- Email: [email protected]
The peripheral nervous system and the perception of verticality
Gait & Posture 27 (2008) 202–208 www.elsevier.com/locate/gaitpost
The peripheral nervous system and the perception of verticality G. Mazibrada a,*, S. Tariq b, D. Pe´rennou c, M. Gresty c, R. Greenwood b,e, A.M. Bronstein d a
Sobell Department of Neurophysiology, Institute of Neurology, Queen Square, London, UK b Regional Neurological Rehabilitation Unit, Homerton University Hospital, London, UK c Service de Re´e´ducation Neurologique, CHU 23, rue Gaffarel BP 77908, Dijon cedex, France d Academic Department of Neuro-otology, Division of Neuroscience, Imperial College London, Charing Cross Hospital, London, UK e Acute Brain Injury Unit, The National Hospital for Neurology and Neurosurgery, Queen Square, London, UK Received 26 July 2005; received in revised form 14 March 2007; accepted 19 March 2007
Abstract Orientation of the body with respect to gravity is based on integration of visual, vestibular and somatosensory signals. Here, we investigated the subjective postural vertical (SPV) and visual vertical (SVV) in three patients with bilateral somatosensory deafferentation and a group of age-matched normal subjects. Our hypothesis was that the patients with bilateral somatosensory deafferentation may show tilt induced bias in the construction of their SPV, with a normal SVV. Patient 1 had a severe Guillain Barre´ syndrome and almost complete absence of peripheral sensation, the two other patients had a thoracic spinal injury with a sensory loss from T6-7 down. On initial testing, compared with normal subjects and the patients with spinal injury, Patient 1 had a significant bias in SPV towards the side of a preceding tilt in both directions. Several months later, after significant improvement of sensation, this tilt-induced bias in SPV had resolved completely. In addition, Patient 1 had a significantly enlarged ‘‘cone of verticality’’, which did not change following improvement in peripheral sensation, reflecting persisting disturbance in the perception of body verticality. In the two patients with spinal injury, bias towards the side of a preceding tilt was not significant. These findings confirm the importance of somatosensory input from the trunk to the perception of SPV in the seated position. # 2007 Elsevier B.V. All rights reserved. Keywords: Subjective postural vertical; Subjective visual vertical; Somatosensory input; Guillain Barre´ syndrome
1. Introduction Spatial orientation in relation to gravity is crucial for the maintenance of upright posture, gait and most motor activities. Three different sensory systems regulate these complex behaviours, the vestibular, the visual and the somatosensory systems [1]. The afferent information is then integrated and processed, at both brain stem and hemispheric level [2]. Damage to the central integrating system or disturbance of the central or peripheral vestibular system, can lead to abnormal perception of the body’s orientation in space, and abnormal perception of various modalities of the vertical [3–5]. Patients after hemispheric stroke, for * Corresponding author at: Queen Elizabeth Hospital, Edgbaston, Birmingham B15 2TH, UK. Tel.: +44 7867697958. E-mail address: [email protected] (G. Mazibrada). 0966-6362/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2007.03.006
example, can have a bias in the behavioural postural vertical towards the affected contralesional side [3,4], a contralesional bias of the subjective postural vertical (SPV) [7], and a bias of the subjective visual vertical (SVV) [5,6], with a possible dissociation between these modalities [8,9]. By contrast, patients with a brain stem lesion can have a large ipsilesional bias in SVV [10] but preserved perception of somatosensory (haptic) verticality [11]. Similarly, patients with a peripheral vestibular lesion [12] show an ipsilesional bias in SVV without a bias in SPV. Although there is a consensus that somatosensory input plays a major role in the formation of SPV and body verticality, it is not yet clear how a peripheral disturbance of somatosensory signals affects the perception of the postural vertical. Anastasopoulos et al. [7] analysed patients with hypoesthesia in whom the deafferentation was not complete. They reported a 4–58 bias in SPV towards the side of the
G. Mazibrada et al. / Gait & Posture 27 (2008) 202–208
sensory loss in two patients with moderate to severe hemihypoesthesia caused by hemispheric lesions. However, they did not find a significant bias in patients with spinal ischemia or polyneuropathy. In addition to the existence of a bias, some patients can show a large cone of verticality reflecting an uncertainty in the construction of their subjective vertical. This has been mainly shown in avestibular patients [12]. In contrast, the subjective postural and visual vertical of patients with bilateral somaesthetic deafferentation has only occasionally been investigated [13,23]. The aim of this study was to assess and compare the subjective postural and visual vertical in patients with a somaesthetic deafferentation of the limbs and trunk. The first patient, Patient 1, with severe Guillain Barre´ syndrome initially had almost complete bilateral sensory loss below the neck; two other patients had thoracic spinal cord injuries with severe sensory disturbance below the level of the lesion. Their results were compared with a group of normal subjects. 