Altered Resting‐State Intranetwork and Internetwork Functional Connectivity in Patients With Chronic Unilateral Vestibulopathy

Altered Intranetwork FC in Patients With CUVP

In the present study, intranetwork FC analysis revealed decreased FC in the right middle occipital gyrus within LVN in patients with CUVP. It is well known that vision, vestibular and somatosensory systems work together to perceive our body and its relationship with the environment, which are further integrated and coordinated by the central nervous system to accurately perceive spatial location, ensure clear and stable vision and postural balance during various movements.12, 18 The interaction between different senses makes it possible for sensory substitution in patients with unilateral peripheral vestibular dysfunction (UPVD).12 When one sense is absent, the body will compensate for the lack through substitution of other senses. Many studies have found that when disturbing vision and proprioception, patients with UPVD exhibit greater center-of-pressure sway than healthy subjects, indicating that patients with UPVD rely more on vision and somatosensory input to maintain their balance.19, 20 zu Eulenburg et al21 demonstrated increased gray matter volume in visual, motor cortical areas, gracile nucleus, and bilateral somatosensory cortex in patients with VN. A voxel-based morphometry study of nine patients with vestibular neuritis performed by Hong et al22 showed that gray matter volume was increased in the lingual gyrus of the occipital lobe in patients. The results of these studies indicated that the functional activities in the visual cortex, somatosensory cortex and subcortical structure were enhanced in patients with VN, which supported the mechanism of sensory substitution. The results of our study revealed decreased FC in the right middle occipital gyrus within LVN in patients with CUVP, suggesting that the dynamic compensation is not complete in these patients, and that a strong sensory substitution mechanism is not initiated, which may lead to chronic dizziness. However, in order to further verify these findings, further studies are needed to investigate the structural changes such as gray matter volume difference between the patients with CUVP and health controls and explore whether changes in FC is related with brain structure changes in patients with CUVP.

In this study, we also found that the FC in the SMA within SMN was enhanced in patients with CUVP. A study has shown that SMA contributes to regulation of posture and control of movement and is an important node in the information flow of postural regulation (cortex-parieto-occipital junction-SMA-premotor cortex [PMC]-anterior horn of spinal cord), which plays an important role in high-level motor control, such as gait adjustment.23 SMA receives information about the external environment and internal states of the body from the parieto-occipital junction and receives input from the basal ganglia and cerebellum through the thalamus. After the information is integrated and processed, SMA projects the efferent information to the motor areas, which are then involved in postural regulation and motor control.23, 24 The expected postural control can be achieved by activating SMA, which is responsible for motion programming of movements based on visual motion processing. Premotor area (PM)/SMA may forward programs of precise foot–foot movement to the primary motor cortex and then send movement commands via corticospinal tract. The programs of precise movement and postural control are generated in the PMC and SMA. The vestibule, vision, and proprioceptive sensations are integrated in the parieto-occipital cortex, the bodily information is then transmitted to the PM/SMA, that encodes movement patterns.23-26 Therefore, it can be speculated that due to reduced spontaneous activity in the visual cortex in patients with CUVP, information flow into areas such as SMA through the parieto-occipital cortex is reduced, functions attributed to the SMA including self-initiation and planning of movements, and feedback calibration are not accurate, so patients with CUVP have to strengthen postural control through behavioral substitution to maintain their balance. However, this may form high-risk postural control strategies, leading to instability.

Altered Internetwork FC in Patients With CUVP

In this study, the internetwork FC analysis revealed weakened FC between the LVN and AN, as well as between the SMN and AN in patients with CUVP. Studies have shown that AN, VN, and SMN are independent processing systems for auditory, visual, and sensorimotor functions, respectively, that further integrate visual, vestibular information and different spatial frames of reference, therefore, ensuring the accuracy of spatial orientation, forming clear spatial perception.18, 27, 28 In this study, we found that: 1) AN is mainly composed of the temporal lobe and parietal cortex around the lateral fissure, which is mainly involved in auditory information processing and plays a major role in spatial perception and orientation. Studies29, 30 have shown that auditory and vestibular information converge in the overlapping areas of the caudal part of the superior temporal sulcus and posterior insula, suggesting that AN highly overlaps with the vestibular cortex and is a multi-sensory integration cortex.31 Previous fMRI studies on patients with UPVD during the recovery period showed that the vestibular cortex with enhanced FC was mostly located within AN.8, 10, 11, 19-21 2) LVN is the visual association cortex and participates in the integration of visual information and other information.32 3) SMN, which was first identified by Biswal et al,33 mainly includes the primary motor cortex (Ml), SMA, and PMC and plays an important role in execution and coordination of movement. Previous studies have shown that SMA is an important node in the postural regulation network and is essential for accurate gait control.23-25, 33 The temporoparietal cortex includes the posterior parietal cortex and vestibular cortex, which can integrate real-time signals in the vision, proprioceptive and vestibular sensations, so that the body's environmental information can be always updated and then transmitted to SMA to encode information for body posture control.25 We speculated that the synergy between visual–auditory-vestibular-sensorimotor regions is decreased in patients with CUVP, which in turn affects the coordination and integrity of motion perception, spatial orientation and motor regulation, resulting in chronic dizziness/instability.

