TY - JOUR
T1 - The absence of resting-state high-gamma cross-frequency coupling in patients with tinnitus
AU - Ahn, Min Hee
AU - Hong, Sung Kwang
AU - Min, Byoung-Kyong
N1 - Funding Information:
This work was supported by the Basic Science Research program (grant numbers 2015R1A1A1A05027233 to BKM; 2017M3A9G1027932 to SKH), the ICT R&D program of MSIP/Institute for Information & Communications Technology Promotion (IITP; grant number 2017-0-00432 to BKM), and the Information Technology Research Center (ITRC) support program (grant number IITP-2017-2016-0-00464 to BKM) supervised by the IITP, which are funded by the Korean government (MSIT) through the National Research Foundation of Korea . The authors declare that they have no competing interests.
Publisher Copyright:
© 2017 The Authors
PY - 2017/12
Y1 - 2017/12
N2 - Tinnitus is a psychoacoustic phantom perception of currently unknown neuropathology. Despite a growing number of post-stimulus tinnitus studies, uncertainty still exists regarding the neural signature of tinnitus in the resting-state brain. In the present study, we used high-gamma cross-frequency coupling and a Granger causality analysis to evaluate resting-state electroencephalographic (EEG) data in healthy participants and patients with tinnitus. Patients with tinnitus lacked robust frontal delta-phase/central high-gamma-amplitude coupling that was otherwise clearly observed in healthy participants. Since low-frequency phase and high-frequency amplitude coupling reflects inter-regional communication during cognitive processing, and given the absence of frontal modulation in patients with tinnitus, we hypothesized that tinnitus might be related to impaired prefrontal top-down inhibitory control. A Granger causality analysis consistently showed abnormally pronounced functional connectivity of low-frequency activity in patients with tinnitus, possibly reflecting a deficiency in large-scale communication during the resting state. Moreover, different causal neurodynamics were characterized across two subgroups of patients with tinnitus; the T1 group (with higher P300 amplitudes) showed abnormal frontal-to-auditory cortical information flow, whereas the T2 group (with lower P300 amplitudes) exhibited abnormal auditory-to-frontal cortical information control. This dissociation in resting-state low-frequency causal connectivity is consistent with recent post-stimulus observations. Taken together, our findings suggest that maladaptive neuroplasticity or abnormal reorganization occurs in the auditory default mode network of patients with tinnitus. Additionally, our data highlight the utility of resting-state EEG for the quantitative diagnosis of tinnitus symptoms and the further characterization of tinnitus subtypes.
AB - Tinnitus is a psychoacoustic phantom perception of currently unknown neuropathology. Despite a growing number of post-stimulus tinnitus studies, uncertainty still exists regarding the neural signature of tinnitus in the resting-state brain. In the present study, we used high-gamma cross-frequency coupling and a Granger causality analysis to evaluate resting-state electroencephalographic (EEG) data in healthy participants and patients with tinnitus. Patients with tinnitus lacked robust frontal delta-phase/central high-gamma-amplitude coupling that was otherwise clearly observed in healthy participants. Since low-frequency phase and high-frequency amplitude coupling reflects inter-regional communication during cognitive processing, and given the absence of frontal modulation in patients with tinnitus, we hypothesized that tinnitus might be related to impaired prefrontal top-down inhibitory control. A Granger causality analysis consistently showed abnormally pronounced functional connectivity of low-frequency activity in patients with tinnitus, possibly reflecting a deficiency in large-scale communication during the resting state. Moreover, different causal neurodynamics were characterized across two subgroups of patients with tinnitus; the T1 group (with higher P300 amplitudes) showed abnormal frontal-to-auditory cortical information flow, whereas the T2 group (with lower P300 amplitudes) exhibited abnormal auditory-to-frontal cortical information control. This dissociation in resting-state low-frequency causal connectivity is consistent with recent post-stimulus observations. Taken together, our findings suggest that maladaptive neuroplasticity or abnormal reorganization occurs in the auditory default mode network of patients with tinnitus. Additionally, our data highlight the utility of resting-state EEG for the quantitative diagnosis of tinnitus symptoms and the further characterization of tinnitus subtypes.
KW - Causality
KW - Cross-frequency coupling
KW - Electroencephalogram
KW - Phase-amplitude coupling
KW - Resting state
KW - Tinnitus
UR - http://www.scopus.com/inward/record.url?scp=85033677639&partnerID=8YFLogxK
U2 - 10.1016/j.heares.2017.10.008
DO - 10.1016/j.heares.2017.10.008
M3 - Article
C2 - 29097049
AN - SCOPUS:85033677639
VL - 356
SP - 63
EP - 73
JO - Hearing Research
JF - Hearing Research
SN - 0378-5955
ER -