Insular lateralization in tinnitus distress
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.
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