Resting-state functional MRI (fMRI) which is a noninvasive imaging technique measures low-frequency fluctuations in BOLD signals (Fox and Raichle, 2007). Cortical and subcortical areas of spatially distinct and functionally related groups will show related spontaneous fluctuations during the resting state, composed of intrinsic functional networks of the human brain (Seeley et al., 2009). Changes in internal functional networks will affect performance of tasks in real life (Fox et al., 2007; (Hesselmann et al., 2008). In addition, the resting-state method has been widely used to reveal the typical and atypical functional structures inherent in the brain (Fox and Raichle, 2007; Greicius, 2008). Changes in characteristics at rest can be used as indicators of the progression of various diseases, such as heroin addiction (Yuan et al., 2010; Yuan et al., 2010; Yuan et al., 2010), Alzheimer’s disease (Greicius et al., 2004) and schizophrenia (Lui et al., 2009).
Most resting-state fMRI studies use FC to study temporal relationships between internal fluctuations observed in spatially distinct brain regions. However, there are few local features of spontaneous brain activity observed in specific areas by the method of FC. As a complement to the method of FC, the ALFF (Zang et al., 2007) method which measures regional spontaneous neuronal activity during resting-state fMRI is also widely used. In this study, we evaluated regional changes in both regional spontaneous neuronal activity and corresponding brain circuits during rest.
In this study, we identified several brain regions showing differences among the three groups during the resting state. “Balance triple” refers to the visual, proprioceptive and vestibular systems that maintain the balance of the human body. The primary visual cortex, as well as the lingual gyrus and lateral geniculate body, belongs to the medial visual cortex, which is responsible for processing visual information (Beckmann et al., 2005; Mantini et al., 2007). This study showed that the ALFF values of lingual gyrus in patients with VM were significantly higher than that in patients with MWoA and HCs, which indicated that the spontaneous neuronal activity of lingual gyrus in patients with VM under resting state was enhanced and the excitability was increased. It may reflect the changes in the integration function of visual information in the brain of patients with VM, which is most likely an adaptive change in response to repeated vertigo. The caudate nucleus and the lenticular nucleus are important components of the basal ganglia involved in the regulation of pain. In the study, the function of basal ganglia in the most patients with VM and MWoA was abnormal. Most scholars believe that the basal ganglia need to be involved in pain regulation due to repeated headaches, and the basal ganglia may be damaged during the process, which leads to a decrease in the ability of pain regulation. And with the increase of frequency and duration of attacks, this decline is more obvious.
As one of the most commonly used analytical methods of FC, the ROI correlation analysis method has been widely used in the research of brain sensation, cognitive and emotion. In this study, the ALFF values of the three groups of subjects were calculated, and it was found that the brain area with the most significant difference was the right putamen. Therefore, it was designated as the ROI, and ALFF and FC were combined to describe the functional characteristics between brain regions. The ALFF combined with FC method has been widely used in a variety of brain diseases and provides important information for understanding these diseases, such as Alzheimer’s disease (Sorg et al., 2007), heroin addiction (Yuan et al., 2010; Yuan et al., 2010; Yuan et al., 2010; Jiang et al., 2011), schizophrenia (Hoptman et al., 2010; Zhou et al., 2007) and depression (Anand et al., 2005).
