Intervertebral disc innervation (axial plane). 1. Anterior longitudinal ligament. 2. Intervertebral disc. 3. Posterior longitudinal ligament. 4. Dura mater. NSV sinu-vertebral nerve, VR ventral root, DR dorsal root, RC rami communicantes, LVG latero-vertebral ganglia
Constitution of sinu-vertebral nerve—posterior view (from Groen et al. [1]). SVN sinu-vertebral nerve, PLL posterior longitudinal ligament
Lumbar rami communicantes (left side view). LVG latero-vertebral ganglia, DTRC deep transverse rami communicantes, SORC superficial oblique rami communicantes
Which Receptors?
The InterVertebral Disc (IVD) is usually described, in the wrong way, as a non-innervated and a non-vascular tissue. This concept is not exactly correct, but we have to consider the scarcity of nervous fibers, as we have to for the vessels, within the IVD. This scarcity is linked to the huge intra-discal pressure which does not allow the existence of small fibers, especially within the normal nucleus pulposus (NP) [2].
However, some free nerve endings within a few peripheral millimeters of outer annulus fibrosus (AF) , and especially within lateral parts of IVD [3], have been described. Ventral and dorsal portions of the IVD are associated with a powerful ligamentous system, crucial structures in this intrinsic innervation of the anterior column of the spine. Indeed, the anterior longitudinal ligament (ALL or VLL) and especially the posterior longitudinal ligament (PLL or DLL) contain many free nerve endings.
There are only few encapsulated endings evocating mechanosensitive afferent units. These rare mechanoreceptors which inform about pressure and tension are located between the layers of AF [4, 5]. This main articular system of the spine transmits little proprioceptive information but is dedicated to a real nociceptive function [6].
Finally, some receptors have been described within the vertebral end plates, mainly free nerve endings. These fibers reach the vessels of the vertebral body (basivertebral vein and artery) which carry these nerve fibers toward the center of the vertebral body and then to the PLL [7].
Which Pathways to the Spinal Root?
Sensory pathways coming from AF, ALL, and PLL converge toward lumbar ganglia of the sympathetic chain. Autonomic sensitive fibers coming from those peridiscal ligaments may transfer nociceptive messages. Presence of neurotransmitters like CGRP, VIP, and NPY, within these nervous structures, demonstrates their role in low back pain [5, 8]. The sympathetic nature of these nerves implies some specific features including numerous nervous and inter-nervous structures, therefore numerous ways to restore function in case of injury [9]. In addition, connections between the sympathetic nervous system and somatic nervous system imply that nociceptive messages may lead to somatic paravertebral muscular contractures [10].
Fibers coming from ALL and from the ventral part of the IVD form a ventral plexus which connects the two, right and left, latero-vertebral sympathetic chains. Each chain is constituted by four or five ganglia.
The largest contingent of sensitive fibers comes from PLL and dorsal part of AF. These fibers lead to the formation of the sinu-vertebral nerve. In addition to discal and ligamentous origins, fibers coming from the ventral part of the dura mater are associated with the constitution of the sinu-vertebral nerve . The real anatomical territory of this nerve is perfectly described by the clinical work of Kuslich [11], based on nearly 200 lumbar microdiscectomy procedures under local anesthesia. The sharing of neural pathways between IVD and dura mater, also demonstrated in dogs [8], can be explained by a common mesenchymal origin with the PLL. Otherwise, the sinu-vertebral nerve also engages with the few fibers coming from the basivertebral vessels [1].
The sinu-vertebral nerve, millimetric structure, has been first described by Luschka in 1850 [12].
The territory of each sinu-vertebral nerve partly overlaps that of the others. Indeed, connections between sinu-vertebral nerves exist on the midline and on at least one vertebral level above and below [1, 4].
Each sinu-vertebral nerve is formed at the ventral and cranial part of the intervertebral foramen, constituted by an ascending branch and a descending branch. This sinu-vertebral nerve is located just ahead of the spinal root. It continues to the extraforaminal part of the spinal root while recovering fibers from the lateral portion of the AF. Some fibers of the sinu-vertebral nerve are connected to this part of the root. It is therefore considered, from a morphological point of view, as a recurrent branch of the spinal root. From a functional point of view, most of its fibers extend through the rami communicantes, connecting the spinal root to the latero-vertebral chain.
