Elsevier

Neurobiology of Aging

Volume 34, Issue 7, July 2013, Pages 1853-1863
Neurobiology of Aging

Regular article
“Distressed aging”: the differences in brain activity between early- and late-onset tinnitus

https://doi.org/10.1016/j.neurobiolaging.2013.01.014Get rights and content

Abstract

Recent findings regarding different characteristics according to the age of tinnitus onset prompted us to conduct a study on the differences in tinnitus-related neural correlates between late-onset tinnitus (LOT; mean onset age, 60.4 years) and early-onset tinnitus (EOT; mean onset age, 29.7 years) groups. Hence, we collected quantitative electroencephalography findings of 29 participants with LOT and 30 with EOT, and from 59 controls. We then compared the results between the 2 groups and between the tinnitus groups and age- and sex-matched control groups using resting state electroencephalography source-localized activity and connectivity analyses. Compared with the EOT and older control groups, the LOT group demonstrated increased localized activity and functional connectivity in components of previously described tinnitus distress networks, and the default mode and intrinsic alertness networks, such as the prefrontal cortices, dorsal anterior cingulate cortex, and insula. The current findings of intrinsic differences in tinnitus-related neural activity between the LOT and EOT groups might be applicable for planning individualized treatment modalities according to age of onset. Moreover, differences with regard to the age of tinnitus onset might be a milestone for future studies on onset-related differences in other similar pathologies, such as pain or depression.

Introduction

Tinnitus is an auditory phantom phenomenon of a sound perception in the absence of any objective physical sound source (Jastreboff, 1990). Tinnitus afflicts 5%–15% of the western population, and tinnitus severely affects the quality of life for 2–3 in 100 individuals, because it causes a considerable amount of distress (Heller, 2003). The neurobiological basis of tinnitus is characterized by an ongoing abnormal spontaneous activity and reorganization of the auditory central nervous system (Moazami-Goudarzi et al., 2010; Weisz et al., 2005b). However, nonauditory brain structures, such as the dorsolateral prefrontal cortex (DLPFC), anterior cingulate cortex (ACC), amygdala, and the parahippocampus, have been suggested to be associated with the perception of tinnitus and its salience, tinnitus-related distress, and tinnitus memory (De Ridder et al., 2011a).

Tinnitus is more problematic for the geriatric population, because more than 30% of adults aged 55–99 years report having experienced tinnitus (Sindhusake et al., 2003). Further, the prevalence of chronic tinnitus increases with age, peaking at 60–69 years of age (Shargorodsky et al., 2010). This high prevalence of tinnitus in the geriatric population can been partly explained by the fact that hearing loss is an important risk factor for tinnitus, and that the prevalence of hearing loss increases with age (Spoor, 1967). Additionally, recent studies have discovered that late-onset tinnitus (LOT) differs from early-onset tinnitus (EOT) not only with regard to prevalence, but also with regard to tinnitus-related distress. That is, participants with LOT are more abruptly distressed and suffer significantly more than those with EOT (Schlee et al., 2011).

These differences in tinnitus-related distress according to age at onset might be related to differences in neural correlates associated with tinnitus between LOT and EOT individuals. Considering that aging is associated with functional disruption or underrecruitment of cortical networks (Logan et al., 2002) and compensatory cortical recruitment (Davis et al., 2008), and that neuroplastic processes play a crucial role in the generation of tinnitus and its related distress, we hypothesized that neural correlates involved in the generation of tinnitus and related distress might be different between LOT and EOT groups. These potential differences might lead to different treatment options for patients with EOT and LOT.

Hence, it is essential to perform a study that examines the differences in neural correlates associated with tinnitus between LOT and EOT groups. By matching all known affecting factors for tinnitus, excluding age of onset, we would obtain onset-related differences in the neural correlates for tinnitus-related distress. Moreover, by comparing differences in these results between young and old control groups, we explored whether these results merely originated from the normal aging process. We further attempted to unravel the distinct nature of the tinnitus brain, the possibility of individualized treatment modalities according to the age of onset, and a possible universal mechanism that might be found in other pathologies.

Hereinafter, we describe our results, which were analyzed by source-localized quantitative electroencephalography, and discuss possible explanations for the differences.

Section snippets

Participants

To recruit a homogenous study group with regard to tinnitus characteristics, we selected participants with narrow-band noise (NBN) bilateral tinnitus from the database of the multidisciplinary Tinnitus Research Initiative Clinic at the University Hospital of Antwerp, Belgium. Individuals with pulsatile tinnitus, Ménière's disease, otosclerosis, chronic headache, hearing loss exceeding the range of serviceable hearing (40 dB) (Farrior, 1956) in at least 1 ear, neurological disorders such as

The LOT group versus the EOT group

Compared with the EOT group, the LOT group showed significantly increased activities in the DLPFC (BA 9), the left side for beta3, and bilaterally for the gamma frequency bands in the right orbitofrontal cortex (OFC; BA 10) for the gamma, in the right supplementary motor area (BA 6) for the beta1, and in the right superior frontal gyrus (BA 8) for the beta2 frequency band extending into the right dorsal anterior cingulate cortex (dACC; BA 24). In contrast, delta band activity in the bilateral

Discussion

Recent examinations of normal healthy aging have revealed that anatomical and functional changes in the brain occur as we age and might be, at least partly, responsible for the age-related decline in cognitive functions (Backman et al., 2006; Raz and Rodrigue, 2006). Total brain volume declines with age (Giedd et al., 1999), with markedly accelerated loss in the insula, superior parietal gyri, central sulci, cingulate sulci, caudate, cerebellum, hippocampus, and the association cortices (Good

Disclosure statement

The authors disclose no conflicts of interest.

This study was approved by the local ethical committee at Antwerp University Hospital and was in accordance with the Declaration of Helsinki. Participants gave oral informed consent before the procedure. The EEG was obtained as a standard procedure for diagnostic and neuromodulation treatment purposes.

Acknowledgements

The authors thank Jan Ost, Bram Van Achteren, Bjorn Devree and Pieter van Looy for their help in preparing this manuscript. This research was supported by the Research Foundation Flanders (FWO), Tinnitus Research Initiative, TOP project University Antwerp, The Neurological Foundation of New Zealand, and Korean government (MOST) [Korea Science and Engineering Foundation (KOSEF) (no. 2012-0030102)].

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