2. Methods SPV and SVV were assessed in normal subjects, Patient 1 with Guillain Barre´ syndrome, and two other patients (Patients 2 and 3), with a thoracic spinal injury. Motor weakness and sensory function were assessed using standardised assessment scales (see below). All subjects gave their informed consent to the study according to the guidelines of the local ethics committee. 2.1. Normal subjects Twenty normal subjects (12 males, 8 females), age 22–72 years (42, S.D. 13) participated in the study. None of the subjects had a history of stroke, peripheral vestibular disorder or any other disorder affecting the central or peripheral nervous system. The SPV and SVV results from our group of normal patients have not been reported before. 2.2. Patients Patient 1 was a 44-year-old male with a severe Guillain Barre´ syndrome. Clinical examination 8 months after onset of the illness revealed a severe bilateral facial weakness and flaccid quadriparesis with inability to lift the arms or legs against gravity, superficial sensory loss from the neck down and a Barthel Index of 4 (Table 1). Electromyography (EMG) performed 1 month after the onset of the illness showed absent radial sensory action potentials and no recordable response to stimulation in the arms or legs. Repeated testing 8 months after the onset of the illness showed a small response following ulnar nerve stimulation and active reinnervation of the proximal and distal arm and leg muscles (clinical recovery is described in Table 1). Patients 2 and 3, both males aged 29, were assessed 6 and 9 months after a spinal cord injury. Patient 2 had a traumatic spinal cord injury resulting in complete sensory loss below the level of T7. Patient 3 had spinal tuberculosis resulting in an incomplete sensory loss bellow the level of T6.
203
3. Assessments 3.1. Sensory–motor examination The severity of motor weakness was recorded using the Motricity index [14], a brief assessment scale of motor function of arm, leg and trunk. Somatosensory function was assessed by subtests of the Rivermead Somatosensory test (RST) [15]. This included pinprick sensation assessing small myelinated sensory fibres and light touch, deep pressure and joint position (proprioception) sensation assessing large myelinated sensory fibres. The maximum RST score is 300. Bilateral caloric vestibular stimulation was also performed. Finally, overall functional independence was assessed using the modified Barthel Index. 3.2. Subjective postural vertical The assessment was carried out in a darkened room with the subjects’ eyes covered. They were seated on a chair mounted in a cylindrical frame with head, shoulders, hips and legs restrained and feet supported. The frame was slowly rolled manually by the examiners at less than 1.58 s 1, a velocity which does not provoke significant semicircular canal stimulation [16]. Immediately after a random offset in the roll (coronal) plane from the starting position to the left or right side, the subject was rolled back at the same speed (less than 1.58 s 1) towards the vertical position. This avoided adaptation to a tilted posture [17,18]. The subject’s task was to indicate as soon as s/he started to feel upright. This position was recorded as an entry point into the ‘‘cone of verticality’’, as defined by Bisdorff et al. [12]. The motion was then continued in the same direction and the subject was asked to indicate as soon as s/he started to feel tilted again which was recorded as an exit point from the ‘‘cone of verticality’’. The rotation was interrupted both when the patient felt ‘‘vertical’’ or ‘‘tilted’’ to allow minor adjustment to the left or right. This paradigm determined the SPV and the ‘‘cone of verticality’’ during motion from left to right and right to left, and is illustrated in Fig. 1. Ten tilts to the left and 10 tilts to the right were executed with a different angle of inclination (tilt) varying from a maximum of 508 (left) to 508 (right). The axis of rotation was at mid-abdominal level. The angle of inclination away from gravitational vertical was measured by an inclinometer attached to the back of the tilting frame. Patient 1 was tested three times initially (Test 1) and three times after 7 months (Test 2). The patients with spinal injury were assessed twice initially (Test 1), and twice after 2 months (Test 2). Patients were tested two or three times in each session to ensure test–retest reliability and results were averaged. 3.3. Subjective visual vertical A luminous line (15 cm long) was displayed on a computer screen 1.2 m away from the subject, at eye level, in
204
G. Mazibrada et al. / Gait & Posture 27 (2008) 202–208
deviation) for the 10 trials. For the control group (n = 20), the average value as well as the intersubject standard deviation were calculated in order to express the data of each patient as Z-scores and analyse his/her individual results with respect to normality ranges. A Z-score above 2 by definition means an abnormality with the alpha risk of 0.05. A non-parametric (Mann–Whitney) test was used to compare SPV orientation, uncertainty and ‘‘size of the cone’’ between the leftwards and rightwards trials in normal subjects and patients. The normal range for the cone of verticality and cone size of SPV and SVV orientation were defined as normal subjects group mean 2S.D. measurement error. Measurement error for the SPV was estimated at 0.58 as the inclinometer scale measured a minimum difference of 18. Measurement error for the SVV was 0.28, the accuracy corresponding to the step of the angular displacement of the luminous line. Throughout the manuscript data are given as mean standard deviation.
