Elsevier

Autonomic Neuroscience

Volume 165, Issue 2, 7 December 2011, Pages 191-194
Autonomic Neuroscience

Insular lateralization in tinnitus distress

https://doi.org/10.1016/j.autneu.2011.06.007Get rights and content

Abstract

Tinnitus affects 15% of the population. Of these 1–2% are severely disabled by it. The role of the autonomic system in tinnitus is hardly being investigated. The aim of this study is to investigate the relationship between tinnitus distress and lateralization of the anterior insula, known to be involved in interoceptive awareness and (para)sympathetic changes. For this, Tinnitus Questionnaire scores are correlated to Heart Rate Variability markers, and related to neural activity in left and right anterior insula. Our results show that tinnitus distress is related to sympathetic activation, in part mediated via the right anterior insula.

Introduction

Tinnitus is a symptom that affects 15% of the population (Axelsson and Ringdahl, 1989). Most people who have tinnitus can effectively cope with it, however a small percentage of tinnitus sufferers demonstrate maladaptive coping (Scott et al., 1990, Budd and Pugh, 1996, Tyler et al., 2006): 1–2% of tinnitus sufferers are severely disabled by their tinnitus (Axelsson and Ringdahl, 1989). This maladaptive coping group suffers significantly more from associated somatic complaints such as headaches, neck and shoulder pain, low back pain, muscle tension, sleep and concentration problems (Hiller et al., 1997, Scott and Lindberg, 2000) and demonstrates cognitive inefficiency (Hallam et al., 2004), poor stress coping (Scott and Lindberg, 2000) and depression (Harrop-Griffiths et al., 1987, Sullivan et al., 1988, Scott and Lindberg, 2000, Dobie, 2003, Folmer and Shi, 2004).

The amount of distress people experience related to tinnitus can be evaluated by the use of validated tinnitus questionnaires. Tinnitus distress is associated to a higher orthosympathetic (OS) tone (Datzov et al., 1999) and tinnitus suppression induces an increased parasympathetic (PS) tone (Matsushima et al., 1996). Previous functional imaging studies show that specific frontal cortical areas closely relate to emotion perception and interoception. The right anterior insula seems to be specifically involved in the representation of subjective feelings (Craig, 2003, Critchley et al., 2004). Based on human lesion and electrical stimulation studies it has also been suggested that the right insula controls cardiac OS activity whereas the left insula is predominantly associated to PS activity (Oppenheimer et al., 1992, Oppenheimer, 1993, Oppenheimer, 2006, Oppenheimer et al., 1996). Functional Magnetic Resonance Imaging (fMRI) studies of sympathetic skin conductance response seem to confirm this lateralization by revealing right insula activation (Critchley et al., 2000). Furthermore, when correlating dichotic visual stimuli with Heart Rate Variability (HRV) the same lateralization effect is found (Wittling et al., 1998a, Wittling et al., 1998b).

Heart Rate Variability (HRV) is a simple and non-invasive quantitative marker of autonomic function. As a result of continuous variations of the balance between OS and PS neural activity influencing heart rate, intervals between consecutive heartbeats (RR intervals) show spontaneously occurring oscillations. For HRV spectral analysis three main underlying frequencies have been used in literature: the very-low-frequency range (VLF  0.04 Hz), the low-frequency range (LF: 0.04–0.15 Hz) and the high frequency range (HF: 0.15–0.4 Hz). The high frequency component of HRV is believed to be influenced by vagal activity and is also related to the frequency of respiration (Yasuma and Hayano, 2004). Low-frequency (LF) power is modulated by baroreceptor activities and fluctuations in heart rate in the LF range reflect OS as well as PS influences. Low-frequency power, therefore, cannot be considered to reflect pure OS activity. However if normalized units of LF and HF are considered, the OS and PS influences respectively are emphasized (Electrophysiology, 1996). In HRV frequency domain, normalized units (n.u.) of LF and HF components therefore reflect OS and PS influences respectively.

The aim of this study is to investigate the relation between tinnitus distress and lateralisation of the anterior insula, known to be involved in interoceptive awareness and OS as well as PS changes. For this, tinnitus questionnaire (TQ) scores (Goebel and Hiller, 1994) are correlated to HRV markers, and related to neural activity in left and right anterior insula.

