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Influence of Subclinical Neck Pain on the Ability to Perform a Mental Rotation Task: A 4-Week Longitudinal Study With a Healthy Control Group Comparison

Published:January 30, 2016DOI:https://doi.org/10.1016/j.jmpt.2015.12.002

      Abstract

      Objective

      Mental rotation of objects and the frame of reference of those objects are critical for executing correct and skillful movements and are important for object recognition, spatial navigation, and movement planning. The purpose of this longitudinal study was to compare the mental rotation ability of those with subclinical neck pain (SCNP) to healthy controls at baseline and after 4 weeks.

      Methods

      Twenty-six volunteers (13 SCNP and 12 healthy controls) were recruited from a university student population. Subclinical neck pain participants had scores of mild to moderate on the Chronic Pain Grade Scale, and controls had minimal or no pain. For the mental rotation task, participants were presented with an object (letter “R”) on a computer screen presented randomly in either normal or backwards parity at various orientations (0°, 45°, 90°, 135°, 180°, 225°, 270°, and 315°). Participants indicated the object's parity by pressing “N” for normal or “B” for backwards. Each orientation for normal and backward parities was presented 5 times, and the average response time for all letter presentations was calculated for each participant, at baseline and 4 weeks later.

      Results

      Both groups had overall improved response times from baseline to 4 weeks. Healthy participants had significantly improved response times compared to SCNP, both at baseline (P < .05) and 4 weeks (P < .05).

      Conclusions

      Healthy participants performed better than the SCNP group at both time points. Subclinical neck pain may impair the ability to perform a complex mental rotation task involving cerebellar connections, possibly due to altered body schema.

