Hippocampal-prefrontal theta-gamma coupling during performance of a spatial working memory task

Tamura, Makoto; Spellman, Timothy; Rosen, Andrew M.; Gogos, Joseph A.; Gordon, Joshua A.

doi:10.1038/s41467-017-02108-9

Cited by 160 publications

(164 citation statements)

References 39 publications

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“…It has been previously argued that for CA1, this corresponds to the phenomenon of theta-gamma coupling, where optimal improvement in decoding accuracy corresponds to number of nested gamma (~40-80 Hz) cycles within theta cycles (Jensen and Lisman, 2000). Theta-gamma coupling is also known to be related to CA1 theta sequences (Colgin, 2011; Zheng et al, 2016), and theta-gamma coupling has also been recently reported in hippocampal-prefrontal networks (Tamura et al, 2017), raising the possibility that a similar phenomenon can influence PFC spatial representations.…”

Section: Discussionmentioning

confidence: 99%

Coherent coding of spatial position mediated by theta oscillations in hippocampus and prefrontal cortex

Zielinski

Shin

Jadhav

2019

Preprint

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21Foundation award to SPJ. We would like to thank the late John Lisman for inspiring the 22 investigation of theta phase and prefrontal spatial representations. 23 2 ABSTRACT 24Interactions between the hippocampus (area CA1) and prefrontal cortex (PFC) are crucial for 25 memory-guided behavior. Theta oscillations (~8 Hz) underlie a key physiological mechanism for 26 mediating these coordinated interactions, and theta oscillatory coherence and phase-locked 27 spiking in the two regions have been shown to be important for spatial memory. Hippocampal 28 place cell activity associated with theta oscillations encodes spatial position during behavior, 29 and theta-phase associated spiking is known to further mediate a temporal code for space 30 within CA1 place fields. Although prefrontal neurons are prominently phase-locked to 31 hippocampal theta oscillations in spatial memory tasks, whether and how theta oscillations 32 mediate processing of spatial information across these networks remains unclear. Here, we 33 addressed these questions using simultaneous recordings of dorsal CA1 -PFC ensembles and 34 population decoding analyses in male rats performing a continuous spatial working memory task 35 known to require hippocampal-prefrontal interactions. We found that in addition to CA1, 36 population activity in PFC can also encode the animal's current spatial position on a theta-cycle 37 timescale during memory-guided behavior. Coding of spatial position was coherent for CA1 and 38 PFC ensembles, exhibiting correlated position representations within theta cycles. In addition, 39incorporating theta-phase information during decoding to account for theta-phase associated 40 spiking resulted in a significant improvement in the accuracy of prefrontal spatial 41 representations, similar to concurrent CA1 representations. These findings indicate a theta-42 oscillation mediated mechanism of temporal coordination for shared processing and 43 communication of spatial information across the two networks during spatial memory-guided 44 behavior. 45 46 47 48 49 3 50 SIGNIFICANCE STATEMENT 51Theta oscillation (~8 Hz) mediated interactions between the hippocampus and prefrontal cortex 52 are known to be important for spatial memory. Hippocampal place-cell activity associated with 53 theta oscillations underlies a rate and temporal code for spatial position, but it is not known 54 whether these oscillations mediate simultaneous coding of spatial information in hippocampal-55 prefrontal networks. Here, we found that population activity in prefrontal cortex encodes 56 animals' current position coherently with hippocampal populations on a theta-cycle timescale. 57Further we found that theta-phase associated spiking significantly improves prefrontal coding of 58 spatial position, in parallel with hippocampal coding. Our findings establish that theta oscillations 59 mediate a temporal coordination mechanism for coherent coding of spatial position in 60 hippocampal-prefrontal networks during memory-guided behavior.

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Section: Discussionmentioning

confidence: 99%

Coherent coding of spatial position mediated by theta oscillations in hippocampus and prefrontal cortex

Zielinski

Shin

Jadhav

2019

Preprint

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“…(3) the implication of theta-gamma coupling in working memory which may serve as a biomarker of behavioural performance (Axmacher et al, 2010;Park et al, 2013;Tamura, Spellman, Rosen, Gogos, & Gordon, 2017;Tort et al, 2009). …”

Section: Selection Of Individualised Frequencies Of Itbs Based On Tmentioning

confidence: 99%

“…The individualised frequency for Ind iTBS was determined by the phase-amplitude cross-frequency coupling (PAC) between frontal theta (phase) and parietal gamma (amplitude) oscillations during the 3-back task. The rationale for using working memory task EEG rather than resting EEG for the individualisation was: (1) to mimic the original TBS study in mice where the stimulation protocol was derived from the patterns of neuronal firing which occurred during learning or exploratory behaviour (Larson et al, 1986); (2) to minimise the variance of individuals' state by actively engaging in the same task for each subject, in contrast to resting EEG recordings during which participants could be performing a wide variety of neural functions and (3) the implication of theta-gamma coupling in working memory which may serve as a biomarker of behavioural performance (Axmacher et al, 2010;Park et al, 2013;Tamura, Spellman, Rosen, Gogos, & Gordon, 2017;Tort et al, 2009).…”

