The transverse, alar, and capsular ligaments are important in stabilizing the upper cervical spines. The transverse ligament originates from a small tubercle on the medial surface of the lateral mass of the atlas, and inserts into the contralateral tubercle. Thus, it restricts anterior displacement of the atlas and flexion of the head (Steilen et al., 2014). The right and left alar ligaments run from the respective sides of the foramen magnum of the skull to the dens of the axis. They may be oblique or vertical, and limit the axial rotation and contralateral lateral flexion of the head (Steilen et al., 2014). The capsular ligaments surround the facet joints. They provide neck stability, especially during axial rotation (Rasoulinejad et al., 2012; Steilen et al., 2014). They also protect the nervous system such as brain stem, and spinal cord during excessive movements (Cusick and Yoganandan, 2002; Steilen et al., 2014).

The suboccipital muscles locate in the deepest layer of the neck. These are four paired muscles (rectus capitis posterior major, rectus capitis posterior minor, obliquus capitis superior, and obliquus capitis inferior). Unilateral contraction of these muscles induces head rotation, and bilateral contraction causes head extension (Yamauchi et al., 2017). These muscles have a high muscle spindle density that not only allows flexible movement, but also act as specific sensory receptors (Kulkarni et al., 2001). Therefore, these muscles allow to control delicate movements in atlanto-occipital (C1–C0) and atlanto-axial (C1–C2) joint (Yamauchi et al., 2017). However, sustained and excessive stress in the cervical spine resulted from incorrect posture causes problems in these muscles. (Yamauchi et al., 2017). McPartland et al. (1997) reported that weakness of cervical muscle after whiplash is associated with chronic neck pain and poor balance.

The deep cervical flexor muscles comprise of the longus colli and longus capitis muscles (Harrison et al., 2003). There are many proprioceptors in these muscles. These proprioceptors respond to the initial movement of a head or upper arm and contract these muscles. Thus, dysfunction of proprioceptors in these muscles could guide inappropriate movement in neck (Falla et al., 2004). As well, of these muscles, weak longus colli muscles can lead to cervical spine instability. The cervical spine instability would stimulate more the sympathetic trunk that is structurally close. This can be caused vertigo symptoms (Ibrahim et al., 2010; Liu et al., 2017; Saylam et al., 2009).

The proprioceptive system is extremely well developed in the cervical zygapophyseal joints. These joints are highly innervated by mechanoreceptive and nociceptive free nerve endings (Li and Peng, 2015). Hulse (1983) found that 50% of all cervical proprioceptors were present in the joint capsules from C1–C3. In addition, the deep upper cervical muscles have abundant mechanoreceptors in the γ-muscle spindles, which are highly sensitive to head yaw rotation (Chan et al., 1987; Pettorossi and Schieppati, 2014; Sterling et al., 2003). These abundant receptors play an important role in controlling afferent cervical activity, and controlling the movement of the eyes and body posture (Li and Peng, 2015). De Vries et al. (2015) reported that cervical proprioception has a neurological basis in muscle spindles rather than in the Golgi tendon organ, cutaneous receptors, and joint receptors. Afferent information from the cervical muscle and head movement related the visual and vestibular system converges in the vestibular nuclei (Corneil et al., 2002; de Vries et al., 2015). Accurate head-on-trunk orientation can be achieved by proprioceptive information of the cervical spine without vestibular information (de Vries et al., 2015; Malmström et al., 2009). However, changes in these structures due to direct trauma, muscular fatigue, degenerative changes, or direct pain can progress to subsequent damage of the ligament or muscle fibers, leading to instability at the cervical zygapophyseal joints (Chen et al., 2009; L’Heureux-Lebeau et al., 2014; Steilen et al., 2014). The function of receptors in the cervical spine can be altered. Damaged receptors in the upper cervical region relay abnormal signals to the vestibular nucleus, and a sensory mismatch between the vestibular and cervical inputs could result in cervicogenic vertigo (Bracher et al., 2000; Li and Peng, 2015; Michels et al., 2007).

