Distribution and density of muscle spindles (MS), atypical proprioceptors (types I to III) and isolated nerve fibers (INF) in muscles supplied by the trigeminal nerve (green), facial nerve (blue), hypoglossal nerve (white) and glossopharyngeal nerve (brown).
The proprioception from the head is mainly mediated via the trigeminal nerve and originates from special sensitive receptors located within muscles called proprioceptors. Only muscles innervated by the trigeminal nerve, and rarely some muscles supplied by the facial nerve, contain typical proprioceptors, i.e. muscle spindles. In the other cephalic muscles (at the exception of the extrinsic muscles of the eye) the muscle spindles are replaced by sensory nerve formations (of different morphologies and in different densities) and isolated nerve fibers expressing mechanproteins (especially PIEZO2) related to proprioception. This chapter examines the cephalic proprioceptors corresponding to the territories of the trigeminal, facial, glossopharyngeal and hypoglossal nerves.
- muscle spindles
- atypical proprioceptors
- cephalic muscles
Proprioception is a quality of the somatosensory system that informs the central nervous system about the static and dynamics conditions of muscles and joints. This type of sensitivity has been studied in deep in the muscles depending on the spinal nerves and today the neurobiology of spinal proprioception is well known [1, 2, 3, 4]. On the contrary, the neuroanatomy as well as the cellular and molecular bases of the proprioception in the cephalic muscles is not well known. Nevertheless, it is clear that cephalic muscles permanently develop fine adjustments of stretching and tone in facial movements, regulation of chewing force, oromotor reflex behaviors, verbal and nonverbal facial communication, swallowing, coughing, vomiting or breathing [5, 6, 7].
The skeletal muscles contain an intrinsic mechanosensory system, the proprioceptive system, which provides unconscious and conscious information to the central nervous system. The proprioceptive inputs originate in specialized sensory organs (proprioceptors) present in muscles (muscle spindles [8, 9]), tendons (Golgi’s tendon organs ), joint capsules (Ruffini-like sensory corpuscles, Pacinian corpuscles and free nerve endings ), and presumably also the skin but their physiological properties suggest they are not the alternative to muscle spindles [2, 12, 13, 14]. The information encoded by the propioceptors gives rise to unconscious and conscious sensations, necessary for most basic motor functions . For those interested in a recent review and in detail on both types of proprioceptors, we refer to the Banks  and Macefield and Knellwolf .
Some decades ago, Baumel  suggested that proprioceptive impulses from facial muscles are conveyed to the central nervous system via different branches of trigeminal nerve throughout multiple communications with the branches of the facial nerve. Actually, it is accepted that the proprioception of all cephalic muscles depends on the trigeminal nerve [6, 18].
Therefore, the first unresolved issue in cephalic proprioception is whether all cranial nerves that innervate striated muscles also collect their proprioceptive innervation. According to Lazarov  the proprioceptive innervation of all cephalic muscles depends exclusively on the trigeminal nerve. In other words: the sensory ganglia of cranial nerves lack of primary sensory neurons and the proprioceptors of the cephalic muscles are supplied by neurons from the trigeminal mesencephalic nucleus .
The second aspect pending clarification is: if the proprioception of the cephalic muscles depends exclusively, or mainly, on the trigeminal nerve, how do the fibers of this nerve reach the muscles of the territories of other nerves? This question can be answered because to extensive communications of the trigeminal nerve with other cranial nerves. The trigeminal nerve has numerous connections to the facial nerve [20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34] and the data collected from animal models indicate that the nerve fiber interchange is always from the trigeminal to the facial nerve and not on the contrary . To serve facial proprioception additional connections between the facial and cervical spinal nerves exists [36, 37]. Apart from those communications no specific reference of communications between the trigeminal nerve with the glossopharyngeal, vagal and hypoglossal nerves were found. But presumably the trigeminal proprioceptive fibers pass from the trigeminal nerve to them directly on the target organs themselves (tongue, pharynx, palate) or through their connections with the facial nerve [28, 31, 32].
