The morphology, biomechanics, and physiological function of the suboccipital myodural connections

Abstract

The myodural bridge (MDB) connects the suboccipital musculature to the spinal dura mater (SDM) as it passed through the posterior atlanto-occipital and the atlanto-axial interspaces. Although the actual function of the MDB is not understood at this time, it has recently been proposed that head movement may assist in powering the movement of cerebrospinal fluid (CSF) via muscular tension transmitted to the SDM via the MDB. But there is little information about it. The present study utilized dogs as the experimental model to explore the MDB's effects on the CSF pressure (CSFP) during stimulated contractions of the suboccipital muscles as well as during manipulated movements of the atlanto-occiptal and atlanto-axial joints. The morphology of MDB was investigated by gross anatomic dissection and by histological observation utilizing both light microscopy and scanning electron microscopy. Additionally biomechanical tensile strength tests were conducted. Functionally, the CSFP was analyzed during passive head movements and electrical stimulation of the suboccipital muscles, respectively. The MDB was observed passing through both the dorsal atlanto-occipital and the atlanto-axial interspaces of the canine and consisted of collagenous fibers. The tensile strength of the collagenous fibers passing through the dorsal atlanto-occipital and atlanto-axial interspaces were 0.16 ± 0.04 MPa and 0.82 ± 0.57 MPa, respectively. Passive head movement, including lateral flexion, rotation, as well as flexion-extension, all significantly increased CSFP. Furthermore, the CSFP was significantly raised from 12.41 ± 4.58 to 13.45 ± 5.16 mmHg when the obliques capitis inferior (OCI) muscles of the examined specimens were electrically stimulated. This stimulatory effect was completely eliminated by severing the myodural bridge attachments to the OCI muscle. Head movements appeared to be an important factor affecting CSF pressure, with the MDB of the suboccipital muscles playing a key role this process. The present study provides direct evidence to support the hypothesis that the MDB may be a previously unappreciated significant power source (pump) for CSF circulation.

Figure 1

Diagram of the method for showing the connected area between the MDB and the SDM. The contour of the area of the MDB attached to the SDM was showed by infiltrated black ink. Figure 1A: The complex of RCDmi-MDB-SDM located at the dorsal atlanto-occipital interspace; Fig. 1B: The complex of OCI-MDB-SDM located at the dorsal atlanto-axial interspace; Fig. 1a: Illustration for Fig A; Fig. 1b: Illustration for Fig. 1B. Thin black rrows: black ink infiltrated into the narrow gap between the SDM and muscles. Dot line: the connected area between the MDB and the SDM showed up by black ink infiltrating. Stars: DAOM and MDB. Arrowheads: Roots of the spinal nerve.

Figure 2

Illustration of preparation (A) and fixation (B) of the test specimen.

Figure 3

The MDB at the dorsal atlanto-occipital or atlanto-axial interspaces. The RCDmi overlay the dorsal atlanto-occipital interspace (Fig. 3a). When the RCDmi was reflected and stretched caudally the DAOM was severed along the posterior margin of occipital bone, and a fibrous connection was observed between the RCDmi and the DAOM (trigeminy stars), and also between the DAOM and the SDM (double arrowheads)(Fig. 3b). After the DM was cut along the margin of foramen magnum, and the RCDmi was reflected caudally, it was found that the DM was stretched dorsally via the MDB (enclosed by the dotted line) (Fig. 3c). On the other hand, the connective tissues (enclosed by the dotted line) among the RCDmi, the DAOM, and the DM were observed from the caudal side when the posterior arch of the atlas and the vertebral lamina were removed and the RCDmi was reflected to the cephalic side (Fig. 3d). At the lateral side of the dorsal atlanto-occipital interspace, the posterior arch of the atlas and the vertebral lamina of the axis were removed and the RCDmi was reflected laterally, and the connective tissues (enclosed by the dotted line) among the RCDmi, the DAOM, and the DM were again observed (Fig. 3e). Between the atlas and axis, the short head of the RCDma (RCDmaS)and the OCI passed over the dorsal atlanto-axial interspace (Fig. 3f). The fibrous connections between the OCI and the DAAM (white arrow), and between the short head of the RCDma and the DAAM (black arrow) were exposed in cranial aspect (Fig. 3g) and in the caudal aspect (double arrowheads) (Fig. 3h). After the lamina of the axis was removed and the OCI was reflected cranially, the dense connective tissue (enclosed by the dotted line) among the OCI, DAAM, and DM was observed (Fig. 3i). OCC: Occipital bone, RCDmi: Rectus capitis dorsal minor, DAOM: Dorsal atlanto-occipital membrane, DM: Dura mater, SC: Spinal cord, MDB: Myodural bridge, OC: Occipital condyle. OCI: Obliquus capitis inferior, RCPma S: Short head of the rectus capitis dorsal major, DAAM: Dorsal atlanto-axial membrane.

Figure 4

The MDB showed in sagittal section of the dorsal atlanto-occipital or atlanto-axial regions, with H&E stained (a, c, e) and Masson stained (figure b, d, f, g). Abundant dense connective tissues (white arrows in Fig. 4d) were found to be continued with the muscular bundles of the RCDmi and inserted into the DAOM. And then dense fibrous tracks (thick arrows in Fig. 4c,d) from the ventral side of the DAOM connected with the SDM. Meantime, abundant dense connective tissues (white stars in Fig. 4f) were found to be originated from the caudal end of the short head of RCDma and the ventral side of the OCI and inserted into the DAOM. And then the ventral fibers of the dense part of the DAAM are connected to the SDM (black arrow in Fig. 4f,g), where the SDM appeared multilayer structure and became thick caudally (arrowhead in Fig. 4f,g). OCC: the occiput, C1: the atlas, C2: the axis; DAOM: Dorsal atlanto-occipital membrane; DAAM: Dorsal atlanto-axial membrane; RCDmi: Rectus capitis dorsal minor; OCI: Obliquus capitis inferior; RCPma S: Short head of the rectus capitis dorsal major; MDB: the myodural bridge; DM: the spinal dura mater.

Figure 5

Connections between the DAOM and SDM or between the DAAM and SDM showed under the SEM. Figure (b) and (c): Magnification of the boxes in figure (a). Figure (e): Magnification of the box (e) in figure (d). Figure (f): Magnification of the box (e) in figure (e). Abundant cord-like tissues were a terminal part of the MDB, connecting the DAOM to the SDM (Fig. 5a). These connective cords were fused compactly with the DAOM (Fig. 5b) and the SDM (Fig. 5c) respectively. The DAAM gave off bundle of plexiform collagen fibers (Fig. 5d), which were woven into the collagen fibers array of SDM (Fig. 5e,f), thus anchoring the SDM to the DAAM. DAOM: Dorsal atlanto-occipital membrane; DAAM: Dorsal atlanto-axial membrane; MDB: Myodural bridge; SDM: Spinal dura mater.

Figure 6

Measurements of CSF pressure during electrical stimulation of the suboccipital muscles or during passive head movements. The CSF pressure was significantly increased when the OCI muscle was stimulated but no change occurred in the blood pressure and respiration rate (Fig. 6a). And a rise and waveform change of CSFP appeared during the lateral head flexion (Fig. 6b), head rotation (Fig. 6c), and head flexion and extension (Fig. 6d), without changes in the respiration and blood pressure. CSFP: Cerebrospinal fluid pressure, R: Respiration, BP: Blood pressure, Hollow Triangle: the beginning of passive motion of the head, Filled Triangle: the end of passive motion of the head.