The vestibular center also includes the subtentorial brainstem and cerebellar associated nucleus mass. Some scholars (Marcelli et al., 2009) have conducted fMRI studies on the vestibule of patients with cold water stimulation. They found that the brain areas with neuronal activity changes mainly included the insular cortex, thalamus, brainstem and cerebellum. The sensorimotor components associated with balance include the brainstem pathway, which produces motor responses to the body (such as the vestibule-oculomotor reflex) and visceral (the vestibular sympathetic and parasympathetic nerves) (Balaban and Yates, 2004; Holstein et al., 2011). These vestibular sensorimotor responses are regulated by cerebellum (Balaban and Yates, 2004; Ito, 1984). Patients with VM did show impaired central integration of semicircular canal rotation signal and otolithic organ gravity signal center (Wang and Lewis, 2016). Some studies have found that some patients with VM had lesions at the caudal part of the cerebellum, so the correct processing of otolitic information couldn’t be carried out, and patients with VM would be highly sensitive to head movement (Espinosa-Sanchez and Lopez-Escamez, 2015). The most common abnormality of eye movement in patients with VM is central positional nystagmus(Radtke et al., 2012), which may suggest that the cerebellum inhibits the release of vestibular effect (Bronstein and Lempertt, 2007). Some studies suggested that central positional nystagmus was the result of lesions at nodules and lingual lobe of cerebellum which made vestibular maladjustment (Choi et al., 2014). Therefore, cerebellar dysfunction may be involved in the pathogenesis of VM. Previous study found that functional imaging at the onset of VM showed bilateral cerebellar activation (Shin et al., 2014). Cerebellar hyperactivity during the onset and interictal stages of patients with VM was considered to be an adaptive mechanism to inhibit hyperactivity of the vestibular system (Jeong et al., 2015). VM is closely linked to motion sickness (Akdal et al., 2015), and even during the interictal stages, patients with VM are less tolerant of riding a carousel, a car, or even watching a 3D movie. Changes in the functional activity of the cerebellum in patients with VM found in this study might partially explain this phenomenon, suggesting that VM was not a simple episode disease. In functional imaging studies, it was found that the brain regions involved in pain information processing mainly included the anterior cingulate cortex, prefrontal cortex, insula, cerebellum, brainstem and somatosensory cortex (Yu et al., 2011). The cerebellum, as part of the pain matrix, is involved in pain processing and regulation (Yu et al., 2011). In animals and humans, the deep cerebellar nucleus process harmful stimuli and participate in pain perception and suppression through the relationship with the brainstem nucleus and thalamus. When cerebellar activity is forcibly enhanced, the pain threshold will increase, suggesting that cerebellum’s anti-nociceptive effect is enhanced (Pereira et al., 2017). The cerebellum also exhibits emotional processing functions (Klingner et al., 2013), which indicates that changes in cerebellar function can easily lead to adverse emotions. Unfavorable emotions are important factors that can trigger VM and MWoA. When the emotional function of cerebellum is abnormal, it may induce VM attacks.
Dorsolateral superior frontal gyrus is an important part of limbic system and an important part of emotional pathway of pain perception. This study found that the FC between the cerebellum, dorsolateral superior frontal gyrus and ROI of patients with VM were enhanced, and the FC between the dorsolateral superior frontal gyrus and ROI was enhanced in patients with MWoA. It suggested that patients with VM and MWoA had suffered from painful stimulation for a long time, and their endogenous analgesic mechanisms were adjusted, which might be used to process and modify painful emotional responses, or to reduce pain perception and cognition, so as to reduce input of pain signals.
Median cingulate and paracingulate gyri are not only involved in the attention and emotional response to pain, but also in the subjective perception of pain and its cognition and memory (Bluhm et al., 2007). They are also important brain regions that form the default network (Uckner et al., 2008). In a comparative study (Liu et al., 2006) of HCs and patients with chronic pain, a high concentration of opioid receptor binding sites was observed in the cingulate gyrus, suggesting that median cingulate and paracingulate gyri played an important role in the formation and regulation of pain sensation. In this study, FC of the median cingulate and paracingulate gyri and ROI was weakened in patients with VM, which might be the result of adaptation of nervous system. The attenuation of the nervous system itself can not only reduce the pain response and emotional response, but also reduce the subjective perception of pain.
The pathogenesis of VM is not clear. Imbalance of excitement or inhibition of various sensory information, vestibular information and pain signals may lead to the occurrence of vestibular migrane (Espinosa-Sanchez and Lopez-Escamez, 2015). The study found that patients with VM had reduced activity in multiple vestibular functional areas, while other vestibular functional areas showed compensatory increased activity, and activity of pain-related brain areas changed similar to patients with migraine. In patients with VM, abnormal brain functional networks associated with the right putamen were observed. All of these findings are likely due to adaptive changes in the brain regions of patients with VM.