      Key Indexing Terms

      The concept of an altered body schema in individuals with chronic pain has become a recent area of interest, with the altered schema extending to peripersonal space.
      • Moseley GL
      • Gallace A
      • Spence C
      Bodily illusions in health and disease: physiological and clinical perspectives and the concept of a cortical “body matrix”.
      Mental rotation is the ability to rotate mental representations of 2 or 3 dimensional figures rapidly and accurately. Mental rotation is a complex task requiring prediction and cerebellar involvement,
      • Creem-Regehr SH
      • Neil JA
      • Yeh HJ
      Neural correlates of 2 imagined egocentric transformations.
      • Popa LS
      • Hewitt AL
      • Ebner TJ
      Purkinje cell simple spike discharge encodes error signals consistent with a forward internal model.
      and 1 past study showed that ability to mentally rotate an object improved with a single session of neck manipulation.
      • Kelly DD
      • Murphy BA
      • Backhouse DP
      Use of a mental rotation reaction-time paradigm to measure the effects of upper cervical adjustments on cortical processing: a pilot study.
      Neck pain has been shown to impact upper limb proprioception,
      • Haavik H
      • Murphy B
      Subclinical neck pain and the effects of cervical manipulation on elbow joint position sense.
      and recent neurophysiologic studies suggest that individuals with neck pain may have altered cerebellar processing.
      • Daligadu J
      • Haavik H
      • Yielder PC
      • Baarbe J
      • Murphy B
      Alterations in cortical and cerebellar motor processing in subclinical neck pain patients following spinal manipulation.
      Subclinical neck pain (SCNP)
      • Lee H
      • Nicholson LL
      • Adams RD
      Cervical range of motion associations with subclinical neck pain.
      • Lee H
      • Nicholson LL
      • Adams RD
      • Bae S-S
      Proprioception and rotation range sensitization associated with subclinical neck pain.
      • Lee H-Y
      • Wang J-D
      • Yao G
      • Wang S-F
      Association between cervicocephalic kinesthetic sensibility and frequency of subclinical neck pain.
      refers to mild-to-moderate recurrent neck pain for which participants have not yet sought treatment. Individuals with SCNP show decreased neck range of motion, cervical kinesthesia, and muscle endurance.
      • Lee H
      • Nicholson LL
      • Adams RD
      Cervical range of motion associations with subclinical neck pain.
      • Lee H
      • Nicholson LL
      • Adams RD
      • Bae S-S
      Proprioception and rotation range sensitization associated with subclinical neck pain.
      • Lee H-Y
      • Wang J-D
      • Yao G
      • Wang S-F
      Association between cervicocephalic kinesthetic sensibility and frequency of subclinical neck pain.
      Individuals with SCNP may have days when they do not experience pain. Therefore, they provide an opportunity to explore the neurophysiologic impact of chronic changes in sensory input from the neck
      • Bolton P
      • Holland C
      An in vivo method for studying afferent fibre activity from cervical paravertebral tissue during vertebral motion in anaesthetised cats.
      without the confounding effect of current pain, which has been shown in previous studies to affect measures of sensorimotor integration and motor control.
      • Rossi S
      • della Volpe R
      • Ginanneschi F
      • et al.
      Early somatosensory processing during tonic muscle pain in humans: relation to loss of proprioception and motor “defensive” strategies.
      • Strutton PH
      • Theodorou S
      • Catley M
      • McGregor AH
      • Davey NJ
      Corticospinal excitability in patients with chronic low back pain.
      • Waberski T
      • Lamberty K
      • Dieckhöfer A
      • Buchner H
      • Gobbele R
      Short-term modulation of the ipsilateral primary sensory cortex by nociceptive interference revealed by SEPs.
      Recent work using transcranial magnetic stimulation
      • Daligadu J
      • Haavik H
      • Yielder PC
      • Baarbe J
      • Murphy B
      Alterations in cortical and cerebellar motor processing in subclinical neck pain patients following spinal manipulation.
      showed that cerebellar function is altered in individuals with SCNP in comparison to healthy controls. Normally, the cerebellum disinhibits to allow learning of new motor skills. This ability is impaired in individuals with low-level neck pain. This influence raises the possibility that altered cerebellar processing of afferent input may contribute to alterations in other cerebellar dependent functions such as kinesthesia and spatial awareness.
      The cerebellum is important in both feedback and feedforward models of motor control, using afferent feedback to update body schema to maintain accuracy of feedforward control of movement.
      • Popa LS
      • Hewitt AL
      • Ebner TJ
      Purkinje cell simple spike discharge encodes error signals consistent with a forward internal model.
      The cerebellum also plays a critical role in spatial processing and object recognition.
      • Picazio S
      • Oliveri M
      • Koch G
      • Caltagirone C
      • Petrosini L
      Cerebellar contribution to mental rotation: a cTBS study.
      The study by Picazio et al
      • Picazio S
      • Oliveri M
      • Koch G
      • Caltagirone C
      • Petrosini L
      Cerebellar contribution to mental rotation: a cTBS study.
      used continuous theta burst stimulation (cTBS) to decrease cerebellar hemispheric excitability in healthy adult participants performing a mental rotation task. Mental rotation ability is important for a number of abilities such as acquiring spatially complex skills, object recognition, problem solving, and action planning.
      • Creem-Regehr SH
      • Neil JA
      • Yeh HJ
      Neural correlates of 2 imagined egocentric transformations.
      Mental rotation is used in flight navigation
      • Taylor HA
      • Brunyé TT
      • Taylor ST
      Spatial mental representation: implications for navigation system design.
      as well as sport performance.
      • Moreau D
      • Mansy-Dannay A
      • Clerc J
      • Guerrien A
      Spatial ability and motor performance: assessing mental rotation processes in elite and novice athletes.
      In the study by Picazio et al,
      • Picazio S
      • Oliveri M
      • Koch G
      • Caltagirone C
      • Petrosini L
      Cerebellar contribution to mental rotation: a cTBS study.
      decreasing the input from the left cerebellar hemisphere using cTBS led to slower mental rotation response times for both an embodied mental rotation task requiring an egocentric mental rotation strategy and an abstract mental rotation task, which required an allocentric strategy, as compared to sham cTBS.
      The involvement of the cerebellum in mental rotation is intriguing in light of 1 previous study that showed that upper cervical manipulation enhanced mental rotation ability in individuals with neck joint dysfunction compared to a group receiving a sham treatment.
      • Kelly DD
      • Murphy BA
      • Backhouse DP
      Use of a mental rotation reaction-time paradigm to measure the effects of upper cervical adjustments on cortical processing: a pilot study.
      Altered kinesthetic awareness is known to occur in SCNP participants,
      • Haavik H
      • Murphy B
      Subclinical neck pain and the effects of cervical manipulation on elbow joint position sense.
      • Lee H
      • Nicholson LL
      • Adams RD
      • Bae S-S
      Proprioception and rotation range sensitization associated with subclinical neck pain.
      • Lee H-Y
      • Wang J-D
      • Yao G
      • Wang S-F
      Association between cervicocephalic kinesthetic sensibility and frequency of subclinical neck pain.
      and it seems likely that this may extend to altered spatial awareness of objects. If mental rotation ability is impaired in individuals with recurrent neck pain relative to healthy controls, it would suggest that the altered cerebellar processing could be contributing to not only a disrupted body schema but also disruptions in spatial recognition of objects.
      Therefore, the aim of the current study was to compare mental rotation in a group of individuals with recurrent neck pain to a healthy control group and to follow up this comparison at 4 weeks in the absence of any treatment for the neck pain group. We hypothesized that those in the SCNP group would have slower response times when performing mental rotation and that this would not be explained by changes in movement time (indicated by response time when the object was presented in normal orientation at 0° of rotation). Furthermore, we hypothesized that although both groups would improve over time due to task familiarity, the SCNP group would still show decreased mental rotation ability relative to the control group after 4 weeks.

