Table 1.
Cross-frequency phase-amplitude coupling alterations in animal models of AD and DS.
| Reference | Animal model | Age (months) | Type of study | Brain area (s) recorded | Recording conditions | Brain oscillations studied | Type of alteration observed | Type of index used |
|---|---|---|---|---|---|---|---|---|
| Goutagny et al., 2013 | TgCRND8 mice | 1-month-old | In vitro | Hippocampus (subicular area) | Spontaneous LFP activity. | Theta (3-12 Hz) and fast gamma (120-250 Hz) oscillations. | Decrease in theta-fast gamma phase-amplitude coupling. | Tort et al., 2008 |
| Ittner et al., 2014 | APP23 mice | 4-month-old | In vivo | Hippocampus | Spontaneous LFP activity was recorded during freely-roaming condition. | Theta (4-12 Hz) and gamma (25-100 Hz) oscillations. | Decrease in theta-gamma phase-amplitude coupling. | Tort et al., 2008 |
| Kalweit et al., 2015 | Aβ(1-42)-treated rats | 6-month-old | In vivo | Hippocampus (dentate gyrus area) | LFP activity was recorded during high-frequency stimulation (HFS) of the perforant path-dentate gyrus synapse in freely-behaving rats. | Theta (4-10 Hz) and gamma (30-100 Hz) oscillations. | Decrease in theta-gamma phase-amplitude coupling. | Bruns and Eckhorn, 2004 |
| Booth et al., 2016 | rTg4510 mice | 7- to 8-month-old | In vivo | Hippocampus (CA1 area) | LFP activity was recorded while mice runned from end to end in a linear track for appetitive rewards. | Theta (4-12 Hz) and gamma (25-120 Hz) oscillations. | Decrease in theta-gamma phase-amplitude coupling. | Canolty et al., 2006 |
| Stoiljkovic et al., 2016 | 5xFAD mice | 8-month-old | In vivo | Hippocampus (CA1 area) | Stimulation-induced (electrical stimulation of the nucleus pontis oralis) hippocampal LFP activity. Recordings were done under urethane anesthesia. | Theta (3-12 Hz), low (30-50 Hz) and high gamma (75-95 Hz) oscillations. | Decrease in theta-high gamma phase-amplitude coupling. | Tort et al., 2008 |
| Zhang et al., 2016 | APP knockout (APP-KO) mice | 9-month-old | In vivo | Hippocampus (CA1 area), medial prefrontal cortex, and posterior parietal cortex | Spontaneous LFP activity was recorded during awake (freely-behaving) and REM sleep condition. | Theta (4-12 Hz), gamma (40-100 Hz) and fast gamma (120-160 Hz) oscillations. | Decreased parietal theta-gamma phase-amplitude coupling during awake and REM sleep. Decreased parietal theta-fast gamma phase-amplitude coupling during REM sleep. Decreased hippocampal theta-gamma phase-amplitude coupling during awake and REM sleep. Decreased prefrontal-hippocampal theta-gamma phase-amplitude coupling during awake. | Tort et al., 2008 |
| Fontana et al., 2017 | PS2APP mice | 6- and 12-month-old | In vivo | Hippocampus (dentate gyrus area) | Spontaneous LFP activity was recorded under urethane anesthesia. | Theta (1.7-4.7 Hz), beta (10-25 Hz), slow gamma (25-40 Hz), fast gamma (45-90 Hz), and oscillations epsilon (110-190 Hz). | Increased theta-beta and theta-slow gamma phase-amplitude couplings (6-month-old). Decreased theta-epsilon phase-amplitude coupling (12-month-old). | Penny et al., 2008 |
| Joo et al., 2017 | TgF344-AD rats | 9-month-old | In vivo | Somatosensory cortex | Spontaneous LFP activity was recorded during resting-state condition. | Theta (4-8 Hz) and gamma (30-140 Hz) oscillations. | Decrease in theta-gamma phase-amplitude coupling. | Canolty et al., 2006 |
| Mably et al., 2017 | 3xTg mice | 8- to 9-month-old | In vivo | Hippocampus (CA1 area) | LFP activity was recorded while mice unidirectionally runned around a circular track for appetitive rewards. | Theta (4-12 Hz), slow (25-40 Hz) and fast gamma (65-100 Hz) oscillations. | Decrease in theta-slow gamma phase-amplitude coupling. | Colgin et al., 2009 |
| Nakazono et al., 2017 | APP knock-in (APP-KI) mice | 5-month-old | In vivo | Medial entorhinal cortex | Spontaneous LFP activity was recorded under urethane anesthesia. | Theta (5-10 Hz) and gamma (30-100 Hz) oscillations. | Decrease in theta-gamma phase-amplitude coupling. | Lengths of resultant vectors of theta phase distributions of gamma oscillation maxima were used as an index for theta-gamma coupling. |
| Tanninen et al., 2017 | P301L-mutant human tau-expressing rats | not reported | In vivo | Hippocampus and medial prefrontal cortex | LFP activity was recorded while rats performed trace eyeblink conditioning (TEBC). | Theta (6-12 Hz) and gamma (30-100 Hz) oscillations. | Increased prefrontal theta-gamma phase-amplitude coupling. Decreased prefrontal-hippocampal theta-gamma phase-amplitude coupling. | Tort et al., 2008 |
| Bazzigaluppi et al., 2018 | TgF344-AD rats | 9-month-old | In vivo | Hippocampus and medial prefrontal cortex | Spontaneous LFP activity was recorded during resting-state condition. | Theta (3-9 Hz), low (30-58 Hz) and high gamma (62-120 Hz) oscillations. | Decrease in theta-high gamma phase-amplitude coupling in both hippocampus and medial prefrontal cortex. | Canolty et al., 2006 |