In this study, the internetwork FC analysis also revealed decreased FC between pDMN and RFPN in patients with CUVP. 1) DMN was discovered by Raichle et al34 and is the most important component of the resting-state brain network and the most widely studied brain network. DMN mainly contains medial prefrontal cortex, posterior cingulate cortex, precuneus, anterior cingulate cortex, bilateral inferior parietal lobule, and medial temporal lobe.35 Among these brain regions, the medial prefrontal cortex and anterior cingulate cortex belong to aDMN, and the remaining regions, such as posterior anterior cingulate cortex, precuneus, and bilateral angular gyrus belong to pDMN. 2) Frontoparietal network (FPN) is also known as frontoparietal control network or executive attention network and is mainly composed of the dorsolateral prefrontal cortex and posterior parietal cortex.36 RFPN is right sided, containing a dorsal pathway including angular gyrus, dorsolateral prefrontal cortex, frontal eye field and insula, that participates in cognitive control such as memory, attention, and visual processing37 and almost any cognitive control tasks, as well as somatosensory perception and pain processing. A study38 found that FPN is between the DAN and DMN, which is related to the integration of information from these two networks.

A previous study39 documented mutual antagonism between task negative network (DMN) and task positive network (FPN, DAN), with DMN being positively activated during the resting state and deactivated during the task states, while task positive networks display opposite patterns of activation. It is believed that spontaneously organized brain functional activities exist during states of rest or quiet wakefulness, and these spontaneous brain activities during the resting state may be closely related to human thought, emotion and self-cognitive processes. Klingner et al11 performed an fMRI study on patients with AUVP and found that the FC between DMN and multiple other networks, including the somatosensory cortex, auditory/vestibular/insular cortex, motor cortex, occipital cortex, LFPC and RFPC, was reduced. With the restoration of peripheral vestibular function, the FC returns to normal. The author believed that this is a compensatory strategy of body, which can meet the increased demand on task networks to deal with multisensory conflicts, even during a resting state. In this study, reduced FC between pDMN and RFPN was observed in patients with CUVP. This may be the result of the body's long-term adaptation, with task positive networks being further strengthened to obtain information about the surrounding environment and patients' own spatial position.

DHI was developed by Jacobson and Newman15 and is widely used to determine the self-perceived handicap on emotion (E), physical (P), and functional (F) aspects as a consequence of dizziness and unsteadiness. The physical subscale of the DHI assesses the physical factors associated with dizziness/unsteadiness, the functional subscale of the DHI assesses functional consequences of dizziness/unsteadiness, and the emotional subscale of the DHI assesses emotional consequences of dizziness/unsteadiness, such as feelings of depression and anxiety. In this study, the average DHI score for patients with CUVP indicated that they had a moderate level of disability. There were no significant differences between the total and subscale scores (F, E, and P) of the DHI. These results suggest that in addition to chronic vestibular symptoms of varying severity, such as head movement- and visually-induced dizziness, patients with CUVP may often present with varying degrees of anxiety and depression. There was no significant correlation between CP value and the duration of disease, as well as total and subscale scores (F, E, and P) of the DHI. This result is consistent with previous studies showing that there was no correlation between peripheral vestibular function impairment and chronic symptoms.2, 5 Residual peripheral vestibular function deficiency cannot be the sole factor for chronicity of clinical symptoms in patients with CUVP. This may be due to the fact that vestibular compensatory mechanisms have not properly restored higher order perceptual functions, leaving patients vulnerable to subjective sensations of dizziness and unsteadiness in motion environments.

In this study, correlation analysis revealed a negative correlation between the FC of the MVN, AN, and the DHI score, but no significant correlation between changes in FC of brain networks and CP values in patients with CUVP, indicating that chronic symptoms following CUVP may be related to incomplete vestibular central compensation, rather than to the degree of peripheral vestibular loss. A previous study5 also showed that the chronicity of clinical symptoms in patients with CUVP may be related to incomplete vestibular central compensation, psychosocial factors and persistent over-reliance on visual signals. In this study, due to the feelings of fear and dread caused by the severe symptoms such as dizziness and unsteadiness during the acute phase, all patients actively avoided visual stimuli and did not undergo active vestibular rehabilitation treatment. For such patients, vestibular suppressants may be used, which in turn lead to a decrease in sensitivity to visual stimuli, failure of initiation of strong visual substitution, and poor visual substitution. This may ultimately result in chronic dizziness and unsteadiness. These symptoms are aggravated during turning head quickly and movement. Therefore, we speculate that psychological factors and visual dependence may affect vestibular central compensation and the extent of recovery after vestibular rehabilitation in patients with CUVP, which might be related to the chronicity of dizziness symptoms. However, their relationship needs to be explored in future studies.

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