      Methods

      Participants

      Thirteen participants (age, 21.2 ± 1.9 years; 8 females and 5 males) with self-reported neck pain but minimal acute pain on the day of testing participated in the study. Participants were shown a continuous 10-cm line and were asked to indicate their average pain in the experimental week from minimal pain severity on the far left of the line to maximal pain severity on the far right, also known as the visual analog scale. These participants additionally were classified as grades I to III on the Chronic Pain Grading Scale which categorizes pain intensity and disability between a grade of 0, meaning the participant had minimal pain in the previous 6 months, and a grade of IV, meaning very severe pain intensity and disability in the previous 6 months.
      • Guzman J
      • Hurwitz EL
      • Carroll LJ
      • et al.
      A new conceptual model of neck pain: linking onset, course, and care: the Bone and Joint Decade 2000-2010 Task Force on Neck Pain and Its Associated Disorders.
      • Von Korff M
      • Ormel J
      • Keefe FJ
      • Dworkin SF
      Grading the severity of chronic pain.
      The Chronic Pain Grade Scale indicates the average pain over 6 months, so the scores indicate the amount of pain of the participant on average over 6 months, but on the day of the experiment, they had no pain. Participants had to be free of pain on the day of the experiment or else they could not participate in the study. All participants were right handed with a mean score (±SD) of 71.6 ± 18.2 on the Edinburgh Handedness Inventory.
      • Oldfield RC
      The assessment and analysis of handedness: the Edinburgh inventory.
      Data were also collected from a healthy control group of 12 participants (21.9 ± 2.1 years; 3 females and 9 males) without neck pain or a history of neck pain/injury. These participants had an Edinburgh Handedness Inventory score (±SD) of 73.0 ± 30.5 and very low grading on the Chronic Pain Grade Scale (0 disability points and characteristic pain intensity score ≤23).
      Exclusion to participate included major structural injuries or anomalies to the cervical spine including disk herniation or fracture. As well, participants were excluded if they had received care for their neck condition in the past 3 months. Other exclusion items included inflammatory or system conditions (eg, rheumatoid arthritis or infection), trauma or other severe injury to the spine, radicular arm pain, hypermobility, intake of anticoagulant medication or bleeding disorders, history of stroke or cancer in the past 5 years, and vertigo or dizziness. Neck pain participants had to provide the history, frequency, duration, location, and severity in the week of testing and during flare-ups in the previous 6 months, as well as functional ability to participate in activities of daily living. Ethical approval was obtained from the University of Ontario Institute of Technology Research Ethics Board, participants provided informed consent before participating, and the study was performed in keeping with the human right principles set out in the Declaration of Helsinki.

      Experimental Protocol

      The participants attended 2 sessions, at baseline and 4 weeks later. At each session, they were seated in a comfortable chair facing a laptop computer (ThinkPad T500 series; Lenovo, Beijing, China). A fixation point would appear on the screen, and at random intervals of 200 to 400 ms, the letter “R” was presented. “R” was randomly presented in either backwards (“Я”) or normal orientation, at various degrees of rotation (0°, 45°, 90°, 135°, 180°, 225°, 270°, and 315°) (Figure 1). The letter “R” was chosen as past research has demonstrated that there was no difference between males and females in the ability to perform mental rotation of letters and polygons.
      • Cohen W
      • Polich J
      No hemispheric differences for mental rotation of letters or polygons.
      Because we did not know at the outset the number of males and females that would end up in each group, we wanted to be sure that differences in male and female participation numbers between the groups would not influence group results. We also ensured that the experimental session was performed in a comfortable posture which would limited excessive movement of shoulders and neck (only the index and middle finger had to move to select the response) to prevent the onset of fatigue or movement-induced pain. The computer was also set at an eye level that was comfortable to the participant and allowed them to maintain a comfortable upright head posture. To be sure that participants were without pain on the day of testing, participants were told to report pain that may have occurred with the experimental session, and the laboratory attendants were trained to ask participants whether they had pain and if need be collect on another day. Participants had to be free of pain on the day of the experiment or else they could not be tested.
      Figure thumbnail gr1
      Fig 1The letter “R” at various orientation angles in both its normal and mirror-image orientations.
      Participants had to indicate the object's orientation by pressing “N” for normal or “B” for backwards with their dominant hand index finger which was positioned proximate to the computer key pad. These 2 letters are adjacent to each other on the key pad which meant that there would be no difference in the time required to reach each letter. After the participant's judgement as to normal or backwards orientation, a visual prompt was presented saying “Press any key to continue.” Each orientation was presented 5 times, and the response time from object presentation to key press was measured using E-prime software (Psychology Software Tools, Sharpsburg, MD). The average response time to all letter presentations was calculated for each participant both at baseline and when they repeated the task 4 weeks later.

