Over one third of individuals with a whiplash injury develop chronic neck pain and disability, leading to high clinical, social, and economic costs (Al-Khazali et al., 2020, Pink et al., 2016). The persistence of neck pain in whiplash-associated disorders (WAD) is understood to be caused by a combination of biopsychosocial factors (Holm et al., 2009). However, the biomechanical mechanisms underlying chronic neck pain in WAD are poorly understood. Imaging studies have identified increased muscle fat infiltration (MFI) in the neck muscles of individuals with WAD, with the greatest concentration of MFI found in the deep cervical extensor (DCE) muscles (multifidus and semispinalis cervicis) (Abbott et al., 2015, Elliott et al., 2006). While the role of MFI in the development and maintenance of pain and movement dysfunction is unknown, it is indicative of muscle atrophy and likely associated with a decrease in force generating capacity of the affected muscles. Reduced neck strength and altered muscle activation patterns have been reported in individuals with WAD. Previous studies have found that those with WAD exhibit a marked decrease in isometric neck strength in all cardinal planes (flexion–extension, lateral bending, and rotation) when compared to healthy controls, with the greatest relative weakness reported in extension (Krogh and Kasch, 2018, Pearson et al., 2009, Prushansky et al., 2005). Altered muscle activation patterns during dynamic tasks are characterized by decreased and delayed anticipatory recruitment of the deep cervical flexors (longus colli and capitis) (Falla et al., 2004b) and increased tonic recruitment of superficial muscles (sternocleidomastoid, upper trapezius, scalenes, and levator scapulae) (Falla et al., 2004a, Jull et al., 2004, Juul-Kristensen et al., 2013, Nederhand et al., 2000). Understanding the biomechanical role of the DCE muscles can help establish a link between muscle morphological changes and altered strength and activation patterns in WAD.

The human neck is structurally complex, with 7 intervertebral joints and more than 20 muscle pairs acting across multiple joints and axes (Kamibayashi and Richmond, 1998). Kinematic and muscle redundancy prevent the direct computation of individual muscle forces, as any forces and moments measured at the head could be produced by many unique combinations of active muscle forces. Electromyography (EMG) can improve estimates of muscle forces based on activation levels, but there are barriers to the effective use of EMG in the neck. EMG of the DCE muscles is invasive, requiring insertion of intramuscular electrodes through several layers of muscle and fascia before reaching these deep muscles. Previous studies using EMG for select muscles have found that the directional preference of many neck muscles does not precisely align with the biomechanical line of action, highlighting the complex interdependence of the neck muscles (Blouin et al., 2007, Keshner et al., 1989).

An advantage of computational models is that they enable access to all parameters, many of which cannot be manipulated or measured in vivo, such as muscle forces and intervertebral joint torques. Neck models in the literature vary considerably in their kinematic and muscle complexity, from planar single-joint inverted pendulums with 2 muscles to 48 degree of freedom (DOF) models with 129 muscle elements (de Bruijn et al., 2016). Given the lack of consensus regarding the degree of independent control humans have of neck muscle activations and joint torques, this study includes a comparison of seven musculoskeletal models with varying kinematic DOFs and muscle groupings.

Experimental studies of isometric neck strength and muscle spatial tuning typically measure torques about 3 axes crossing at the C7-T1 intervertebral joint (Fice et al., 2018, Vasavada et al., 2001). This mapping from the 6-D head space to 3-D torque space about a single joint does not capture the differential contribution of torques about the upper and lower cervical spine. The feasible force set (FFS) is a computational technique that defines the bounds of maximum isometric strength in all directions radiating from a point on the end-effector (Valero-Cuevas, 2016). The standard FFS has been used to probe the role of individual muscles in producing forces in the human finger (Valero-Cuevas, 2009), leg (Kutch and Valero-Cuevas, 2011, Sohn et al., 2019), and cat hindlimb (Sohn et al., 2013). This study extends the FFS to represent neck strength as the maximum forces that can be resisted at prescribed locations on the head, corresponding to maximum isometric wrenches (forces and torques) about the head axes.

The objective of this study was to determine the effect of DCE muscle weakness on multi-directional neck strength and muscle activation patterns. A secondary objective was to evaluate the effects of kinematic and muscle model complexity on neck strength and the role of the DCE muscles. These aims were achieved by computing the modified FFS of the neck with varying strengths of the DCE muscles. Maximum isometric neck strength and associated muscle activation patterns were simulated in 25 test directions, selected to reflect locations on the head where a clinician could realistically perform manual muscle testing.

The primary contribution of this work is a biomechanistic link between morphological changes in the DCE muscles and altered neck strength and muscle activation patterns. This knowledge can be used to develop assessments and targeted interventions to improve clinical outcomes for chronic neck pain in WAD. There are several additional contributions. First, the extension of the traditional FFS is presented to account for the wrench (3 forces and 3 torques) applied about the end-effector (skull) axes to represent multi-directional neck strength. Second, the finding that the outcomes are sensitive to musculoskeletal model kinematic and muscle redundancy demonstrates the importance of considering these factors in model design. Finally, directional muscle activation mappings are provided that can be used to guide assessment and strengthening of specific neck muscle groups.