The atlas articulates with the occipital condyles. Normal flexion to hyperextension at C1–C0 joint is between 15°–20° (Swartz et al., 2005). A C1–C2 joint has anatomically biconvex nature. Thus, flexion or extension movement in cervical spine often leads to motion in the opposite direction that is experienced in the atlas (Swartz et al., 2005). Rotation at C1–C0 joint is not possible due to the depth of the atlas sockets (Bogduk and Mercer, 2000). However, C1–C2 joint is possible. About 50% of all cervical spine rotation occurs at the C1–C2 (Steilen et al., 2014). As three primary ligaments (apical, alar, and transverse ligament) hold the dens of the C2, the normal range of rotation of C1 on C2 is 50° on each side (Bogduk and Mercer, 2000; Swartz et al., 2005).

The dizziness handicap inventory (DHI) is a questionnaire to evaluate dizziness (Jacobson and Newman, 1990). The DHI has been used to quantify the morbidity associated with dizziness in patients with vestibular system or other origin injuries (Ardiç et al., 2006; Tamber et al., 2009; Treleaven et al., 2005). The DHI is a self-reported questionnaire that includes 25 questions (seven physical, nine functional, and nine emotional questions). The physical subscale is well relevant to patients with CGD in Q1, Q11, and Q25 questions. The emotional subscale (Q9) showed a very low score in CGD patients than in those with general dizziness (Reid et al., 2017). The total score adds up the scale of answers, and the higher the score indicates severe dizziness and dysfunction (Treleaven, 2006; Whitney et al., 2004). It is reported that patients’ symptoms are relieved when the total DHI score is reduced by at least 18 points (Jacobson and Newman, 1990). Test-retest reliability (r=0.92 to 0.97) and internal consistency (α=0.72 to 0.89) have been shown to be high (Treleaven, 2006).

This test is widely used to confirm selectively contracting the deep neck flexors (longus capitis and longus colli) during active craniocervical flexion in supine position (Araujo et al., 2018; Juul et al., 2013). A clinician places a pressure biofeedback unit under the patient’s head and trains the patient to perform appropriate craniocervical flexion movements. The clinician should observe that the patient contracts only the deep neck flexor muscles without contracting the superficial neck flexors (e.g., sternocleidomastoid and anterior scalene) during the movements. Patients start at 22 mmHg and increase the steps by 2 mmHg to 30 mmHg (Araujo et al., 2018; Juul et al., 2013). This test can also be used to strengthen the deep neck flexors (Jull and Falla, 2016; Jull et al., 2008; Juul et al., 2013).

The alar ligaments originated from the ipsilateral of foramen magnum to the posterior dens of the axis. They are to limit axial rotation. They have the strongest tension during rotation and flexion (Steilen et al., 2014). To test the alar ligament, the patient is made to flex the head slightly in a seated or supine position. The clinician stabilizes the patient’s spinous process of C2 using a pincer grasp, and passively performs lateral flexion, rotation, or lateral shear, separately (Harry et al., 2019). A positive sign is a lack of movement of the C2 spinous process during movement (Harry et al., 2019; Reiley et al., 2017). The rotation stress has a sensitivity of 80% and specificity of 69.2%. Both the side-bending stress and lateral shear have a sensitivity of 80% and specificity of 76.9% (Harry et al., 2019).

The Sharp-Purser test is to assess the integrity of the transverse ligament. This helps to maintain the position of the odontoid process on atlas (Reiley et al., 2017). Many clinicians use the test to identify C1–C2 instability prior to the manipulation, joint mobilization, or dry needling of the upper cervical spine (Mansfield et al., 2020). The patient is seated with slightly flexed head position. The clinician fixes the spinous process of axis using a pincer grasp, and the opposite hand applies an anterior to posterior translation force on the patient’s forehead. If symptoms recur during forward flexion or disappear during posterior translation, C1–C2 instability should be suspected. In addition, it is a positive sign if it is displaced by more than 4 mm during posterior translation (Reiley et al., 2017).