      Simple Response Time

      Figure 2 demonstrates events of response time, which mainly include (1) time for recognizing the stimulus, (2) time for cognitively rotating the stimulus, and (3) time for motor initiation and movement. To determine any differences between neck pain and healthy in the time they needed to recognize the stimulus and initiate the movement, which are processes separate from cognitive mental rotation, the response time to respond to letter “R” in normal orientation at 0° was analyzed and called “simple response time.” This measure would more purely indicate response time to perform the task without demands on cognitive resources to rotate the image, so as to provide a way to compare whether recognition and movement time, rather than mental rotation ability, was different between the 2 groups.
      Figure thumbnail gr2
      Fig 2Response time begins at the presentation of a stimulus and includes recognition, the cognitive function of rotating an object, and time for motor initiation and movement until the participant has selected their desired response.

      Data Collection and Analysis

      The data were collected and stored within E-Studio software (Psychology Software Tools). The first presentation of each rotation angle for the forward and mirror-image chiral forms was removed from analysis because these were considered to be part of the warm-up while participants were still learning the task. The remaining trials were averaged to determine response time to identify either the normal or mirror-image chiral form and accuracy of the selection (expressed as percent correct).

      Statistical Analysis

      Changes in mental rotation response time over time were assessed using a 2-way repeated-measures analysis of variance. The average mental rotation response time between the 2 groups was compared at baseline and at 4 weeks using unpaired t tests. Accuracy between neck pain and healthy at baseline and at 4 weeks was assessed using χ2 tests. Statistical analysis was performed using IBM SPSS Statistics for Windows, Version 19.0 (IBM Corp, Armonk, NY). Statistical significance was set at P < .05.
      Simple response time was tested at baseline and at 4 weeks using a 2-way repeated-measures analysis of variance to compare differences in response time between normal and mirror-image chiral forms. Self-paced delay between trials (the time that elapsed from presentation of the screen “Press any key to continue” until participants responded) was also assessed with 2-way repeated-measures analysis of variance to ensure that any improvements after the 4 weeks were not due to changes in mental processing time between trials.

      Results

      The neck pain group pain characteristics are summarized in Table 1, and mean response times for each orientation angle of “R” in its normal parity are shown in Figure 3. There was a main effect of time for mental rotation response time (F1,23 = 8.93; P = .006 with no significant interaction) (Figure 4). The baseline mental rotation response time was significantly faster (P < .05) for healthy vs SCNP groups (994.4 ± 211.9 milliseconds vs 1220.9 ± 294.5 milliseconds). At 4 weeks, mental rotation time improved for the healthy group to 834.0 ± 183.3 milliseconds, a 160.4 ± 156.0 millisecond (or 16.1%) improvement, whereas the SCNP group improved to 1115.8 ± 220.8 milliseconds, a 105.0 ± 263.6 millisecond (or 8.6%) improvement.
      Table 1Neck Pain Group Characteristics at Baseline and After 4 Weeks
      Neck Pain CharacteristicsWeek 0Week 4
      Frequency of neck pain (days per months)13.9 ± 8.112.55 ± 9.1
      Duration of neck pain (y)2.3 ± 2.0N/A
      Average neck pain on experimental week (cm on 10-cm VAS)2.79 ± 2.233.06 ± 2.39
      Chronic Pain Grade Scale score (0-4 minimal to severe)1.46 ± 0.781.42 ± 0.79
      Results are presented as mean ± SD. N/A, not applicable; VAS, visual analog scale.
      Figure thumbnail gr3
      Fig 3Average response times (milliseconds) for each orientation angle of “R” in its normal parity for neck pain and healthy groups at baseline (week 0) and at 4 weeks in the absence of any intervention.
      Figure thumbnail gr4
      Fig 4Average response times (milliseconds) for neck pain and control groups at baseline (week 0) and 4-week follow-up in the absence of any intervention (P < .05; ⁎⁎P < .01). Error bars represent SDs. SCNP, subclinical neck pain.
      The average of the simple response time for the letter “R” presented at 0° of rotation at baseline was 783.7 ± 191.7 milliseconds for the neck pain group and 815.1 ± 311.9 milliseconds for the healthy group, whereas at week 4, it was 793.4 ± 320.3 milliseconds for the neck pain group and 682.3 ± 150.3 milliseconds for the healthy group (Figure 5). There was no difference in this “simple” response time over the 4 weeks and no significant differences between groups for the response time when the letter was not rotated.
      Figure thumbnail gr5
      Fig 5Average simple response times (milliseconds) for the neck pain and healthy groups to recognize shape in normal orientation at 0°. Error bars represent SDs. SCNP, subclinical neck pain.
      There were no differences between the neck pain and healthy groups for accuracy scores at baseline (week 0). However, the healthy group improved from 93.5% ± 8.5% accurate at baseline to 95.9% ± 3.5% at 4 weeks, whereas the neck pain group declined in their accuracy from 94.7% ± 4.7% accurate at baseline to 93.5% ± 7.3% at 4 weeks (χ2 = 4.24; P = .039) (Figure 6). Neck pain participants had an average self-timed delay between events of 363.8 ± 170.8 milliseconds at baseline and 382.8 ± 214.9 at 4 weeks. The healthy participants had an average self-timed delay between events of 433.6 ± 190.2 milliseconds at baseline and 438.0 ± 224.0 milliseconds at 4 weeks (Figure 7). No differences were seen in this self-time delay over the 4-week period, and there were no significant differences between the 2 groups.
      Figure thumbnail gr6
      Fig 6Accuracy of mental rotation performance (P < .05). Error bars represent SDs. SCNP, subclinical neck pain.
      Figure thumbnail gr7
      Fig 7Average time (milliseconds) between events at baseline and 4 weeks for neck pain and healthy participants. Error bars represent SDs. SCNP, subclinical neck pain.

