Date Published: June 29, 2018
Publisher: Public Library of Science
Author(s): Wim Saeys, Nolan Herssens, Stijn Verwulgen, Steven Truijen, Stefan Glasauer.
Perception of verticality is highly related to balance control in human. Head-on-body tilt <60° results in the E-effect, meaning that a tilt of the perceived vertical is observed contralateral to the head tilt in the frontal plane. Furthermore, somatosensory loss also impacts the accuracy of verticality perception. However, when several input sources are absent or biased, less options for sensory weighting and balance control occur. Therefore, this study aims to identify the E-effect and assess the effect of somatosensory loss on the extent of the E-effect. All patients with a first stroke admitted to a Belgian rehabilitation hospital were eligible for inclusion. Patients aged above 80 with other neurological and orthopaedic impairments as well as brainstem, cerebellar or multiple lesions were excluded. In addition, patients with visuospatial neglect and pusher behaviour were also excluded as this can affect verticality perception. The Rivermead Assessment of Somatosensory Performance (RASP), the Subjective Visual (SVV) and Subjective Postural (SPV) Vertical Test were administered. In total, 37 patients were included in the analysis of which 24 patients completed both SVV and SPV assessment. Results show that the E-effect occurred in our sample of stroke survivors for both SVV and SPV. In addition, the presence of somatosensory loss will increase the E-effect in both SVV as SPV assessment. A significant difference in verticality perception was noted for both SVV and SPV between the group with no (SVV: 5.13°(6.92); SPV: 0.30°(1.85)) and highly severe (SVV: 10.54°(13.19); SPV: 5.96°(9.27)) sensory loss. The E-effect occurs in stroke subjects and increases when patients experience somatosensory loss. This suggests that the lack of available afferent information impede estimation of verticality. Therefore, stroke survivors have fewer alternative input sources as a result of impairments, leading to fewer options about sensory reweighting strategies and balance recovery after perturbations.
Postural control emerges from the interaction between the task, the environment and the individual. Within the individual, an efficient interaction between motor, sensory and neural systems is needed in order to maintain postural control. One of the neural processes is the integration of afferent information such as visual, vestibular (otolith organs and semicircular canals) and somatosensory (muscle and joint proprioceptors, skin pressure sensors, truncal somatosensors in the kidneys, mechanoreceptors in large vessels) input to enhance self-orientation in the gravitational space. Humans should be able to align their body vertically with the gravitational vector to ensure axial extension of the body, keeping the centre of pressure within the base of support. To orientate the whole body in space, different reference frames are constructed based on several input sources from head and trunk. Dissociating head- and trunk-based reference frames and their specific sensory input sources to estimate the direction of gravity, underlines the eminent role of the vestibular organs in sensing gravity.[3, 4] However, this does not suggest that internal verticality is solely based on sensory systems in the head. Clearly, verticality perception remains the result of a multisensory integration of various sensory input signals within parietotemporal cortical areas [5–7] and relevant contributions by somatosensory sensors in the neck and trunk (e.g., truncal somatosensors, skin pressure sensors, muscle and joint proprioceptors, and kidney graviceptors) have been reported.[8–13]
The Difra Vertitest type D107201 (Difra, Welkenraedt, Belgium) was used for SVV assessment. The device has an accuracy of 0.1°. A laser bar was projected vertically at a distance of 2.5m on an opposing wall with the center of rotation of the laser bar on an altitude of 1.5m. The device was calibrated in this position, approximating the average altitude of the participants’ eyeline when seated. The patients are seated in front of the device on a fixed chair without any arm- or backrests. The room was darkened and five minutes of waiting period was given allowing the subject to adjust the darkness. Both researcher and participant obtained a remote control to allow rotating the laser bar either clockwise (right) or counter clockwise (left). The researcher’s remote control showed a display with the amount of deviation in relation to the earth’s gravitational vector. The researcher made the laser bar invisible and rotated it in a specific angle in relation to the earth vertical. Subsequently, the line was shown after which the patient had to place the line in upright position again with his nonhemiplegic hand on the remote control. The amount of deviation of each starting roll position was different for each trial. A specified order was followed: first the line was placed in 20° counter clockwise, 10° clockwise, 5° counter clockwise and 0° according to the earth vertical, followed by 5° clockwise, 10° counter clockwise and finally 20° clockwise. This series was executed three times. During the first series the patient was asked to hold the head in normal upright position, followed by a series with the head actively tilted to the left as far as possible (while the head was tilted the subjects needed to keep their trunk upright) and finally a series with the head actively tilted to the right side as far as possible. The clockwise rotation is represented by a positive number and the counter clockwise rotation as a negative number. Head-on-body tilt was tactilely controlled by the researcher to decrease variability in head-on-body tilts and neck proprioceptive information. All patients had a ROM of the head in relation to the sternum between 35 and 45°.