5. Results 5.1. Normal subjects 5.1.1. Subjective postural vertical Fig. 1. Diagram illustrating the SPV measurements obtained during the right to left tilt cycle.
a completely dark room. The luminous line was randomly deviated to the right or left and the subject asked to set the line ‘‘vertical to the earth’’ whilst seated upright in the circular frame. The line was moved with the left/right arrow on a computer keyboard by the examiner on instruction by the subject. A computer measured the angle of inclination away from the earth vertical. Ten adjustments were performed. SVV in the patients was tested once only during Test 1.
The mean SPV orientation was 0.4 0.88 that gave a normality range from 2.58 to 1.78. The mean and the standard deviation of the uncertainty across the normal subjects was 1.8 0.48. For leftwards trials, the mean orientation was 1.4 1.08 that gave normality range from 3.98 to 1.18 and the uncertainty was 1.7 0.58. For the rightwards trials, the mean orientation was 0.6 1.58 that gave a normality range from 2.98 to 4.18 and the uncertainty was 1.8 0.58. The mean size of the cone of verticality was 3.1 1.18when the 10 trials per subject were considered, 3.2 1.38 for the leftwards trials and 3.0 1.18 for the rightwards trials. Normal range for the orientation of the cone of verticality was 5.88 for all trials; 6.38 for the leftwards and 5.78 for the rightwards trials. Mann–Whitney testing between left and right trials showed no significant difference in orientation ( p = 0.4), size of cones of verticality ( p = 0.8), or uncertainty ( p = 0.6).
5.2. Subjective visual vertical 4. Data analysis SPV data in normal subjects and patients were expressed as: (1) orientation of the cone of verticality, defined as the mean of the entry and the exit point of the cone of verticality for each of the 10 trials performed in each subject, SPV orientation was also measured from right to left and left to right motion separately (2) uncertainty, defined as the dispersion (standard deviation) of the 10 orientation values and (3) size of the cone of verticality, defined as the mean angular sector between the entry and exit points of the cone of verticality. These three variables were expressed in degrees. SVV data were expressed as orientation, defined as the mean of the 10 trials performed in each subject and uncertainty, defined as the data dispersion (standard
SVV orientation was 0.1 1.08 (normality range from 2.18 to 2.28) and uncertainty was 0.3 1.08.
6. Patients 6.1. Clinical sensory–motor examination Patient 1 was assessed 8 months after the onset of the illness and after a further 7 months when his neurological condition had significantly improved. The first and second clinical assessments are summarised in Table 1. In both assessments, bilateral cold-water (4 8C) caloric vestibular stimulation produced a normal response.