      Discussion

      The main finding of this study was that the SCNP group had significantly slower mental rotation response times than healthy controls both at baseline and after 4 weeks. Although both groups improved in response time over 4 weeks, as predicted, the healthy group improved more (16.1%) than the control group (8.6%). Participants in the healthy group had significantly greater accuracy at 4 weeks as compared to participants in the SCNP group, who performed slightly worse than baseline. These results suggest that neck joint dysfunction significantly impairs cognitive processing. This impairment is unlikely due to the presence of pain itself because the study population had minimal symptoms on the day they participated in this study.
      These results are unlikely to be due to differences in response time between letter presentations or due to differences in movement time between participants. There was no change in the self-paced delay between events, indicating that participants were not taking more or less time between stimulus presentations after 4 weeks (ie, they were not simply improving because they were faster at the task, but they were actually better at performing the mental rotations). In addition, there was no difference between the groups or between baseline and 4 weeks in the response time for the letter “R” presented in its normal orientation. The response time during a mental rotation task is a made up of the premotor response time to recognize a stimulus, the motor response time from stimulus recognition to the onset of muscle activity, and movement time from when the arm begins to move to press the keys. The similarity in response time to recognize the letter “R” in its normal upright orientation at 0° means that there was no difference between groups in the combination of time to recognize the stimulus and initiate movement (Fig 2), indicating that the neck pain group did not have slower mental rotation response times because they were moving more slowly due to their neck problem.

      Evidence for Increased Time to Mental Congruence as a Result of Altered Cerebellar Processing

      During mental rotation, premotor response time increases linearly as object orientation angle increases, suggesting that subjects mentally rotate the object into congruence before responding.
      • Shepard RN
      • Metzler J
      Mental rotation of three-dimensional objects.
      Therefore, the longer mental rotation response times in the neck pain group in the face of unchanged response times for the letter in its normal orientation indicate that SCNP participants are taking longer to mentally rotate the object into congruence before responding, rather than changing their movement speed. We suspect that this is due to altered cerebellar function in the neck pain group. Recent work has shown altered cerebellar function in SCNP individuals.
      • Daligadu J
      • Haavik H
      • Yielder PC
      • Baarbe J
      • Murphy B
      Alterations in cortical and cerebellar motor processing in subclinical neck pain patients following spinal manipulation.
      A transcranial magnetic stimulation study demonstrated that SCNP patients do not show disinhibition in response to a motor learning task, whereas healthy control participants disinhibit significantly.
      Furthermore, there is decreased kinesthesia in SCNP populations for both the upper limb
      • Haavik H
      • Murphy B
      Subclinical neck pain and the effects of cervical manipulation on elbow joint position sense.
      and neck.
      • Lee H
      • Nicholson LL
      • Adams RD
      Cervical range of motion associations with subclinical neck pain.
      • Lee H
      • Nicholson LL
      • Adams RD
      • Bae S-S
      Proprioception and rotation range sensitization associated with subclinical neck pain.
      • Lee H-Y
      • Wang J-D
      • Yao G
      • Wang S-F
      Association between cervicocephalic kinesthetic sensibility and frequency of subclinical neck pain.
      This suggests that the altered sensory input from the neck may be leading to altered kinesthesia as a result of an altered body schema which is partially encoded in the cerebellum.
      One way that the central nervous system controls movement is by creating an internal model of the body and using this model to predict the sensory consequences of the movement.
      • Shadmehr R
      • Smith MA
      • Krakauer JW
      Error correction, sensory prediction, and adaptation in motor control.
      There is growing evidence that the cerebellum plays a critical role in creating this internal model.
      • Shadmehr R
      • Smith MA
      • Krakauer JW
      Error correction, sensory prediction, and adaptation in motor control.
      The simple spike firing of cerebellar Purkinje cells is highly correlated with movement kinematics.
      • Hewitt AL
      • Popa LS
      • Pasalar S
      • Hendrix CM
      • Ebner TJ
      Representation of limb kinematics in Purkinje cell simple spike discharge is conserved across multiple tasks.
      A recent study in monkeys demonstrated that cerebellar Purkinje neurons demonstrate firing properties consistent with signaling feedforward internal predictions used for compensatory movements, as well as receiving sensory feedback about actual movements to monitor performance.
      • Popa LS
      • Hewitt AL
      • Ebner TJ
      Purkinje cell simple spike discharge encodes error signals consistent with a forward internal model.
      Mental rotation tasks typically require either manipulation of the frame of reference of the participant (ie, egocentric frame of reference) or rotations of the object's frame of reference (ie, allocentric frame of reference). Creem-Regehr et al
      • Creem-Regehr SH
      • Neil JA
      • Yeh HJ
      Neural correlates of 2 imagined egocentric transformations.
      compared performance and functional magnetic resonance imaging activation on 2 different mental rotation tasks, one requiring rotation of the involved body part (hand) and the other requiring body (perspective) transformations. They found that both types of tasks created activation in the lateral occipital areas, inferior and superior parietal cortex, and the cerebellum.
      • Creem-Regehr SH
      • Neil JA
      • Yeh HJ
      Neural correlates of 2 imagined egocentric transformations.
      Further weight to the importance of the cerebellum in the ability to perform mental rotation tasks was provided by the cTBS study by Picazio et al.
      • Picazio S
      • Oliveri M
      • Koch G
      • Caltagirone C
      • Petrosini L
      Cerebellar contribution to mental rotation: a cTBS study.
      These authors demonstrated that decreasing input from the left cerebellar hemisphere using cTBS led to slower mental rotation response times for both an embodied mental rotation task requiring an egocentric mental rotation strategy and an abstract mental rotation task which required an allocentric strategy.

