Not Just an Anchor: The Human Filum Terminale Contains Stretch Sensitive and Nociceptive Nerve Endings and Responds to Electrical Stimulation With Paraspinal Muscle Activation

BACKGROUND: Neural components of the fibrous filum terminale (FT) are well known but are considered as embryonic remnants without functionality. OBJECTIVE: To investigate the ultrastructure of human FT specimens for sensory nerve endings and record paraspinal muscle activity on electrostimulation of the FT. METHODS: We prospectively investigated a cohort of 53 patients who underwent excision of the FT for the treatment of tethered cord syndrome. Surgical FT specimens were investigated by light and transmission electron microscopy. Intraoperative electrophysiological routine monitoring was extended by recording paraspinal muscles above and below the laminotomy level. RESULTS: Light microscopy revealed tiny peripheral nerves piercing the pia mater of the FT and entering its fibrous core. Transmission electron microscopy unveiled within the fibrous core of the FT myelinated nerve structures in 8 of the 53 patients and unmyelinated ones in 10 of the 53 patients. Both nerve endings encapsulated in fibrous tissue or unencapsulated nonmyelinated Schwann cell nerve bundles, that is, Remak cells, were found. Those nerve endings resembled mechanoreceptor and nociceptive receptor structures found in human skin, muscle tendons, and skeletal ligaments. Specifically, we found Ruffini mechanoreceptors and in addition nerve endings which resembled nociceptive glioneural structures of the skin. Bipolar electrostimulation of the FT was associated with paraspinal muscle activity above and below the spinal segment at which the FT was stimulated. CONCLUSION: Morphological and electrophysiological results indicate the presence of functional sensory nerve endings in the FT. Like other spine ligaments, the FT may serve as a proprioceptive element but may also contribute to back pain in spine disorders.

[1]  Owen P. Leary,et al.  Diseased filum terminale as a cause of tethered cord syndrome in Ehlers Danlos syndrome: histopathology, biomechanics, clinical presentation, and outcome of filum excision. , 2022, World neurosurgery.

[2]  P. Klinge,et al.  Evaluation of the Filum Terminale in Hereditary Equine Regional Dermal Asthenia , 2021, Veterinary pathology.

[3]  Camille K. Milton,et al.  Surgical Treatment of Tethered Cord Syndrome in Adults: A Systematic Review and Metanalysis. , 2020, World neurosurgery.

[4]  Jens Hjerling-Leffler,et al.  Specialized cutaneous Schwann cells initiate pain sensation , 2019, Science.

[5]  R. W. Banks,et al.  New functions for the proprioceptive system in skeletal biology , 2018, Philosophical Transactions of the Royal Society B: Biological Sciences.

[6]  K. Monk,et al.  Unwrapping the unappreciated: recent progress in Remak Schwann cell biology , 2017, Current Opinion in Neurobiology.

[7]  I. Biton,et al.  The Proprioceptive System Masterminds Spinal Alignment: Insight into the Mechanism of Scoliosis. , 2017, Developmental cell.

[8]  R. Tubbs,et al.  The filum terminale internum and externum: A comprehensive review , 2017, Journal of Clinical Neuroscience.

[9]  R. Sciot,et al.  The Filum Terminale: A Cadaver Study of Anatomy, Histology, and Elastic Properties. , 2016, World neurosurgery.

[10]  M. Baykaner,et al.  Pathological evaluation of the filum terminale tissue after surgical excision , 2015, Child's Nervous System.

[11]  M. Meglio,et al.  Neurophysiology of Complex Spinal Cord Untethering , 2014, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[12]  M. Fleming,et al.  The anatomy, function, and development of mammalian Aβ low-threshold mechanoreceptors , 2013, Frontiers in Biology.

[13]  A. Husain,et al.  Neurophysiologic intraoperative monitoring during surgery for tethered cord syndrome. , 2009, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[14]  M Solomonow,et al.  Sensory-motor control of ligaments and associated neuromuscular disorders. , 2006, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[15]  E. Liberti,et al.  Ultrastructural Study of the Filum Terminale and Its Elastic Fibers , 2006, Neurosurgery.

[16]  M. Miyamoto,et al.  Effects of anterior lumbar spinal fusion on the distribution of nerve endings and mechanoreceptors in the rabbit facet joint: quantitative histological analysis , 2003, Journal of orthopaedic science : official journal of the Japanese Orthopaedic Association.

[17]  M. Solomonow,et al.  Sensorimotor control of the spine. , 2002, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[18]  Yu-Ming Kang,et al.  Electrophysiologic Evidence for an Intersegmental Reflex Pathway Between Lumbar Paraspinal Tissues , 2002, Spine.

[19]  M Solomonow,et al.  The Ligamento‐Muscular Stabilizing System of the Spine , 1998, Spine.

[20]  M. Solomonow,et al.  Ligamento-muscular protective reflex in the lumbar spine of the feline. , 1998, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[21]  A. Kaigle,et al.  Interaction Between the Porcine Lumbar Intervertebral Disc, Zygapophysial Joints, and Paraspinal Muscles , 1997, Spine.

[22]  I. Lambrichts,et al.  Encapsulated Ruffini‐like endings in human lumbar facet joints , 1997, Journal of anatomy.

[23]  Z. Halata,et al.  The structure of sensory nerve endings in the knee joint capsule of the dog. , 1996, Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft.

[24]  Michiyasu Suzuki,et al.  The ventriculus terminalis and filum terminale of the human spinal cord. , 1992, Human pathology.

[25]  H. Johansson,et al.  Role of knee ligaments in proprioception and regulation of muscle stiffness. , 1991, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[26]  N. Bogduk,et al.  The human lumbar dorsal rami. , 1982, Journal of anatomy.

[27]  Z. Halata,et al.  The ultrastructure of the sensory nerve endings in the articular capsule of the knee joint of the domestic cat (Ruffini corpuscles and Pacinian corpuscles). , 1977, Journal of anatomy.

[28]  C. Miller,et al.  The ultrastructure of the conus medullaris and filum terminale , 1968, The Journal of comparative neurology.

[29]  John Watson Harmeier THE NORMAL HISTOLOGY OF THE INTRADURAL FILUM TERMINALE , 1933 .

[30]  V. Rajshekhar,et al.  Gross and microscopic study of the filum terminale: does the filum contain functional neural elements? , 2012, Journal of neurosurgery. Pediatrics.

[31]  Z. Halata,et al.  The ultrastructure of sensory nerve endings in the human knee joint capsule , 2004, Anatomy and Embryology.

[32]  剛 小野寺 Effects of anterior lumbar spinal fusion on the distribution of nerve endings and mechanoreceptors in the rabbit facet joint : quantitative histological analysis , 2003 .

[33]  T. Maeda,et al.  The Ruffini Ending as the Primary Mechanoreceptor in the Periodontal Ligament: Its Morphology, Cytochemical Features, Regeneration, and Development: , 1999 .

[34]  H. J. Gamble Electron microscope observations upon the conus medullaris and filum terminale of human fetuses. , 1971, Journal of anatomy.