G. Mazibrada et al. / Gait & Posture 27 (2008) 202–208
205
Table 1 Patient 1, 1st and 2nd clinical assessment 1st assessment
2nd assessment
Motricity index Arm Leg Side
Left 53 34 43.5
Proprioception
Normal bilaterally at the elbows and wrists Absent bilaterally at the thumbs, fingers, ankles and toes
Normal bilaterally apart from toes –
Rivermead Somatosensory test (max = 300)
Minimal sensation to pin prick in the left and right hand, otherwise no superficial sensation in the trunk and limbs Total score 22
Normal sensation in the trunk. Superficial sensation in the limbs improved in all modalities apart from two point discrimination No sensation below the knees Total score 130
Barthel score (max = 20) Mobility
4 Hoist required for transfers
18 Able to walk with a Zimmer frame
Patient 2 had a complete sensory loss below the level of T7. His motricity scores were normal in the arms (100/100); in the legs the score was 73/100, giving a total score of 86.5/ 100 bilaterally. Patient 3 had an incomplete sensory loss bellow the level of T6. Surface pressure touch was moderately impaired on the left and severely on the right side. Proprioception was normal in the left ankle and decreased in the right ankle. Motricity scores were normal in the arms (100/100); the left leg score was 58/100, the right leg score was 53/100 giving a total score of 79/100 left and 76.5/100 right. Clinical examination of patients 2 and 3 was the same at both time points. Both patients had a normal response to bilateral cold-water caloric vestibular stimulation. 6.2. Subjective postural vertical
Right 43 39 41.5
Left 81 67 79
Right 81 67 79
Orientation for the leftwards and rightwards trials, Z-scores were 5.1 and 4.9, respectively. Z-scores for the size of the cone including cone size for the leftwards and rightwards trials were 4.5, 3.8 and 4.4, respectively. Z-scores for mean orientation, including orientation for leftwards and rightwards trials of SPV in Patients 2 and 3 were within the normal range (0.3–1.3). The cone size for leftwards trials in Patient 2 was just outside the normal range, the cone size for the leftwards and rightwards trials together was at the upper limit of normal. Z-scores for cone size were 2.5, 2.7 for leftwards trials and 2 for the rightwards trials. The cone size in Patient 3 was within the normal range with Z-scores for the cone size, leftwards and rightwards trials ranging from 0.1 to 0.8. Non-parametric (Mann–Whitney) comparison between the left to right and right to left sided trials in orientation (absolute values), uncertainty and size of the cone showed no significant differences in Patient 1 ( p = 0.7, 0.2 and 0.1, respectively), Patient 2 ( p = 0.06, 0.1 and 0.5, respectively) and Patient 3 ( p = 0.2, 0.1 and 0.1 respectively).
6.2.1. Test 1 SPV orientation estimation from the left and right as well as leftwards and rightwards cone size were all outside the normal range in Patient 1. Patient 1 Z-score for mean orientation was 0.8.
6.2.2. Test 2 The SPV orientation, uncertainty and cone size in normal subjects and patients in Tests 1 and 2 are shown in Table 2.
Table 2 Test 1 and Test 2, SPV orientation, uncertainty and cone size in patients and normal subjects (abnormal values in bold type) SPV orientation/ uncertainty left to right trials Normals
SPV orientation/ uncertainty right to left trials
SPV orientation/ uncertainty left + right trials 0.48/1.8
SPV cone size/ S.D. leftwards trials
SPV cone size/ S.D. rightwards trials
SPV cone size/ S.D. left + right trials
3.28/1.38
38/1.18
3.18/1.18
1.48/1.78
0.68/1.88
Test 1 Patient 1 Patient 2 Patient 3
S6.5-/4.11.18/2.48 2.28/2.48
7.9-/2.63.38/2.48 3.48/2.58
18/3.38 1.48/3.68 0.68/3.78
8.2-/1.48 6.3-/2.18 48/0.78
7.8-/0.68 58/1.58 3.18/1.28
8-/0.68 5.8-/1.98 3.68/1.18
Test 2 Patient 1 Patient 2 Patient 3
0.38/28 0.28/1.48 1.78/1.48
1.98/2.98 38/2.38 1.28/28
18/2.58 1.68/2.98 0.38/2.38
8.2-/0.48 4.88/1.48 3.28/2.18
7.2-/0.28 4.78/1.78 3.58/28
7.7-/0.28 4.88/1.58 3.48/28
206
G. Mazibrada et al. / Gait & Posture 27 (2008) 202–208
SPV orientation estimation from the left and right as well as leftwards and rightwards cone size were all within the normal range in Patients 2 and 3. Cone size, including the cone size for the leftwards and rightwards trials remained abnormal in Patient 1 with Z-scores 4.2, 4.3 and 4.2, respectively. In Patient 1, non-parametric (Mann–Whitney) comparison between orientation (absolute values), uncertainty and size of the cone for the left to right and right to left sided trials did not show significant differences ( p = 0.5, 0.1 and 0.2, respectively). Similarly, comparison of SPV orientation, uncertainty and cone size between Tests 1 and 2 in Patient 1 showed that the mean SPV orientation was not different ( p = 1.0), but orientation for the left to right and right to left sided trials was significantly different ( p = 0.002 and 0.001, respectively). Uncertainty, including uncertainty for the leftwards and rightwards trials, and cone size, including cone size for the leftwards and rightwards trials, were not significantly different ( p = 0.1, 0.6 and 0.3, and p = 1.0, 0.1 and 0.4, respectively). For Patient 1, repeated assessments within testing session 1 and within testing session 2 were not statistically different. This shows good test–retest reliability.