      Potential Influence of SCNP in Real-World Tasks

      Neck pain is known to influence our internal reference frame, affecting spatial judgement and processing. Paulus and Brumagne
      • Paulus I
      • Brumagne S
      Altered interpretation of neck proprioceptive signals in persons with subclinical recurrent neck pain.
      found that participants with neck pain judged their shoulder to be raised higher during passive shoulder elevation compared to asymptomatic controls. Haavik and Murphy
      • Haavik H
      • Murphy B
      Subclinical neck pain and the effects of cervical manipulation on elbow joint position sense.
      found that participants with nonsevere SCNP performed poorly when replicating elbow position with eyes closed compared to healthy controls. Participants with neck pain also show an impaired ability to reposition the head to a neutral position.
      • Lee H-Y
      • Wang J-D
      • Yao G
      • Wang S-F
      Association between cervicocephalic kinesthetic sensibility and frequency of subclinical neck pain.
      • Kristjansson E
      • Dall'Alba P
      • Jull G
      A study of five cervicocephalic relocation tests in three different subject groups.
      Lee et al
      • Lee H-Y
      • Wang J-D
      • Yao G
      • Wang S-F
      Association between cervicocephalic kinesthetic sensibility and frequency of subclinical neck pain.
      found that participants with neck pain showed more absolute error when positioning their head to a neutral position (eg, comfortable position with head facing straight ahead) compared to a target (eg, self-selected midpoint within the participant's maximum range of motion).
      The head's position may also influence the body's perception of itself in space and may be a source of altered representation in the body's internal model. Paulus and Brumagne
      • Paulus I
      • Brumagne S
      Altered interpretation of neck proprioceptive signals in persons with subclinical recurrent neck pain.
      found that participants with nonsevere but recurrent neck pain repositioned their head more dramatically (eg, with greater degree of displacement) away from the side where the trunk was bending than asymptomatic controls. Of interest, this more dramatic head positioning during passive shoulder elevation corresponded with greater trunk movement and perception of a higher shoulder during passive shoulder elevation.
      • Paulus I
      • Brumagne S
      Altered interpretation of neck proprioceptive signals in persons with subclinical recurrent neck pain.
      Guerraz et al
      • Guerraz M
      • Caudron S
      • Thomassin N
      • Blouin J
      Influence of head orientation on visually and memory-guided arm movements.
      found that head posture greatly impacted the ability of participants to replicate an object using simple arm tracing. For this study, participants lay supine and were asked to view an object and then trace the shape of this object with their unseen index finger using elbow and shoulder movements. The tracing was completed in 2 conditions: with eyes closed and with eyes open (viewing only the object and not arm movements or the tracing). When the head was tilted, there was a bias of spatial arm movements toward the opposite direction during both memory-guided and visually guided movements. Two experiments were performed: Specifically for the first experiment, the head was held straight while viewing the object and then tilted during tracing. In the second experiment, the head was tilted at 30° during both viewing and tracing. Bias was seen in both instances as long as participants replicated the movements with their head tilted. The bias was not seen when participants replicated the movement with their head straight. When vision was added (to view arm movements and tracing), bias decreased significantly for the leftward head tilt in both experiments. Notably, the participants perceived the tracing as being in line with their body, although the traces were biased by the head tilt.
      • Guerraz M
      • Caudron S
      • Thomassin N
      • Blouin J
      Influence of head orientation on visually and memory-guided arm movements.
      A recent study found that changing visual feedback altered the amount of pain-free neck rotation in a group of chronic neck pain patients.
      • Harvie DS
      • Broecker M
      • Smith RT
      • Meulders A
      • Madden VJ
      • Moseley GL
      Bogus visual feedback alters onset of movement-evoked pain in people with neck pain.
      This indicates an increased reliance on visual input in this group, possibly because their internal body schema or body map is not accurately calibrated, leading to altered integration of sensory input.

