporal cortices, but the mechanisms underlying their coordination remain elusive. One suggestion is that oscillatory coherence mediates inter-regional communication, implicating theta phase and theta-gamma phase-amplitude coupling in mnemonic function across species. To examine this hypothesis, we used non-invasive whole-head magnetoencephalography (MEG) as participants retrieved the location of objects encountered within a virtual environment. We demonstrate that, when participants are cued with the image of an object whose location they must subsequently navigate to, there is a significant increase in 4-8 Hz theta power in medial prefrontal cortex (mPFC), and the phase of this oscillation is coupled both with ongoing theta phase in the medial temporal lobe (MTL) and perceptually induced 65-85 Hz gamma amplitude in medial parietal cortex. These results suggest that theta phase coupling between mPFC and MTL and theta-gamma phase-amplitude coupling between mPFC and neocortical regions may play a role in human spatial memory retrieval.

Citing Articles

Understanding Learning from EEG Data: Combining Machine Learning and Feature Engineering Based on Hidden Markov Models and Mixed Models.

Palma G, Thornberry C, Commins S, Moral R Neuroinformatics. 2024; 22(4):487-497.

PMID: 39254794 PMC: 11579152. DOI: 10.1007/s12021-024-09690-6.

Effects of continuous versus intermittent theta-burst TMS on fMRI connectivity.

Hermiller M Front Hum Neurosci. 2024; 18:1380583.

PMID: 38883322 PMC: 11177618. DOI: 10.3389/fnhum.2024.1380583.

Months-long tracking of neuronal ensembles spanning multiple brain areas with Ultra-Flexible Tentacle Electrodes.

Yasar T, Gombkoto P, Vyssotski A, Vavladeli A, Lewis C, Wu B Nat Commun. 2024; 15(1):4822.

PMID: 38844769 PMC: 11156863. DOI: 10.1038/s41467-024-49226-9.

McGill M, Kieffaber P PLoS One. 2024; 19(4):e0297995.

PMID: 38564573 PMC: 10986947. DOI: 10.1371/journal.pone.0297995.

Acetylcholine modulates the temporal dynamics of human theta oscillations during memory.

Gedankien T, Tan R, Qasim S, Moore H, McDonagh D, Jacobs J Nat Commun. 2023; 14(1):5283.

PMID: 37648692 PMC: 10469188. DOI: 10.1038/s41467-023-41025-y.

References

Sauseng P, Klimesch W, Doppelmayr M, Hanslmayr S, Schabus M, Gruber W . Theta coupling in the human electroencephalogram during a working memory task. Neurosci Lett. 2003; 354(2):123-6. DOI: 10.1016/j.neulet.2003.10.002. View

Griesmayr B, Gruber W, Klimesch W, Sauseng P . Human frontal midline theta and its synchronization to gamma during a verbal delayed match to sample task. Neurobiol Learn Mem. 2009; 93(2):208-15. DOI: 10.1016/j.nlm.2009.09.013. View

Fletcher P, Shallice T, Frith C, Frackowiak R, Dolan R . Brain activity during memory retrieval. The influence of imagery and semantic cueing. Brain. 1996; 119 ( Pt 5):1587-96. DOI: 10.1093/brain/119.5.1587. View

Fuentemilla L, Penny W, Cashdollar N, Bunzeck N, Duzel E . Theta-coupled periodic replay in working memory. Curr Biol. 2010; 20(7):606-12. PMC: 2856918. DOI: 10.1016/j.cub.2010.01.057. View

Hasselmo M, Bodelon C, Wyble B . A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput. 2002; 14(4):793-817. DOI: 10.1162/089976602317318965. View

Anderson K, Rajagovindan R, Ghacibeh G, Meador K, Ding M . Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. Cereb Cortex. 2009; 20(7):1604-12. DOI: 10.1093/cercor/bhp223. View

Vanhatalo S, Palva J, Holmes M, Miller J, Voipio J, Kaila K . Infraslow oscillations modulate excitability and interictal epileptic activity in the human cortex during sleep. Proc Natl Acad Sci U S A. 2004; 101(14):5053-7. PMC: 387372. DOI: 10.1073/pnas.0305375101. View

Herrmann C, Munk M, Engel A . Cognitive functions of gamma-band activity: memory match and utilization. Trends Cogn Sci. 2004; 8(8):347-55. DOI: 10.1016/j.tics.2004.06.006. View

Mitchell D, McNaughton N, Flanagan D, Kirk I . Frontal-midline theta from the perspective of hippocampal "theta". Prog Neurobiol. 2008; 86(3):156-85. DOI: 10.1016/j.pneurobio.2008.09.005. View

10.

Jones M, Wilson M . Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol. 2005; 3(12):e402. PMC: 1283536. DOI: 10.1371/journal.pbio.0030402. View

11.

Fries P . A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci. 2005; 9(10):474-80. DOI: 10.1016/j.tics.2005.08.011. View

12.

Foster B, Kaveh A, Dastjerdi M, Miller K, Parvizi J . Human retrosplenial cortex displays transient theta phase locking with medial temporal cortex prior to activation during autobiographical memory retrieval. J Neurosci. 2013; 33(25):10439-46. PMC: 3685837. DOI: 10.1523/JNEUROSCI.0513-13.2013. View

13.

Guitart-Masip M, Barnes G, Horner A, Bauer M, Dolan R, Duzel E . Synchronization of medial temporal lobe and prefrontal rhythms in human decision making. J Neurosci. 2013; 33(2):442-51. PMC: 3562870. DOI: 10.1523/JNEUROSCI.2573-12.2013. View

14.

Litvak V, Mattout J, Kiebel S, Phillips C, Henson R, Kilner J . EEG and MEG data analysis in SPM8. Comput Intell Neurosci. 2011; 2011:852961. PMC: 3061292. DOI: 10.1155/2011/852961. View

15.

Buzsaki G, Logothetis N, Singer W . Scaling brain size, keeping timing: evolutionary preservation of brain rhythms. Neuron. 2013; 80(3):751-64. PMC: 4009705. DOI: 10.1016/j.neuron.2013.10.002. View

16.

Jensen O, Kaiser J, Lachaux J . Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci. 2007; 30(7):317-24. DOI: 10.1016/j.tins.2007.05.001. View

17.

Hall S, Holliday I, Hillebrand A, Singh K, Furlong P, Hadjipapas A . The missing link: analogous human and primate cortical gamma oscillations. Neuroimage. 2005; 26(1):13-7. DOI: 10.1016/j.neuroimage.2005.01.009. View

18.

Euston D, Gruber A, McNaughton B . The role of medial prefrontal cortex in memory and decision making. Neuron. 2012; 76(6):1057-70. PMC: 3562704. DOI: 10.1016/j.neuron.2012.12.002. View

19.

Hyman J, Hasselmo M, Seamans J . What is the Functional Relevance of Prefrontal Cortex Entrainment to Hippocampal Theta Rhythms?. Front Neurosci. 2011; 5:24. PMC: 3052540. DOI: 10.3389/fnins.2011.00024. View

20.

Buzsaki G, Chrobak J . Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neurobiol. 1995; 5(4):504-10. DOI: 10.1016/0959-4388(95)80012-3. View