Top-down and bottom-up neurodynamic evidence in patients with tinnitus

Sung Kwang Hong, Sejik Park, Min Hee Ahn, Byoung-Kyong Min

Research output: Contribution to journalArticlepeer-review

35 Citations (Scopus)

Abstract

Although a peripheral auditory (bottom-up) deficit is an essential prerequisite for the generation of tinnitus, central cognitive (top-down) impairment has also been shown to be an inherent neuropathological mechanism. Using an auditory oddball paradigm (for top-down analyses) and a passive listening paradigm (for bottom-up analyses) while recording electroencephalograms (EEGs), we investigated whether top-down or bottom-up components were more critical in the neuropathology of tinnitus, independent of peripheral hearing loss. We observed significantly reduced P300 amplitudes (reflecting fundamental cognitive processes such as attention) and evoked theta power (reflecting top-down regulation in memory systems) for target stimuli at the tinnitus frequency of patients with tinnitus but without hearing loss. The contingent negative variation (reflecting top-down expectation of a subsequent event prior to stimulation) and N100 (reflecting auditory bottom-up selective attention) were different between the healthy and patient groups. Interestingly, when tinnitus patients were divided into two subgroups based on their P300 amplitudes, their P170 and N200 components, and annoyance and distress indices to their tinnitus sound were different. EEG theta-band power and its Granger causal neurodynamic results consistently support a double dissociation of these two groups in both top-down and bottom-up tasks. Directed cortical connectivity corroborates that the tinnitus network involves the anterior cingulate and the parahippocampal areas, where higher-order top-down control is generated. Together, our observations provide neurophysiological and neurodynamic evidence revealing a differential engagement of top-down impairment along with deficits in bottom-up processing in patients with tinnitus but without hearing loss.

Original languageEnglish
Pages (from-to)86-100
Number of pages15
JournalHearing Research
Volume342
DOIs
Publication statusPublished - 2016 Dec 1

Bibliographical note

Funding Information:
This work was supported by the Basic Science Research program [grant number 2015R1A1A1A05027233 to BKM; 2014R1A1A2A16054791 to SKH], which is funded by the Ministry of Science, ICT, and Future Planning through the National Research Foundation of Korea. The authors would like to thank Jung-Hye Park for her help during data acquisition. The authors declare that they have no competing interests.

Publisher Copyright:
© 2016 The Authors

Keywords

  • Attention
  • Causality
  • Electroencephalogram
  • Tinnitus
  • Top-down

ASJC Scopus subject areas

  • Sensory Systems

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