Fig. 2. Patient 1(A) SPV orientation in trials from left to right. (B) SPV orientation in trials from right to left. Results at 8 months (Test 1) and 15 months (Test 2) after illness onset are shown.
Patient 1 change in SPV orientation in Test 1 and Test 2 for the left to right and right to left sided trials are visually summarized in Fig. 2.
6.3. Subjective visual vertical All measures of SVV were within the normal range. SVV orientation in Patient 1 was 1.1 1.08 with an uncertainty of 1.0 0.58, in Patient 2 0.5 0.88 with uncertainty of 1.5 0.58 and in Patient 3 1.5 1.38 with an uncertainty of 1.5 0.68.
7. Discussion Normal subjects have an accurate orientation of postural vertical with a small, symmetrical cone of verticality. They also had a minimal tilt-induced directional bias in SPV orientation, represented by a slight influence of the preceding tilt on the perception of SPV. These findings are comparable with the results reported by Bisdorff et al. [12]. The size of the cone of SPV, that is the width of the sector in which our normal subjects felt vertical, was smaller than the one described by the Bisdorff et al. [12]. This could be because rotation from left to right and right to left was continuous in the study by Bisdorff et al. [12], while in our study the rotation was interrupted when the patient felt ‘‘vertical’’ or ‘‘tilted’’ to allow minor adjustments either to the left or to the right. Patient 1 with Guillain Barre´ syndrome changed in some, but not all, of his SPV measures across time, a dissociation that could be explained by changes in his recovery from peripheral somatosensory loss across time. His initial SPV orientation for the left to right and right to left tilts showed a significant directional bias, a tendency to perceive the body being vertical towards the side of the preceding tilt. This directional bias was much larger than the physiological bias found in our normal subjects, 6.58 versus 1.48 for the leftwards trials and 7.98 versus 0.68 for the rightwards trials, with Z-scores of 4.8 and 4.7, well outside the normal range defined as mean 2S.D. measurement error. As expected from the sensory examination, which showed symmetrical loss of sensation in the trunk and limbs, there was no significant asymmetry between the left to right and right to left sided trials. At Test 2, when sensation had recovered significantly in the trunk and limbs, there was a normalisation of the SPV orientation in rightwards (1.98) and leftwards ( 0.38) trials. By contrast increase in size of the ‘‘cone of verticality’’ and abnormal Z-scores in both directions of tilt shown at Test 1 remained during Test 2 despite the improvement of directional bias in SPV orientation. This dissociation could be explained by incomplete recovery of peripheral somatosensory information. The Guillain-Barre´ syndrome principally affects the myelin sheaths and, in severe cases, axons of larger diameter spinal roots and peripheral nerves. In a significant number of
G. Mazibrada et al. / Gait & Posture 27 (2008) 202–208
cases, it also affects sympathetic and parasympathetic autonomic nerves, and small fibre sensory nerves [19]. The significant directional bias, the loss of sensitivity in SPV orientation and the increased size of the ‘‘cone of verticality’’ in both directions of tilt in our patient with Guillain-Barre´ syndrome must therefore be the result of abnormal peripheral somatosensory input caused by widespread, severe damage to the peripheral nerves and spinal roots. Results from the two spinal patients suggest that afferent input from the lower limbs is relatively unimportant to the perception of verticality in the seated position. In both spinal patients, the mean SPV orientation and uncertainty in the leftwards and rightwards trials were similar and within the normal range. In Patient 2, who had more profound sensory loss, the size of the ‘‘cone of verticality’’ was at the upper limit of normal with a Z-score of 2.5, possibly caused by impaired sensory input from the lower trunk. These results confirm the importance of peripheral somatosensory signals from the trunk in the perception of subjective postural vertical and vertical orientation of the body. Our data were obtained in the seated position where contact/pressure from trunk and shoulders was of prime importance. Presumably, inputs from the lower limbs are critical for orientation in the standing position, but patient data in this position are lacking. The findings are in line with previous studies, suggesting a role for peripheral somatosensory signals in postural orientation of the body. Brown [20] and Nelson [21] reported that reduction in proprioceptive cues by whole body immersion in water significantly impairs estimates of uprightness. Do et