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Table 2 Human findings regarding theta-gamma coupling (TGC)

From: Disturbed theta and gamma coupling as a potential mechanism for visuospatial working memory dysfunction in people with schizophrenia

Authors & Year of Publication Subjects Measure Region of Brain/Scalp Examined Task Performed/Behavior during Measurement WM Subprocess(es) Analyzed Relevant Findings Conclusions
Studies utilizing intracranial EEG (iEEG)
i. Fell et al. (2003) [106] 9 patients with pharmacoresistant temporal lobe epilepsy iEEG Hippocampus, entorhinal cortex Single-trial word list learning paradigm Encoding - Phase-phase TGC across the rhinal cortex and hippocampus during WM encoding
- Coupling greater for words successfully recalled
TGC crucial to actual memory formation rather than general state of WM encoding
ii. Mormann et al. (2005) [76] 12 patients with pharmacoreistant temporal lobe epilepsy (5 women, aged 40.3 ± 10.1 years) iEEG Hippocampus, rhinal cortex Continuous visual word recognition paradigm Continuous recognition (Combination of encoding and retrieval) - Modulation of gamma- amplitude by theta- phase in both rhinal cortex hippocampus
- Rhinal modulation greatest for correct rejections, hippocampal modulation greatest for hits
Phase-amplitude TGC may underlie encoding processes in rhinal cortex and retrieval processes in hippocampus
iii. Axmacher et al. (2010) [33] 14 participants with pharmacoresistant temporal lobe epilepsy (3 female, aged 38.3 ± 11.8 years) iEEG Hippocampus Visual analogue of Sternberg task Maintenance - Theta phase to gamma power TGC increased during maintenance compared to baseline
- More precise coupling associated with faster reaction times
- Increased WM load related to less modulation of gamma
- Medial temporal lobe involved in WM when multiple stimuli are to be maintained
- TGC functionally relevant to WM processes
iv. Canolty et al. (2006) [61] 5 females (aged 24 to 45 years) iEEG Frontal, temporal, parietal lobes - Passive listening
- Active listening/target detection
- Picture naming
- Verb generation
- Finger tapping
- Mouth movement & articulation
- Auditory/vibrotactile stimulus presentation with unimodal target detection
- Auditory N-back task
- Visual search task
- Visual silent reading task
- Facial emotion recognition task
- Motor, auditory and tactile imagery
Unclear - Strong modulation of gamma throughout examined areas by theta phase across all tasks; highest modulation in high gamma (80–150Hz)
- Largest gamma amplitudes occur at trough of theta
TGC coordinates various cortical regions for purposeful activity
v. van der Meij, Kahana, & Maris (2012) [107] 27 patients (12 female) with pharmacoresistant epilepsy iEEG Frontal, temporal, parietal, occipital, limbic Sternberg task Encoding, maintenance Widespread phase-amplitude coupling between multiple frequency bands across distances greater than 10 cm between sensors spread throughout cortex and other measured areas - Phase-amplitude coupling is pervasive, has a wide spatial distribution, and varies greatly in terms of frequencies involved and phases preferred
- As such, phase-amplitude coupling likely involved in various forms of selective communication between brain areas
vi. Maris, van Vugt, & Kahana (2011) [108] 26 patients with implanted electrodes for purpose of presurgical diagnosis iEEG Varied from patient-to-patient, but included frontal, temporal and parietal sites Sternberg task Encoding, maintenance - Phase to amplitude coupling widely distributed across frequency as well as location; included frontal, temporal and parietal sites
-TGC most prominent in within-electrode analyses
- Phase-amplitude coupling increased in some areas during WM and decreased in others
- In most coupling patterns, high-frequency bursts are synchronized across locations
- WM processes affect coupling heterogeneously, depending on location and frequencies involved
- Phase-amplitude coupling important to coordination of neural activity spatiotemporally
vii. Chaieb et al. (2015) [34] 14 patients with pharmacoresistant temporal lobe epilepsy iEEG Hippocampus Modified Sternberg paradigm featuring facial stimuli Maintenance - Increases in phase-phase TGC observed for multi-item but not single-item trials for coupling factor of 6 (e.g., 6 gamma cycles to 1 theta cycle)
- Changes in coupling measures across WM loads predicted WM capacities
TGC particularly important to multi-item WM
Studies utilizing scalp-level recordings
viii. Schack, Vath, Petsche, Geissler, & Mӧller (2002) [70] 10 right-handed female adults (aged 25 to 35 years) Scalp EEG Frontal, prefrontal, frontopolar regions Sternberg tasks featuring number words and random figures Encoding, maintenance and retrieval - Phase-coupling between theta activity over frontal areas and gamma activity over frontopolar areas during maintenance of number words TGC is prominent during human maintenance of information in WM, supporting Lisman & Idiart’s [1] model