Few of the sinu-vertebral nerve fibers go directly into the spinal root and thus into the somatic nervous system [13]. These certainly have a role in acute pain which is often better localized and lateralized.
The specific element of this pathway of disco-corporeal innervation consists of the passage of this nociceptive corporeal and discal information in the latero-vertebral ganglia. This is done by the multiple connections (rami communicantes) between the gangliae of the latero-vertebral chain and the spinal roots [14]. These rami communicantes bring all of the sympathetic sensory information to the intra-axial centers, from spinal metameres C8 to L2.
Considering intrinsic innervation of the lumbar spine, it is important to be aware that there are two types of rami communicantes : direct ones and oblique ones [15]. Direct rami communicantes are similar to those found on all vertebral levels, located on a transverse plane next to the middle of the vertebral body. Higuchi [15] more specifically names them as transverse deep rami as they pass, with the segmental vessels, under the arches of the psoas muscle. But the most interesting rami communicantes are probably those called oblique superficial rami also passing under the psoas but externally to the previous ones. They are called oblique as they ascend toward L1 and L2 spinal roots. Therefore, the L2 root receives 4–5 rami communicantes while the underlying roots receive only one or two each [15].
L2 roots, which are not so important from a motor point of view, thus take the lead role in lumbar innervation, well beyond the innervation of the IVD since this root is also predominant on the cutaneous territory of the lumbar region. Indeed, L2 roots cover the sensory territory of the underlying roots whose dorsal branches have, in part, “aborted.” The skin of the lumbar region is almost exclusively innervated by these roots. This phenomenon is called the “innervation hole” by Lazorthes and Zadeh [16].
As a brief summary, innervation of IVD and PLL depends on the sinu-vertebral nerve, characterized by minimal lateralization and metamerization. The fibers originating from the various sinu-vertebral nerves, via the complexity of the sympathetic nervous system, preferentially join some specific roots.
We have seen the case of lumbar innervation where fibers originating from IVD essentially go to the most cranial lumbar roots.
At the thoracic level, the vegetative organization is much more closely modeled on the metamerization.
At the cervical level, rami communicantes preferentially move toward the cervico-thoracic or cervical superior ganglia and therefore either to metameres C8 to Th1 or to metameres C2–C4. The concept of the “innervation hole ” may also be used at the cervical level [16]. Concerning the first cervical metamere, it is important to remember that the cervical gray matter is closely related to the nociceptive part of the trigeminal nucleus. This interpenetration of gray matter is usually called “trigemino-occipital complex” [17].
Evolution
It is now essential to consider modifications that may exist over time, not with regard to the transmission pathways, but the receptors within the ligamentous structures. The description of the receptors within IVD is that of a healthy and mature disc, which is only a transient state. After the age of 20, the IVD evolves, most often toward a physiological senescence, sometimes toward a pathological degeneration.
During these processes, a neoinnervation develops [18], at the same time as a neovascularization [19]. This nerve sprouting, related to inflammatory phenomena, is also described in the vertebral end plates [20].
Clinical Anatomy
Discogenic low back pain has some particular semiological characteristics, even troubling for problems limited to a single disc. Patients usually describe all the peculiarities of pain mediated by the sympathetic nervous system, including deep and diffuse pain, sensitivity of the skin (healthy skin but reflective of the organ it covers) and reflex muscular reactions. Classical inguinal irradiation of low back pain, including L4–L5 and L5–S1 discopathies, may be explained by the convergence of nociceptive information transmitted by the sympathetic system preferentially to the L1 and L2 roots. We can recall that the cutaneous territory of these roots corresponds to this zone immediately under the inguinal fold [21].
This concept of nociceptive convergence toward L1 and mostly L2 roots has resulted in some clinical trials such as L2 root infiltration which has a well-proven temporary antalgic effect, rather specific of discogenic low back pain [22, 23]. In the same way, L2 rami communicantes infiltration also provides pain relief [10, 24]. However, we remain disappointed by the relative ineffectiveness of the surgical division of these rami communicantes [25]. The idea of suppressing this pathway was promising; its failure probably reflects the existence of the many compensatory mechanisms of the autonomic nervous system [9].
This type of referred pain is also described with neck pain that radiate either in the interscapular space, the skin territory of upper thoracic roots, or to the head, called “cervicogenic headaches” [17] linked to the trigemino-occipital system.