The cervical joint position error test is used to assess the function of cervical proprioception in patients with neck pain, dizziness, and balance problems (Lee et al., 2008; Treleaven et al., 2006). It reflects afferent input from the receptors of joint and muscle in neck (Treleaven et al., 2003). The patient wears a laser cap and eye patch, sits 90 cm away from the wall, and actively moves the head and neck in the specified direction (flexion, extension, or rotation). Movement is measured in 10 trials in each direction, and then the patient returns to the natural head posture. The difference between the start (zero) and return positions is calculated in degrees for each trial. If the difference is more than 4.5°, it indicates dysfunction of neck proprioception (Pinsault et al., 2008; Quartey et al., 2019; Treleaven et al., 2003).

The vertebrobasilar insufficiency (VBI) test is to check blood flow in the vertebral artery (Kerry and Taylor, 2006). The clinician performs a combined extension and rotation of the cervical spine or rotation alone (Vidal, 2004; Zaina et al., 2003). Patients with VBI complain of dizziness, drop attacks, diplopia, dysarthria, dysphagia, ataxia, nausea, numbness, and nystagmus during the test (Thiel and Rix, 2005). As VBI can generate cerebral ischemia, leading to severe morbidity, patient with positive sign has to transfer to neurology (Asavasopon et al., 2005). Among the causes of VBI, poor head and neck posture and malalignment of the upper cervical spine can cause mechanical compromise, resulting in decreased velocity of vertebrobasilar blood flow and dizziness (Biesinger, 1988; Fitz-Ritson, 1991).

Impact of neck pain on motor output of cervical muscles: Impaired motor output of cervical muscles represents decreased strength, endurance, and force steadiness, as well as alteration in cervical muscle behavior, such as decreased activity of deep postural muscles, reduction of directional specificity, delayed onset of muscle responses, muscle fatigue, and increased neck muscle cocontraction (Blomgren et al., 2018; Falla et al., 2004; Schomacher et al., 2012). Thoomes-de Graaf and Schmitt (2012) showed that training of deep cervical flexors could increase the range of motion of the cervical spine, and reduce dizziness, pain, and limitations in activities in a patient with chronic nonspecific neck pain after prolonged bed rest.

Some patients with neck pain complain of impaired proprioception and postural control (O’Leary et al., 2009). To solve these problems, many therapists apply various exercises such as headneck recognition exercises, oculomotor exercises, or balance training (Gallego Izquierdo et al., 2016; Kristjansson and Treleaven, 2009). These approaches enhance sensorimotor control, and reduce neck pain and disability (Jull et al., 2007). Gallego Izquierdo et al. (2016) showed that cervical proprioception training has an effect on not only improvement of pain and disability, but also the coordination between the deep and superficial cervical flexors in patients with chronic neck pain.

As 50% of all cervical proprioceptors is in the joint capsules of C1–C3, abnormal mechanical stress of the cervical zygapophyseal joints is related with poor balance and dizziness (Hulse, 1983; Wrisley et al., 2000). Colledge et al. (1996) reported that cervical spondylosis was the cause of dizziness in 65% of the elderly. Thus, upper cervical degeneration or neck injury is one of causes of CGD. The CGD occurs a mismatch of sensory information (Reid et al., 2014a; Treleaven, 2006; Wrisley et al., 2000; Young and Chen, 2003). To solve the CGD, many therapists apply manual therapy to increase stimulation of proprioceptors to the upper cervical spine (Reid et al., 2008).

Mulligan introduced an intervention for CGD called sustained natural apophyseal glides (SNAGs) (Reid et al., 2014a). The SNAGs are safe and effective. It had an immediate and sustained effect in reducing dizziness, neck pain, and disability (Reid et al., 2008, Reid et al., 2012). Hall et al. (2007) provided evidence for the efficacy of SNAGs technique for C1–C2 in patients with cervicogenic headaches. Maitland mobilization is also a manual therapy technique for the management of cervical pain and CGD (Reid et al., 2012; Reid et al., 2014b). Both SNAGs and Maitland mobilization provide reductions in intensity and frequency of chronic CGD (Reid et al., 2014b).