ix. Baerbel Schack & Weiss (2005) [109] 23 females (aged 23.7 ± 2.7 years) Scalp EEG Scalp-wide Single-trial word list learning paradigm Encoding - Increased frontocentral phase-phase TGC for words later recalled vs. those not
- Phase-phase TGC also observed between Fz and Cz
Gabor expansion is a useful means of assessing phase-phase TGC from scalp EEG
x. Sauseng, Klimesch, Gruber, & Birbaumer (2008) [69] 22 analyzed patients (19 females, average age of 23.6 years) Scalp EEG Scalp-wide Cued visual attention task Target presentation - Phase-phase TGC over posterior areas enhanced by attention shift to cued visual field
- Stronger TGC over areas contralateral to cued visual field
Phase-phase TGC over posterior areas reflects matching of stored information to incoming visual input
xi. Sauseng et al. (2009) [32] 21 right-handed participants (15 females, aged 23.9 ± 4.4 years) Scalp EEG Scalp-wide Visuospatial delayed match-to-sample task Maintenance - Phase-amplitude TGC over bilateral parietal and occipital sites
- Phase-phase TGC modulated by WM load over right posterior sites, exclusive to relevant information
- Degree of phase-phase TGC modulation by WM load predictive of WM capacity
- TGC, and particularly phase-phase relationships, are central to visual WM function
- Independent mechanisms for maintenance of relevant vs. suppression of irrelevant info
xii. (Holz, Glennon, Prendergast, & Sauseng (2010) [68] 18 participants (13 female, aged 23.67 ± 2.99 years) Scalp EEG Scalp-wide Visuospatial delayed match-to-sample task Retrieval - Increased phase-phase TGC over parieto-occipital brain regions soon after probe presentation
- Matching increased TGC in right hemisphere; non-matching increased TGC in left hemisphere
Comparison of stored information to visual inputs leads to phase-phase TGC over parieto-occipital regions
xiii. Park, Lee, & Lee (2011) [36] 31 older participants (19 females, aged 66.45 ± 5.75 years) Scalp EEG Scalp-wide Spatial delayed match-to-sample task Maintenance - TGC between theta phase and gamma power across scalp, enhanced in left centro-parietal regions
- Strength of TGC at FP1 predicted task performance
- Strength of TGC at P8 predicted delayed figure recall performance
TGC is important to visual memory function (e.g., parietal correlation) but may also reflect attentional processes (e.g., prefrontal correlation)
xiv. Park, Jhung, Lee, & An (2013) [35] 13 right-handed participants (5 females, aged 20.8 ± 3.1 years) Scalp EEG Scalp-wide Visuospatial 2-back task, vigilance task Maintenance TGC between theta phase and gamma power most prominent over prefrontal areas in WM task but not vigilance task TGC recorded from scalp represents WM processes rather than attentional processes
xv. Lee & Yang (2014) [110] 9 right-handed males (aged 21.22 ± 0.97 years) Scalp EEG Scalp-wide Visuospatial delayed match-to-sample task Maintenance Strength of phase-phase TGC at P8 predicted task performance Phase-phase TGC can be used as a measure of WM ability
xvi. Vosskuhl, Huster, & Herrmann (2015) [111] 33 right-handed participants (14 females, aged 25.74 ± 2.69 years) Scalp EEG F3, Fz, F4, C3, Cz, C4 Transcranial alternating current stimulation; digit span task; 3-back task Encoding during stimulation - Short-term memory capacity as assessed using forward digit span was increased during stimulation
- Theta amplitude increased after stimulation
Supports theory that the length of theta cycle (e.g., theta frequency) limits how many gamma cycles can be superimposed upon it
xvii. Heusser, Poeppel, Ezzyat, & Davachi (2016) [77] 20 right-handed males (aged 21–25; mean age 28) MEG Scalp-wide; left lateral and posterior clusters of sensors used for analyses Visual temporal order memory paradigm Encoding - Peak of gamma power shifted progressively later with memory stimuli progressively later in presented sequence
- Relative gamma peaks reflected the order of stimulus presentation in sequence
Strongly supports notion that the sequential order of stimuli is encoded using a theta-gamma code
xviii. Alekseichuk, Turi, de Lara, Antal, & Paulus (2016) [112] 47 healthy people (25 females, aged 19–28) Scalp EEG Scalp-wide Transcranial alternating current stimulation; 2-back visuospatial memory test Encoding/retrieval during stimulation - Transcranial alternating current stimulation improved task performance and increased phase connectivity across scalp
- 80Hz to 100Hz stimulation during theta peak produced optimal effects
- Transcranial current in gamma frequency range improved WM performance
- High gamma may be particularly important to WM-related coupling
  1. WM working memory, TGC theta-gamma coupling, iEEG intracranial EEG, LFP local field potential, CSD current source density, EC entorhinal cortex, HFO high-frequency oscillation, ACC anterior cingulate cortex, PFC prefrontal cortex