Discussion
Head movements are complicated movements involving activities of many muscles. Amongst these muscles, the rectus capitis posterior minor (RCPmi), rectus capitis posterior major (RCPma), and obliquus capitis inferior (OCI) are located deep and posterior to the axis (C1) and atlas (C2). It was well known that they were connected to the upper cervical spinal dura mater via the MDBs through the posterior atlanto-occipital and atlanto-axial interspaces1-6. Furthermore, studies have shown that the suboccipital musculatures including RCPmi, RCPma, OCI, and the nuchal ligament (NL) participated in forming the MDB complex22. The MDB fibers from different origins could associate with each other and synergistically exert a pulling effect on the dura mater22,23.
Sui et al.19 and Zheng et al.6 proposed that the MDB may act as a pump for CSF circulation dynamics, and Xu et al.20 research demonstrated that CSF diastolic flow was significantly affected by the one-minute-head-rotation period, indirectly supporting the MDB’s CSF circulation dynamics hypothesis.
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As a further investigation upon the function of head movements, the present study found that the CSF flow was significantly affected in the one-minute-head-nodding period and the MDFR and ADFR were significantly decreased. That means nodding-head has a strong tendency to slow down the cerebrospinal fluid pulsation velocity toward the cranial cavity, although there was no obvious impact on the volume parameters (VD, VS, NV) of CSF flow.
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Furthermore, the present research found that the effect of head-nodding on CSF circulation was based on the initial NV flow direction. In 70.4% of the subjects with an initial caudal NV flow direction, the NV values were strengthened in the caudal orientation following the one-minute-head-nodding period, while in 60.6% of the subjects with an initial cranial NV flow direction, the NV values were strengthened in the cranial orientation. This indicates that the effect of head-nodding on CSF circulation may have individual differences and depend on its initial direction. For most subjects, the effect of nodding on CSF circulation may increase net flow in the same direction.
Compared with the previous studies, Xu et al.20 found that the MDFR and ADFR were significantly increased following the one-minute-head-rotation period. That means head-rotating has a strong tendency to speed up the cerebrospinal fluid pulsation velocity toward the cranial cavity. That is contrary to the effects of head-nodding. According to the anatomy and physiology of head movements, nodding motion happens at the atlanto-occipital joint along the coronal axis, while head rotating happens at the atlantoaxial joint along the vertical axis. They are different head movements. During nodding head, the RCPma and RCPmi assist in this movement. Their MDB may pull the upper cervical spinal dural sac along the sagittal plane, and cause the posterior wall of the dural sac to move backwards. And then, that may result in the decline of the MDFR and ADFR with some kind of kinetic mechanism. However, during head shaking, the OCI works with other muscles, such as the sternocleidomastoid, to move the atlantoaxial joint. In this process, the OCI’s MDB may pull the posterior wall of upper cervical spinal dural sac laterally and cause the dural sac to twist following the head-rotating. And then, that may lead to the increase of the MDFR and ADFR with some kind of kinetic mechanism. For the conflict between CSF flow rate and volume, we purposed it may be related to changes of the cross-sectional area at the measurement location. However, we still need to explore this conflicting finding in future study.
Accordingly, the present study also found that the CSF pressure in the lumbar region was significantly increased during 5 times head-nodding movements. Based on the results of Cine-PC MRI measurements, the cranial flow rate of CSF was slowed down during head-nodding. it means that more and more cerebrospinal fluid might be transported into the spinal canal during head-nodding and as a result, the CSF pressure would be increased of in the spinal canal. The results of CSF pressure measurement proved the speculation. Consequently, the present study suggests that head-nodding may provide driving force for the diffusion of cerebrospinal fluid from the cerebellomedullary cistern into the spinal canal.
Due to the subjects keeping stationary during the MRI scan, the CSF flow parameters were obtained not in sync with head-nodding but 1.17-4.00 min after head-nodding period. The immediate effects of head-nodding movement might be more pronounced than the measured effect because of the time lap between the head nodding occurring and the CSF measuring. In this way, the results of this study might be follow-up effects of nodding motion and motion mechanisms such as inertia might provide explanation for this effect.
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In addition, at the level of the occipital cervical junction, the cerebellar tonsils are suspended in the cerebellomedullary cistern. During the head flexion and extension, the size of the space between the tonsils and the atlas (C1) will be changed. In this way, we suggest that the relative movement of the cerebellar tonsils might also be a factor affecting CSF circulation during head-nodding movement. That will be studied in the future.
Moreover, there are many factors that affect CSF circulation. The heart rate24,25 and respiration26-29 are well known to affect CSF circulation. In this study, it was found that the heart rate decreased significantly after head-nodding period, which might be related with volunteers’ adaptation of the MR working environment. According to the dynamic mechanism of CSF circulation30, the rhythmic beating of the arteries directly transmits the pulse pressure to the CSF in the brain and promotes the flow of CSF. This study showed that there was no significant correlation between heart rate changes and MDFR, but the heart rate was significantly correlated with ADFR. The lower heart rate could prolong the DDF, thus ADFR may be affected by the lower heart rate. In addition, some authors have shown that when the heart rate is less than 90 beats per minute, the change in heart stroke volume is very weak31. According to the way that heart rate influences the CSF, we may conclude that the heart rate changes in the study may not lead to CSF flow changes. In our current study, the respiratory rate remains statistically unchanged before and after one-minute-head-nodding movement. Therefore, it was reasonable to eliminate the interference of respiratory changes in the studies.
The results of this study also provide a basis for etiology and diagnosis of CSF circulation-related diseases. Several studies have found that changes of CSF circulation are tightly associated with some clinical disorders, such as type I Chiari malformation32-34 and syringomyelia35-37. Anatomy and pathologic changes of the head movements, the MDB, or the suboccipital muscles might be related with them. Additionally, Clinical studies have shown that the dysfunction of the suboccipital muscles under various kinds of pathologic status might be correlated with chronic cervical headache38-40. The findings of this study may be a clue to its potential pathogenesis.
In conclusion, head-nodding can significantly affect the CSF circulation and head movement is one of the important drivers of cerebrospinal fluid circulation.
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