The central mechanism of vestibular habituation

Yasushi Naito, Shigeru Hirano Department of Otolaryngology - Head and Neck Surgery Graduate School of Medicine, Kyoto University Sakyo-Ku, Kyoto 606-8501, Japan

1. The purpose 　The purpose of this study is to analyze the central mechanisms of vestibular habituation, which is important in space medicine, by using functional brain imaging. This study may contribute to the elucidation of macro cortical networks for cortical and sub-cortical processing of vestibular sensation and habituation. 2. Methods 　We applied hot or cold air irrigation to the external auditory canal of 12 normal subjects by an air-caloric stimulator, and monitored eye movement using infrared CCD video system. Habituation of vestibulo-ocular reflex induced by repeated caloric stimulation was monitored, and, at the same time, changes in regional cerebral blood flow (rCBF) were measured by positron emission tomography (PET). rCBF data were analyzed by SPM (Statistical Parametric Mapping) to identify the regions that are activated or deactivated significantly during vestibular stimulation and habituation. 3. Results and Comments 3.1 Regions that were activated or deactivated by caloric vestibular stimulation 　Brain regions that exhibited rCBF increase significantly correlated with the absolute value of slow-phase eye velocity (SPV) of caloric nystagmus were the left middle insular region, the right posterior insular region, the right inferior parietal lobule (Brodmannユs area (BA) 40), the right precuneus (BA7), the right visual area (BA19) and the right and the left cerebellar hemispheres. Among these regions, peri-insular regions were activated depending on the direction of the nystagmus (the right posterior insular region was activated when the nystagmus was beating toward right, and the left middle insular region was activated when the nystagmus was directed toward left), while the right inferior parietal lobule was activated irrespective of the direction of the nystagmus. The regions that exhibited significant negative correlation with the absolute value of SPV were the right and the left cingulate gyri (BA23, 24), bilateral pre-frontal cortices (BA10, 11), the right temporal cortex (BA21), the right cerebellar hemisphere and the right visual cortex (BA18). 3.2 Regions that were activated along with subjective sensation of rotation 　Brain regions that exhibited significant positive correlation with the intensity of subjective sensation of self-rotation were the bilateral posterior parieto-insular regions and the bilateral precuneus (BA7). The activation of peri-insular regions depended on the direction of the nystagmus, while the right precuneus was significantly activated irrespective of the nystagmus direction. 3.3 Changes in rCBF associated with habituation of vestibular responses due to repeated stimuli 　The average SPVs during caloric stimulation were; 7.4 degree/sec for the 1st irrigation, 6.3 degree/sec for the 2nd irrigation, 4.5 degree/sec for the 3rd irrigation and 4.3 degree/sec for the 4th irrigation. The SPV decreased along with the repetition of caloric stimulation, and the SPV during the 3rd and the 4th irrigation was significantly lower than that during the first irrigation. We compared rCBF between the 1st and the 4th measurement. The regions that exhibited significantly lower rCBF during the 4th caloric stimulation, which were thought to be deactivated along with vestibular habituation, were the bilateral parieto-insular regions, the right precuneus (BA7), the motor area (BA4), the supplementary motor area (BA6), the left cingulate gyrus (BA24), the right inferior temporal gyrus (BA20) and the left cerebellar hemisphere. On the other hand, the regions that exhibited higher rCBF at the 4th caloric stimulation, which are the areas that may contribute to vestibular habituation, were the left anterior cingulate gyrus (BA24, 32), the right anterior cingulate gyrus (BA32), the right cingulate gyrus (BA29) and the right parahippocampal gyrus and the bilateral visual cortices (BA17, 18). 3.4 New findings in the present study 　In the present study we found that the activation of the peri-insular vestibular cortex depends on the direction of the nystagmus. We also found that the rCBF becomes lower when the SPV of caloric nystagmus is high, which suggests inhibitory interaction between vestibular and visual systems. The regions of which activation correlated to subjective intensity of self-rotatory sensation were peri-insular cortices and the precuneus. The activation of the precuneus did not depend on the direction of the nystagmus while that of the peri-insular regions did, suggesting that the precuneus might be involved in the perception of self-rotation per-se. 　Since the anterior cingulate gyrus and the visual cortex were associated with decrease in caloric response, it was suggested that these areas might be related to vestibular habituation. The anterior cingulate gyrus is known to be involved in the processing of attention, and has fiber connection with the insular region, it may be possible to assume that this area has inhibitory function on vestibular responses. Attention on a certain object is often accompanied by turning oneユs gaze on it. Sensation of self-rotation induced by caloric vestibular stimulation may lead oneユs attention toward the direction of rotation, which may activate the anterior cingulate gyrus and visual cortices. 3.5 Contribution to space medicine 　The present results suggested that the insular regions, the anterior cingulate gyrus and visual cortices are related to processing of vestibular perception and its habituation. This indicates that monitoring the activities of these regions may give information on oneユs adaptive capacity for micro-gravity in space. Examination on these cortical functions before or after space flight may be used as an aptitude test for stay in space. The present methods may also contribute to quantitative evaluation of subjective sensation accompanied by space motion sickness. List of Publications Review Naito, Y.: Vertigo and the cerebral cortex. Practical Otolaryngology, Bunkodo (2001) in press Oral presentation Naito, Y., Tateya, I., Hirano, S., et al.: Cortical processing of vestibular sensation - a PET study. 104th annual meeting of Oto-Rhino-Laryngological Society of Japan, May 2001. Naito Y, Tateya I, Hirano S, Ito J: Cortical processing of vestibular sensation and its habituation. 38th Annual Workshop of Inner Ear Biology, Rome, September 2001.