| Mondragón-Rodríguez et al., 2018 | J20 mice | 1-month-old | In vitro | Hippocampus (subicular area) | Spontaneous LFP activity. | Theta (2-12 Hz), slow (25-55 Hz) and fast gamma (150-250 Hz) oscillations. | Decrease in both theta-slow and theta-fast gamma phase-amplitude couplings. | Tort et al., 2008 |
| Etter et al., 2019 | J20 mice | 6-month-old | In vivo | Hippocampus (CA1 area) | LFP activity was recorded while mice freely explored a circular platform. | Theta (6-12 Hz) and gamma (30-60 Hz) oscillations. | Decrease in hippocampal theta-slow gamma phase-amplitude coupling. | Belluscio et al., 2012 and Tort et al., 2008 |
| Leparulo et al., 2019 | PS2APP, PS2.30H, and APPSwe mice | 3- and 6-month-old | In vivo | Hippocampus (CA1 area) and posterior parietal cortex | Spontaneous LFP activity was recorded under a mixture of urethane and xylazine/tiletamine-zolazepam anesthesia. | Slow (SO; 0.1-1.7 Hz) and fast gamma (45-90 Hz) oscillations. | Decreased parietal-hippocampal SO-fast gamma coupling in 3- and 6-month-old PS2.30H mice. Decreased parietal-hippocampal SO-fast gamma coupling in 6-month-old PS2APP and APPSwe mice. | Penny et al., 2008 |
| Stoiljkovic et al., 2019 | TgF344-AD rats | 12-month-old | In vivo | Hippocampus (CA1 area) | Stimulation-induced (electrical stimulation of the nucleus pontis oralis) hippocampal LFP activity. Recordings were done under urethane anesthesia. | Theta (3-9 Hz), low (30-55 Hz), and high gamma (65-95 Hz) oscillations. | Decrease in both theta-low and -high gamma phase-amplitude coupling. | Tort et al., 2008 |
| Ahnaou et al., 2020 | P301S mice | 3-, 6-, and 9-month-old | In vivo | Hippocampus (CA1 area), olfactory bulb, frontal cortex, and lateral entorhinal cortex | Spontaneous LFP activity was recorded in freely-behaving mice. | Theta (4-8 Hz) and gamma (40-100 Hz) oscillations. | Decreased theta-gamma phase-amplitude coupling in the olfactory bulb. | Canolty et al., 2006 |
| Alemany-González et al., 2020 | Ts65Dn mice | 2- to 3-month-old | In vivo | Hippocampus (CA1 area) and medial prefrontal cortex | Spontaneous LFP activity was recorded during quiet wakefulness condition. | Delta (3-5 Hz), theta (6-12 Hz), high gamma (80-120 Hz), and high frequency (100-200 Hz) oscillations. | Increased prefrontal delta-high gamma phase-amplitude coupling and increased hippocampal theta-high frequency phase-amplitude coupling. | Tort et al., 2008 |
| Chang et al., 2020 | Dp1Tyb and Dp10Yey mice | 3- to 9-month-old | In vivo | Hippocampus and medial prefrontal cortex | LFP activity was recorded while mice performed a spontaneous alternation task. | Theta (6-12 Hz), low (60-120 Hz), and high gamma (140-160 Hz) oscillations. | Increased hippocampal theta-high gamma phase-amplitude coupling and increased theta-band coherence between the hippocampus and mPFC in Dp1Tyb mice. Decreased hippocampal theta-low gamma phase-amplitude coupling in Dp10Yey mice. | Colgin et al., 2009 |
| Kumari et al., 2020 | APP/PS1 mice | 6-month-old | In vivo | Hippocampus (dentate gyrus area) and dentate gyrus-perforant pathway | LFP activity was recorded following electrical stimulation of the perforant pathway. Recordings were done under urethane anesthesia. | Theta (3-8 Hz), low (30-50 Hz), and high gamma (50-100 Hz) oscillations. | Decreased theta-low and -high gamma phase-amplitude coupling in both dentate gyrus area and dentate gyrus-perforant pathway. | Cheng et al., 2016 |
| Park et al., 2021 | 5xFAD mice | 6-month-old | In vivo | Frontal and parietal areas | Spontaneous EEG was recorded in freely-behaving mice. | Delta (2-5 Hz), theta (5-8 Hz) and gamma (30-80 Hz) oscillations. | Decreased frontal-parietal delta-gamma phase-amplitude coupling. Decreased parietal-frontal theta-gamma phase-amplitude coupling. | Combrisson et al., 2020 |
| Leparulo et al., 2022 | PS2APP mice | 6- and 12-month-old | In vivo | Hippocampus (CA1 area) and posterior parietal cortex | Spontaneous LFP activity was recorded under a mixture of urethane and xylazine/tiletamine-zolazepam anesthesia. | Slow (SO; 0.1-1.7 Hz) and fast gamma (45-90 Hz) oscillations. | Decreased hippocampal-parietal SO-fast gamma coupling. Decreased parietal-hippocampal SO-fast gamma coupling. | Penny et al., 2008 |
| Tok et al., 2022 | Tau-seeded APP-KINL-G-F and APP-KINL mice | 3- and 6-month-old | In vivo | Hippocampus (CA1 area) | Spontaneous LFP activity was recorded in freely-behaving mice. | Theta-1 (4-6 Hz), theta-2 (6-8 Hz), low gamma (30-50 Hz) and high gamma (51-80 Hz) oscillations. | Decreased theta2-high gamma phase-amplitude coupling in both mouse models and age groups one day after injection. | Tort et al., 2008 |