Section snippets

Methods

Ten patients with strictly right-sided unilateral tinnitus are analyzed. EEG and ECG signals are recorded simultaneously over 5 min in supine position using a 32 channel digital EEG (Neuroscan, Compumedics, Houston, TX) in a dimly illuminated and soundproof room (sampling rate = 500 Hz, band passed 0.15–100 Hz). Electrodes are referenced near the vertex and impedances checked to remain below 5 kΩ. To minimize respiratory influences on HRV, respiration is controlled at 12 bpm using auditory cues. All

Results

TQ-scores (M = 40.2; SD = 13.7) correlate positively with the OS marker, the Low Frequency normalized units (r = 0.58), and negatively with the PS marker, the High Frequency normalized units (r =  0.58).

In addition, current density analyses show that increased cortical activity in the left anterior insula at 11 Hz (r = 0.56; alpha band) and decreased activity at 4 Hz (r =  0.63; theta band) and in the high gamma band frequencies (54 Hz, r =  0.58; 59 Hz, r =  0.74) relate to increased TQ-scores. In the right

Discussion

Our results show a positive relation between OS load and tinnitus distress as measured by the TQ (Goebel and Hiller, 1994). In addition the right anterior insula, an area related to OS influence, shows increased delta and gamma activity related to increased tinnitus distress. On the other hand decreased theta and gamma activities are found in the left anterior insula, an area related to PS influence.

At a resting state the sensory cortices are characterized by alpha activity, which has been

Acknowledgments

This study is performed with a grant from the American Tinnitus Association. The Tinnitus Research Initiative and St. Jude Medical Neurodivision are acknowledged for their support. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

References (48)

  • J. Tonndorf

    The analogy between tinnitus and pain: a suggestion for a physiological basis of chronic tinnitus

    Hear. Res.

    (1987)
  • S. Vanneste et al.

    The neural correlates of tinnitus-related distress

    NeuroImage

    (2010)
  • J.W. Warrick

    Stellate ganglion block in the treatment of Meniere's disease and in the symptomatic relief of tinnitus

    Br. J. Anaesth.

    (1969)
  • W. Wittling et al.

    Hemisphere asymmetry in parasympathetic control of the heart

    Neuropsychologia

    (1998)
  • W. Wittling et al.

    Hemisphere asymmetry in sympathetic control of the human myocardium

    Brain Cogn.

    (1998)
  • F. Yasuma et al.

    Respiratory sinus arrhythmia: why does the heartbeat synchronize with respiratory rhythm?

    Chest

    (2004)
  • A. Axelsson et al.

    Tinnitus—a study of its prevalence and characteristics

    Br. J. Audiol.

    (1989)
  • P. Adlington et al.

    Stellate ganglion block in the management of tinnitus

    J. Laryngol. Otol.

    (1971)
  • R.T. Canolty et al.

    High gamma power is phase-locked to theta oscillations in human neocortex

    Science

    (2006)
  • M. Congedo

    Subspace projection filters for real-time brain electromagnetic imaging

    IEEE Trans. Biomed. Eng.

    (2006)
  • A.D. Craig

    Interoception: the sense of the physiological condition of the body

    Curr. Opin. Neurobiol.

    (2003)
  • F. Crick et al.

    A framework for consciousness

    Nat. Neurosci.

    (2003)
  • H.D. Critchley et al.

    Neural activity relating to generation and representation of galvanic skin conductance responses: a functional magnetic resonance imaging study

    J. Neurosci.

    (2000)
  • H.D. Critchley et al.

    Neural systems supporting interoceptive awareness

    Nat. Neurosci.

    (2004)
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      As with pain, tinnitus consists not only of a sensory component, often expressed as tinnitus loudness and frequency or pitch, but also an affective component, reflecting its unpleasantness (De Ridder et al., 2011a) and its related distress (De Ridder et al., 2011b). Tinnitus associated distress involves an autonomic component (van der Loo et al., 2011), and should be differentiated from mood changes, with different neural correlates (Joos et al., 2012). Similarly to pain, suffering is the result from a dysfunctional cognitive, emotional and autonomic response (Craig, 2003; Wade and Hart, 2002; Wade et al., 2011).

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