And the third main question of cephalic proprioception regards the identification and characterization of proprioceptors in the cephalic muscles. The skeletal muscles innervated by spinal nerves contain neuromuscular spindles and Golgi tendon organs, in addition to other types of corpuscles with less functional entity [8, 9, 10, 11]. However, only the cephalic muscles supplied by the mandibular branch of the trigeminal nerve, and
2. Distribution of typical proprioceptors in cephalic muscles
Typical proprioceptors of human cephalic muscles are represented by neuromuscular spindles as most of them lack Golgi tendon organs since they lack true tendons.
Muscle spindles have been found in muscles innervated by the trigeminal nerve while in the territory of the other cranial nerves, with very rare exceptions, are absent . Recently, Junquera  determined the relative density of muscle spindles in human jaw muscles (Figure 1; Table 1). The
|Muscle||MS||Type I||Type II||Type III||INS*|
|M. pterygoideus lateralis||18||3||14||7||Yes|
|M. pterygoideus medialis||21||5||10||3||Yes|
|Venter anterior m. digastricus||2||3||1||1||Yes|
|M. tensor veli palatini||0||2||2||1||Yes|
|M. corrugator supercilii +M. depresor supercilii||1||3||7||Yes|
|M. orbicularis oris|
|M. zygomaticus maior||0||1||4||4||Yes|
|M. zygomaticus minor||0||1||2||0||Yes|
|M. depressor labii inferioris + mentalis||0||0||8||2|
|M. levator labii superioris||0||1||1||3||Yes|
|M. constrictor pharyngis superior||0||0||6||14||Yes|
|M. constrictor pharyngis inferior||0||0||5||9||Yes|
In muscles where the density of muscle spindles is higher, they consist of thick capsule, a shallow intracapsular space filled with variable number of intrafusal muscle fibers (ranging from 4 to 12). In muscles where the density of neuromuscular spindles was low, in general, the size of the spindles was smaller, had fewer intrafusal fibers and the capsule was less developed .
In the territory of the facial nerve one muscle spindle was found in the muscle
3. Atypical putative proprioceptors cephalic muscles
3.1 Criteria to characterize atypical proprioceptors
The identification of putative sensory receptors in the cephalic muscles that may serve as proprioceptors was based on the following criteria: independence of the nerve trajectory, be placed in close relation to muscle fibers, show a morphologically differentiated aspect, and display immunoreactivity for any putative mechanoprotein .
In agreement with the above premises, capsulated and non-capsulated corpuscle-like structures of variable size and shape containing numerous axon profiles complexly arranged, have been identified. Given the morphologic heterogeneity of the corpuscle-like structures that fulfill the preestablished criteria we attempt to classify them into three types: type I, capsulated by a thin capsule, the glial cells variably arranged and showing different morphologies; type II, partially capsulated (the capsule being continuous with the perimysium), with variable morphology and in most of the cases the direction of the long axis was parallel to the one of muscular fibers; type III, non-capsulated and both the axon and Schwann-like cells are variably arranged (Figure 2).
On the other hand, it is now well established that at the basis of mechanosensitivity are mechanically-gated ion channels . At present acid-sensing ion channel 2 (ASIC2) and Piezo2 have been detected in muscle spindles and are strong candidates to initiate the mechanotransduction in proprioceptors [50, 51, 52, 53, 54, 55, 56]. Also, the putative mechanoprotein transient-receptor potential vanilloid 4 (TRPV4) was detected in proprioceptors of the facial and pharyngeal muscles [42, 43].
3.2 Distribution in the territory of the facial nerve
No typical muscle spindles have been found in the human facial muscles [42, 57, 58, 59, 60, 61] with the exception of on the facial part of the muscle
3.3 Distribution in the territory of the glossopharyngeal nerve
Most research have not found typical muscle spindles in the muscles innervated by the glossopharyngeal nerve although they are present in the human
Regarding the pharyngeal muscles, typical muscle spindles were never found with the exception of the
3.4 Distribution in the territory of the hypoglossal nerve
Therefore, as a whole, the cephalic muscles have proprioceptive inervation, although only the muscles innervated by the trigeminal nerve and the