      Limitations

      Only 26 participants (13 SCNP and 12 controls) were tested, and these participants came from a relatively homogenous group of university-aged individuals. The testing of a larger participant population would allow us to assess more fully the influence of SCNP on mental rotation in the general population and especially in older people. Mental rotation on a computer screen is a poor reference to explain the complex tasks that humans engage in, and consideration ought to be given to the behavioral level to explain more fully altered cerebellar processing in SCNP participants and the potential impact to motor control and timing of movement.

      Conclusion

      Mental rotation ability, which is partially encoded by the cerebellum along with body schema, is compromised in individuals with recurrent neck pain. This impairment is unlikely due to the presence of pain itself because the study population had minimal symptoms on the day they participated in this study. We suggest that people who are developing neck pain may have disrupted sensorimotor function of the neck that, even without perceived current pain, can disrupt processing and integration of other sensory inputs.

      Funding Sources and Potential Conflicts of Interest

      The following organizations provided support and funding for this study: Australian Spinal Research Foundation, Natural Science and Engineering Research Council of Canada, Canada Foundation for Innovation and the Canadian Institutes of Health Research, University of Ontario Institute of Technology, and Ontario Graduate Scholarship Fund for graduate student funding. No conflicts of interest were reported for this study.

      Contributorship Information

      • Concept development (provided idea for the research): B.M., H.H., J.B.
      • Design (planned the methods to generate the results): B.M., J.B., M.H., H.H.
      • Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): B.M., H.H., M.H.
      • Data collection/processing (responsible for experiments, patient management, organization, or reporting data): J.B.
      • Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): J.B., H.M., B.M.
      • Literature search (performed the literature search): J.B., B.M.
      • Writing (responsible for writing a substantive part of the manuscript): J.B., B.M.
      • Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): H.H., M.H., H.M., B.M.

      Practical Applications

      • Mental rotation ability is compromised in individuals with subclinical neck pain when compared with healthy controls and remains worse even when remeasured after 4 weeks of with no intervention.
      • There is no difference in simple response time indicating that the differences are not due to differences in movement time
      • This impairment is unlikely due to the presence of pain itself because the study population had minimal symptoms on the day they participated in this study.
      • Altered sensory input from the neck impacts the spatial awareness of objects