Section: Selection Of Individualised Frequencies Of Itbs Based On Tmentioning

confidence: 99%

The effects of individualised intermittent theta burst stimulation in the prefrontal cortex: A TMS‐EEG study

Chung

Sullivan

Rogasch

et al. 2018

Human Brain Mapping

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Recent studies have highlighted variability in response to theta burst stimulation (TBS) in humans. TBS paradigm was originally developed in rodents to mimic gamma bursts coupled with theta rhythms, and was shown to elicit long‐term potentiation. The protocol was subsequently adapted for humans using standardised frequencies of stimulation. However, each individual has different rhythmic firing pattern. The present study sought to explore whether individualised intermittent TBS (Ind iTBS) could outperform the effects of two other iTBS variants. Twenty healthy volunteers received iTBS over left prefrontal cortex using 30 Hz at 6 Hz, 50 Hz at 5 Hz, or individualised frequency in separate sessions. Ind iTBS was determined using theta‐gamma coupling during the 3‐back task. Concurrent use of transcranial magnetic stimulation and electroencephalography (TMS‐EEG) was used to track changes in cortical plasticity. We also utilised mood ratings using a visual analogue scale and assessed working memory via the 3‐back task before and after stimulation. No group‐level effect was observed following either 30 or 50 Hz iTBS in TMS‐EEG. Ind iTBS significantly increased the amplitude of the TMS‐evoked P60, and decreased N100 and P200 amplitudes. A significant positive correlation between neurophysiological change and change in mood rating was also observed. Improved accuracy in the 3‐back task was observed following both 50 Hz and Ind iTBS conditions. These findings highlight the critical importance of frequency in the parameter space of iTBS. Tailored stimulation parameters appear more efficacious than standard paradigms in neurophysiological and mood changes. This novel approach presents a promising option and benefits may extend to clinical applications.

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“…Recent reviews highlight the role of hippocampal-prefrontal interactions across different cognitive domains, such as goal-directed behavior (Womelsdorf et al, 2010), emotion (Jin and Maren, 2015), context-guided memory (Place et al, 2016), episodic memory (Eichenbaum, 2017), decision-making (Tamura et al, 2017) and spatial learning (Maharjan et al, 2018). Here, we sought to revisit and further characterize the electrophysiological signatures of hippocampal-prefrontal interactions during spatial decision.…”

Section: Introductionmentioning

confidence: 99%

Hippocampal-Prefrontal Interactions during Spatial Decision-Making

Tavares

Tort

2020

Preprint

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The hippocampus has been linked to memory encoding and spatial navigation, while the prefrontal cortex is associated with cognitive functions such as decision-making. These regions are hypothesized to communicate in tasks that demand both spatial navigation and decision-making processes. However, the electrophysiological signatures underlying this communication remain to be better elucidated. To investigate the dynamics of the hippocampal-prefrontal interactions, we have analyzed their local field potentials and spiking activity recorded from rats performing an odor-cued spatial alternation task in an 8-shaped maze. We found that the phase coherence of theta peaked around the choice point area of the maze. Moreover, Granger causality revealed a hippocampus->prefrontal cortex directionality of information flow at theta frequency, peaking at starting areas of the maze, and on the reverse direction at delta frequency, peaking near the turn onset.Additionally, the patterns of phase-amplitude cross-frequency coupling within and between the regions also showed spatial selectivity, and a new method revealed that hippocampal theta and prefrontal delta modulated not only gamma amplitude but also inter-regional gamma synchrony. Lastly, we found that the theta rhythm dynamically modulated neurons in both regions, with the highest modulation at the choice area; interestingly, prefrontal cortex neurons were more strongly modulated by the hippocampal theta rhythm than by their local field rhythm. In all, our results reveal maximum electrophysiological interactions between the hippocampus and the prefrontal cortex near the decision-making period of the spatial alternation task. These results corroborate the hypothesis that a dynamic interplay between these regions takes place during spatial decisions.

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Hippocampal-prefrontal theta-gamma coupling during performance of a spatial working memory task

Cited by 160 publications

References 39 publications

Coherent coding of spatial position mediated by theta oscillations in hippocampus and prefrontal cortex

Coherent coding of spatial position mediated by theta oscillations in hippocampus and prefrontal cortex

The effects of individualised intermittent theta burst stimulation in the prefrontal cortex: A TMS‐EEG study

Hippocampal-Prefrontal Interactions during Spatial Decision-Making

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