Original Research
Association of Subclinical Neck Pain With Altered Multisensory Integration at Baseline and 4-Week Follow-up Relative to Asymptomatic Controls

https://doi.org/10.1016/j.jmpt.2017.09.003Get rights and content

Abstract

Objective

The purpose of this study was to test whether people with subclinical neck pain (SCNP) had altered visual, auditory, and multisensory response times, and whether these findings were consistent over time.

Methods

Twenty-five volunteers (12 SCNP and 13 asymptomatic controls) were recruited from a Canadian university student population. A 2-alternative forced-choice discrimination task with multisensory redundancy was used to measure response times to the presentation of visual (color filled circles), auditory (verbalization of the color words, eg, red or blue), and multisensory (simultaneous audiovisual) stimuli at baseline and 4 weeks later.

Results

The SCNP group was slower at both visual and multisensory tasks (P = .046, P = .020, respectively), with no change over 4 weeks. Auditory response times improved slightly but significantly after 4 weeks (P = .050) with no group difference.

Conclusions

This is the first study to report that people with SCNP have slower visual and multisensory response times than asymptomatic individuals. These differences persist over 4 weeks, suggesting that the multisensory technique is reliable and that these differences in the SCNP group do not improve on their own in the absence of treatment.

Introduction

Approximately 30% to 50% of people experience neck pain every year, which places a significant burden on the health care system.1 A specific category of neck pain is subclinical neck pain (SCNP), which refers to lower-grade neck dysfunction in which individuals have recurrent flare-ups of neck pain but have not yet sought regular treatment.2, 3, 4

Altered afferent input through repetition and overuse changes the way that sensory information is processed by causing plastic changes in the central nervous system.5, 6, 7 Several studies have provided evidence for altered proprioceptive and neuromuscular function in individuals with SCNP.8, 9, 10, 11 Further research has suggested that the altered afferent input arising from SCNP leads to altered sensorimotor integration (SMI), altered motor output, and impaired motor control.5, 12, 13, 14 It has been hypothesized that other sensory modalities such as visual and auditory inputs may also be processed differently in SCNP causing altered multisensory integration.12

When visual input is less clear (ie, “noisier”), less emphasis is placed on visual information and accuracy is decreased.15 Adding haptic stimuli leads to improved accuracy and discrimination when visual input is less reliable.15 However, when a sense is less reliable or provides contradictory information, combination of stimuli may not always enhance accuracy. Hogendoorn et al16 reported that when there was contradictory input between proprioception of hand location and a visual afterimage, the visual afterimage of the hand disappeared. This suggests that when multisensory input is contradictory, the central nervous system may try to arrange sensory information in relations to other sensory modalities, or even adapt motor output to muscles (eg, less contraction to more accurately reach the target).

In a study with mismatches between proprioception and vision, participants were asked to point toward a target with their unseen hand.17 The relationship between proprioception and vision was manipulated by imposing erroneous visual feedback about the target’s location.17 With the distorted visual feedback, participants corrected their responses toward the adjusted visual image up to 60% of the distance of the incorrect visual feedback. When a sensory modality is less reliable or provides contradictory information, less weight is placed on the unreliable sense.18, 19 Proprioception is impaired in SCNP.11, 20 However, it is not clear exactly how proprioceptive mismatch affects integration of other senses. It is possible that SCNP may cause greater reliance on senses other than proprioception; however, it is also possible that the less reliable proprioceptive input in SCNP can negatively influence the processing of other sensory stimuli.

Previous research has indicated that multisensory integration in elderly populations is enhanced, as measured using a 2-alternative, forced-choice discrimination task involving measurement of response times.21 Another study reported that the elderly have both altered SMI and altered multisensory integration.22 Tasks such as temporal order judgements may not be effective at measuring multisensory integration in naïve participants because there is an experience component that “increases” intersensory synchrony ability.23