      References

        • Moseley GL
        • Gallace A
        • Spence C
        Bodily illusions in health and disease: physiological and clinical perspectives and the concept of a cortical “body matrix”.
        Neurosci Biobehav Rev. 2012; 36: 34-46
        • Creem-Regehr SH
        • Neil JA
        • Yeh HJ
        Neural correlates of 2 imagined egocentric transformations.
        Neuroimage. 2007; 35: 916-927
        • Popa LS
        • Hewitt AL
        • Ebner TJ
        Purkinje cell simple spike discharge encodes error signals consistent with a forward internal model.
        Cerebellum. 2013; 12: 331-333
        • Kelly DD
        • Murphy BA
        • Backhouse DP
        Use of a mental rotation reaction-time paradigm to measure the effects of upper cervical adjustments on cortical processing: a pilot study.
        J Manipulative Physiol Ther. 2000; 23: 246-251
        • Haavik H
        • Murphy B
        Subclinical neck pain and the effects of cervical manipulation on elbow joint position sense.
        J Manipulative Physiol Ther. 2011; 34: 88-97
      1. Baarbé J Yielder P Haavik H Holmes M Debison-Larabie C Murphy B Enhanced cerebellar disinhibition when cervical manipulation precedes motor learning in patients with subclinical neck pain. World Federation of Chiropractic Biannual Meeting; 2015 May 13-16; Athens, Greece. 2015
        • Daligadu J
        • Haavik H
        • Yielder PC
        • Baarbe J
        • Murphy B
        Alterations in cortical and cerebellar motor processing in subclinical neck pain patients following spinal manipulation.
        J Manipulative Physiol Ther. 2013; 36: 527-537
        • Lee H
        • Nicholson LL
        • Adams RD
        Cervical range of motion associations with subclinical neck pain.
        Spine. 2004; 29: 33-40
        • Lee H
        • Nicholson LL
        • Adams RD
        • Bae S-S
        Proprioception and rotation range sensitization associated with subclinical neck pain.
        Spine. 2005; 30: E60-E67
        • Lee H-Y
        • Wang J-D
        • Yao G
        • Wang S-F
        Association between cervicocephalic kinesthetic sensibility and frequency of subclinical neck pain.
        Man Ther. 2008; 13: 419-425
        • Bolton P
        • Holland C
        An in vivo method for studying afferent fibre activity from cervical paravertebral tissue during vertebral motion in anaesthetised cats.
        J Neurosci Methods. 1998; 85: 211-218
        • Rossi S
        • della Volpe R
        • Ginanneschi F
        • et al.
        Early somatosensory processing during tonic muscle pain in humans: relation to loss of proprioception and motor “defensive” strategies.
        Clin Neurophysiol. 2003; 114: 1351-1358
        • Strutton PH
        • Theodorou S
        • Catley M
        • McGregor AH
        • Davey NJ
        Corticospinal excitability in patients with chronic low back pain.
        J Spinal Disord Tech. 2005; 18: 420-424
        • Waberski T
        • Lamberty K
        • Dieckhöfer A
        • Buchner H
        • Gobbele R
        Short-term modulation of the ipsilateral primary sensory cortex by nociceptive interference revealed by SEPs.
        Neurosci Lett. 2008; 435: 137-141
        • Picazio S
        • Oliveri M
        • Koch G
        • Caltagirone C
        • Petrosini L
        Cerebellar contribution to mental rotation: a cTBS study.
        Cerebellum. 2013; 12: 856-861
        • Taylor HA
        • Brunyé TT
        • Taylor ST
        Spatial mental representation: implications for navigation system design.
        Rev Hum Factors Ergon. 2008; 4: 1-40
        • Moreau D
        • Mansy-Dannay A
        • Clerc J
        • Guerrien A
        Spatial ability and motor performance: assessing mental rotation processes in elite and novice athletes.
        Int J Sport Psychol. 2011; 42: 525-547
        • Guzman J
        • Hurwitz EL
        • Carroll LJ
        • et al.
        A new conceptual model of neck pain: linking onset, course, and care: the Bone and Joint Decade 2000-2010 Task Force on Neck Pain and Its Associated Disorders.
        J Manipulative Physiol Ther. 2009; 32: S17-S28
        • Von Korff M
        • Ormel J
        • Keefe FJ
        • Dworkin SF
        Grading the severity of chronic pain.
        Pain. 1992; 50: 133-149
        • Oldfield RC
        The assessment and analysis of handedness: the Edinburgh inventory.
        Neuropsychologia. 1971; 9: 97-113
        • Cohen W
        • Polich J
        No hemispheric differences for mental rotation of letters or polygons.
        Bull Psychon Soc. 1989; 27: 25-28
        • Shepard RN
        • Metzler J
        Mental rotation of three-dimensional objects.
        Science. 1971; 171: 701-703
        • Shadmehr R
        • Smith MA
        • Krakauer JW
        Error correction, sensory prediction, and adaptation in motor control.
        Annu Rev Neurosci. 2010; 33: 89-108
        • Hewitt AL
        • Popa LS
        • Pasalar S
        • Hendrix CM
        • Ebner TJ
        Representation of limb kinematics in Purkinje cell simple spike discharge is conserved across multiple tasks.
        J Neurophysiol. 2011; 106: 2232-2247
        • Paulus I
        • Brumagne S
        Altered interpretation of neck proprioceptive signals in persons with subclinical recurrent neck pain.
        J Rehabil Med. 2008; 40: 426-432
        • Kristjansson E
        • Dall'Alba P
        • Jull G
        A study of five cervicocephalic relocation tests in three different subject groups.
        Clin Rehabil. 2003; 17: 768-774
        • Guerraz M
        • Caudron S
        • Thomassin N
        • Blouin J
        Influence of head orientation on visually and memory-guided arm movements.
        Acta Psychol. 2011; 136: 390-398
        • Harvie DS
        • Broecker M
        • Smith RT
        • Meulders A
        • Madden VJ
        • Moseley GL
        Bogus visual feedback alters onset of movement-evoked pain in people with neck pain.
        Psychol Sci. 2015; 26: 385-392