The difference between uni- and bilateral auditory phantom percept

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Abstract

Objective

Tinnitus can be considered an auditory phantom percept, in which patients hear an internal sound in the absence of any external sound source, mimicking tonal memory. Tinnitus however can be perceived exclusively uni- or bilaterally.

Methods

The neurophysiological differences were investigated between unilateral and bilateral tinnitus using LORETA source localized resting state EEG recordings.

Results

The difference between unilateral and bilateral tinnitus is reflected by high frequency activity (beta and gamma) in the superior prefrontal gurus, right parahippocampus, right angular gyrus and right auditory cortex. Unilateral tinnitus is characterized by contralateral beta2 in the superior prefrontal gyrus in comparison to bilateral tinnitus, but gamma in comparison to non-tinnitus subjects. Bilateral tinnitus has delta activity in the ventrolateral prefrontal cortex in comparison to unilateral tinnitus, and bilateral beta1 in comparison to non-tinnitus subjects. Bilateral tinnitus is also characterized by bilateral frontopolar beta1 activity.

Conclusions

Unilateral and bilateral tinnitus can be differentiated based on their resting state oscillation patterns: beta3 and gamma-band activity in the superior premotor cortex, parahippocampal area and angular gyrus seem to form the core of a spatial localization network involved in tinnitus.

Significance

These differences should be taken into account when evaluating functional neuroimaging data relating to tinnitus.

Introduction

Tinnitus is an auditory phantom percept, where patients hear an internal sound in the absence of any external sound source. In the population 10–15% experience tinnitus chronically and about 6–25% of the affected people report interference with their lives, as tinnitus causes a considerable amount of distress (Axelsson and Ringdahl, 1989, Baguley, 2002, Eggermont and Roberts, 2004, Heller, 2003). Typically, pain, concentration problems, depression, anxiety, irritability, sleep disturbances, and intense worrying are perceived to be significantly more severe within tinnitus patients (Erlandsson and Holgers, 2001). Hence, this phantom sound can be extremely disruptive and debilitating leading many patients to seek medical attention.

In daily situations, an external sound is perceived bilaterally (Mayer et al., 2009, Wang et al., 2009). In contrast, tinnitus, which is an internal sound, can be experienced exclusively uni- or bilaterally. Previous research reported bilateral tinnitus in 52% of patients (Chermak and Dengerink, 1987). When hearing loss is more severe in the right ear, there is right-sided tinnitus and, when hearing loss is more pronounced in the left ear, the tinnitus is bilateral or more pronounced on the right (Cahani et al., 1984, Nageris et al., 2010). However, phantom pain which can be considered the somatosensory analogue for tinnitus (De Ridder et al., 2007, Moller, 2000, Tonndorf, 1987) is usually perceived unilaterally (Flor et al., 1995, Lockwood et al., 1999). No study to date has looked into the neurophysiological differences between unilateral and bilateral tinnitus, although this could lead to a better understanding of the pathophysiology of tinnitus. Hence, it might be interesting to further explore the perceived spatial localization in tinnitus.

Tinnitus is correlated to gamma-band activity in the auditory cortex (Llinas et al., 1999, van der Loo et al., 2009, Weisz et al., 2007) contralaterally to where the unilateral tinnitus is perceived (Giraud et al., 1999, Lockwood et al., 1998, Smits et al., 2007, van der Loo et al., 2009, Weisz et al., 2007). Bilateral tinnitus could be correlated to bilateral activation in the auditory cortex, similar to perceiving an external sound which usually also evokes bilateral gamma-band activity in the auditory cortex (Pantev et al., 1991a, Pantev et al., 1991b). In contrast, other researchers claim that tinnitus is typically generated in the left auditory cortex, irrespective how tinnitus is perceived (Andersson et al., 2000, Arnold et al., 1996, Schlee et al., 2009).

New insights into the neurobiology of tinnitus suggest that neuronal changes are not limited to the classical auditory pathways. In particular the dorsolateral prefrontal cortex (Alain et al., 1998, Knight et al., 1989, Lewis et al., 2000, Voisin et al., 2006), anterior cingulate cortex (Mirz et al., 2000, Muhlau et al., 2006, Vanneste et al., 2010), and (para)hippocampus (De Ridder et al., 2006, Landgrebe et al., 2009, Vanneste et al., 2010) seem to be involved in tinnitus too, and it has recently been investigated how these areas co-activate (Schlee et al., 2009). Non-auditory brain areas might be important for the difference between unilateral and bilateral tinnitus as well.

The objective of the present study was to verify the neurophysiological differences between unilateral and bilateral in a homogenous but large group of tinnitus patients using source localized resting state EEG recordings.

Section snippets

Participants

Sixty-two patients (N = 62; 30 males and 32 females) with strictly narrow band noise tinnitus with a mean age of 54.43 were selected from the multidisciplinary Tinnitus Research Initiative (TRI) Clinic of the University Hospital of Antwerp, Belgium. Patients were selected based on their tinnitus lateralization. All patients had tinnitus for more than 1 year and perceive this continuously. Individuals with pulsatile tinnitus, Ménière disease, otosclerosis, chronic headache, neurological disorders

Unilateral versus bilateral tinnitus

sLORETA yielded significant differences between unilateral and bilateral tinnitus patients (p < .05) (see Fig. 1). Increased activity was revealed in the left inferior ventrolateral prefrontal cortex (LFG; BA47) for delta, and the parahippocampus (PHC; BA37), angular gyrus (BA39) and the auditory cortex area (sAC; BA22) for both beta3 and gamma for unilateral tinnitus patients in comparison to bilateral tinnitus patients. In addition, we found decreased activity within beta2 in the right superior

Discussion

The main objective was to characterize the neurophysiological differences in unilateral versus bilateral tinnitus. Differences were demonstrated with increased synchronized activity in the ventrolateral prefrontal cortex and decreased synchronized activity in the superior premotor cortex, the parahippocampus, angular gyrus and the secondary auditory cortex area. These areas overlap with areas involved in tonal memory. Tonal memory activates a network comprising ventrolateral prefrontal cortex

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