Areas in the thalamus integrate sensorimotor and multisensory processes.24 The superior colliculus is 1 example of a multisensory site that has access to efferent projections of premotor and motor areas of the spinal cord and brainstem involved in superior colliculus–mediated attentive and orientation behaviors,25 some that involve the saccadic movements of the eye, and neck movements, or “gaze shifts.” In addition to 2 sensory modalities terminating in a target area, a cross-modal projection of 1 sensory modality can also converge onto a different sensory modality site.26 Hairston et al27 reported evidence for inverse effectiveness, where asymptomatic participants with artificially degraded vision (induced myopia) had their localization skills enhanced for audiovisual conditions, whereas in normal conditions the localization for multisensory conditions was similar to unisensory conditions. These papers suggest that a similar effect could occur in populations with altered sensory input from the neck, where that multisensory integration may be enhanced, as a result of ongoing alterations in sensory feedback from the neck joints and muscles that lead to degraded somatosensory input, similar to the degraded vision.

Numerous methods can be used to measure multisensory integration.21, 23, 25, 28 A popular task that uses behavioral enhancements from multisensory integration is a 2-alternative forced-choice discrimination task with semantically congruent, redundant, multisensory stimuli.21, 28 In some studies researchers accounted for the redundancy gain, a quickening of response times that occurs with redundant stimuli, by using the race model.29 When measuring multisensory integration, temporal and spatial factors of the equipment used to present the stimuli must be carefully considered when designing a task, because both timing and location of stimuli may reduce or deplete multisensory activity.30, 31 Unfortunately, many studies fail to state or consider in detail the equipment being used in multisensory tasks, which can hinder interpretation of results,21, 23, 28 a limitation that the present study tries to address.

The purpose of this study was to determine if there were differences in multisensory integration and unisensory and multisensory response times in individuals with SCNP compared with asymptomatic participants, and if the results were consistent over a 4-week interval in the absence of treatment for the SCNP group. It was hypothesized that individuals with SCNP would possess slower response times for both unisensory and multisensory conditions because of the ongoing effects of unreliable proprioceptive feedback from the neck.

Section snippets

Population

Participants were recruited from University of Ontario Institute of Technology campus using advertisements and word of mouth. The mean age for the asymptomatic controls (n = 13; 6 men) was 21.1 ± 2.1 years and for the SCNP group (n = 12; 5 men) was 22.0 ± 2.1 years. The Edinburgh handedness scale32 was used to determine hand dominance because the responses in the protocol were developed for the right hand. This was important to ensure that the numbers of left-handed and ambidextrous individuals

Results

The mean responses less than 250 ms and mean accuracy for these responses can be found in Table 1. The mean accuracy is reported in Table 2. The overall mean response time and accuracy for the asymptomatic controls and SCNP groups exceeded 95% in all stimulus conditions. In all conditions except 1 (week 4 visual), the SCNP group possessed larger variation than the control.

The mean response times for both SCNP and asymptomatic controls reported in Table 2 are also depicted in Figure 2 for

Discussion

The results described are the first to reveal that there is a significant difference in response times for visual and multisensory stimuli in a 2-alternative forced-choice discrimination task between adults with SCNP and asymptomatic controls. These differences are not simply because of slower movement times in general, because previous studies of people with SCNP reported no difference in simple response times in this population but found that the SCNP group had slower response times in more

Conclusion

This is the first study to report that people with SCNP possess slower visual and multisensory response times. These differences persist over 4 weeks, suggesting that the measure is reliable over time and that differences caused by SCNP do not improve on their own in the absence of treatment.

Funding Sources and Potential Conflicts of Interest

The authors received funding from the Australian Spinal Research Foundation (LG 2013-22), Natural Sciences and Engineering Research Council of Canada Discovery Grants, and Canada Foundation for Innovation - John R Evans Leaders Fund. No conflicts of interest were reported for this study.

Practical Applications

  • The ability of the brain to integrate sensory inputs is affected in those with recurrent neck pain.

  • The response time to visual and combined audiovisual inputs was slower in the recurrent neck pain

Contributorship Information

  • Concept development (provided idea for the research): B.F., M.H., H.H., B.A.M.

  • Design (planned the methods to generate the results): B.F., P.Y., B.A.M.

  • Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): B.F., P.Y., B.A.M.

  • Data collection/processing (responsible for experiments, patient management, organization, or reporting data): B.F.

  • Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the

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