The rotation chair works on hydraulic pumps and has a height of 1m. On the back of the chair, a Mitutoyo digital protractor pro 3600 (Belgium) was mounted. This allowed measurement of the deviation in relation to the earth vertical with an accuracy of 0.01°. Both the researcher and patient were given a remote to rotate the chair clockwise (right) and counter clockwise (left). Movements were restricted in the frontal plane. Before the assessment started the patient was blindfolded, depriving the subjects of visual information when readjusting the chair to earth vertical. The researcher rotated the chair as in the procedure of SVV (starting roll position of the chair). The head-on-body position is similar as in the SVV procedure. The subject had to place the chair in upright position again by placing the seating surface of the chair horizontal. The patient used his non-hemiplegic hand on the remote control. The clockwise rotation is shown positively and the counter clockwise rotation negatively.
Statistical Package for Social Sciences, SPSS 22 (SPSS inc, Chicago, IL) for windows was used for statistical analysis.
Thirty-seven patients (22 men and 15 women), with a mean age of 62.43 (± 13.26) years, were included. Time from stroke onset ranged from 8 till 85 days with a mean of 38.05 (± 21.17) days post-stroke. Fifteen patients had a left-hemisphere lesion and twenty-two patients a right-hemisphere lesion. There were no patients with bilateral lesions. Descriptives of each individual, all patients combined and of each group based on sensory loss severity are shown in Tables 1 and 2. Out of the thirty-seven patients, three patients were unable to complete the SVV test-protocol and ten patients were unable to complete the SPV test-protocol due to safety issues or fear of falling. Twenty-four subjects completed both protocols (SVV and SPV).
In this study we explored verticality perception and sensory reweighting strategies in stroke subjects. At first, the E-effect occurred in our stroke subjects in general, which means that a contralateral deviation of SVV and SPV is seen when the head is tilted in the roll plane. Secondly, an effect of somatosensory loss on the extent of the E-effect can be observed. This means that a lower RASP score in combination with a tilted head-on-body position is related to a larger deviation of perceived verticality opposite to the head-on-body tilt in both the SVV and SPV. In the SPV measurements, group 0 and 1 can realign their body very accurately with a mean around the midline.
Sensory weighting is crucial for postural control and is necessary to pretune the body and adapt to different tasks and environmental demands. However, in stroke survivors afferent information can be absent, impaired or inadequately processed. Especially the integration of afferent information is challenging for most patients as seen in visuospatial neglect and the pusher syndrome . As a result, patients will rather rely on one specific input source and therefore lose the ability to switch between sensory strategies to keep balance. As often seen in rehabilitation, patients will use primarily visual information to provide orientation of the body in space as a compensatory mechanism for the inability to up- or deweight sensory information.
The E-effect in verticality perception is present in stroke survivors and is negatively influenced by somatosensory loss. When impairments occur as a result of brain damage, especially on the sensory input and processing level, fewer alternatives are available to pretune and adapt the body to postural perturbations. Clinical rehabilitation should also focus on sensory retraining strategies combined with cognitive rehabilitation to increase balance recovery after stroke.