al. [22] found that the early motor responses contributing to recovery of balance possibly originate from receptors located at the abdominal or lumbar level and not from vestibular cues or leg proprioceptors. Bisdorff et al. [12] suggested that the perception of body verticality in seating is mainly dependent on proprioceptive and contact cues. In addition, Mittelsteadt et al. [23] suggested that gravity receptors in the trunk provide somatosensory graviceptive signals responsible for the perception of posture and body verticality. Furthermore, based on experiments on healthy subjects laying horizontally in a centrifuge with a vertical rotation axis Mittelsteadt [24] suggested the existence of at least two separate graviceptive inputs from the trunk, one entering the spinal cord at the level of the 11th thoracic dorsal root and another delivering the information to the brain presumably via the vagus or phrenic nerve. Our spinal patients perceived verticality normally without a significant directional bias in SPV orientation. Patient with a complete sensory level at T7 only had a borderline increase in size of the ‘‘cone of verticality’’ in the first test in comparison to normal subjects. It seems likely that our spinal patients had no directional bias in SPV orientation because there was a significant sensory input in a constrained sitting position from the upper trunk and shoulders. Sensory input from these areas was significantly impaired in Patient 1 during Test 1, in the
207
absence of any clinical evidence of autonomic involvement. Whilst these results confirm the importance of somatosensory input from the trunk and/or shoulders to the perception of verticality, what sensory modalities convey this information remains unclear. In addition to confirming the importance of somatosensory input from the trunk to the perception of verticality, we showed that the perception of SVV, tested in the upright position, was normal in all three patients. It is questionable whether SVV tested in such a way can predict the effect of somatosensory loss on visual verticality and its relation to the loss of sensitivity found in SPV. Testing SVV just inside and outside the patients’ cone of verticality and comparing it to the healthy subjects taking into account the standard Aand E-effects would perhaps help determine how somatosensory deficit affects visual verticality. Future studies assessing this would be helpful.
Acknowledgements The authors acknowledge 1. The Physiotherapy Department, The Regional Neurological Rehabilitation Unit, Homerton University Hospital. 2. Hilary Watt, statistician at The National Hospital for Neurology and Neurosurgery.
References [1] Anastasopoulos D, Bronstein AM. A case of thalamic syndrome: somatosensory influences on visual orientation. J Neurol Neurosurg Psychiatry 1999;67:390–4. [2] Mergner T, Huber W, Becker W. Vestibular-neck interaction and transformation of sensory coordinates. J Vestib Res 1997;7(4): 347–67. [3] Pe´rennou DA, Amblard B, Leblond C, Pe´lissier J. Biased postural vertical in humans with hemispheric lesions. Neurosci Lett 1998;252:75–8. [4] Pe´rennou DA, Amblard B, Laassel EM, Benaim C, He´risson C, Pe´lissier J. Understanding the pusher behaviour of some stroke patients with spatial deficits: A pilot study. Arch Phys Med Rehabil 2002;83:570–5. [5] Brandt T, Dieterich M, Danek A. Vestibular cortex lesions affect the perception of verticality. Ann Neurol 1994;35:403–12. [6] Kerkhoff G, Zoelch C. Disorders of visuospatial orientation in the frontal plane in patients with visual neglect following right or left parietal lesions. Exp Brain Res 1998;122:108–20. [7] Anastasopoulos D, Bronstein A, Haslwanter T, Fetter M, Dichgans J. The role of somatosensory input for the perception of verticality. Ann N Y Acad Sci 1999;871:379–83. [8] Karnath HO, Ferber S, Dichangs J. The origin of contraversive pushing: evidence for a second gravioceptive system in humans. Neurology 2000;55(9):1298–304. [9] Pe´rennou D, Playford D, Guerraz M, Mazibrada G, Gresty M, Bronstein A. Dissociation in the verticality perception after a stroke. In: Kingma H, Duysens J, editors. Proceedings of the ISPG 2001. 2001. [10] Dieterich M, Brandt T. Ocular torsion and tilt of subjective visual vertical are sensitive brainstem signs. Ann Neurol 1993;33:292–9.
208
G. Mazibrada et al. / Gait & Posture 27 (2008) 202–208
[11] Bronstein AM, Pe´rennou DA, Guerraz M, Playford D, Rudge P. Dissociation of visual and haptic vertical in two patients with vestibular nuclear lesions. Neurology 2003;61:1260–2. [12] Bisdorff AR, Wolsley CJ, Anastasopoulos D, Bronstein AM, Gresty MA. The perception of body verticality (subjective postural vertical) in peripheral and central vestibular disorders. Brain 1996;119:1523– 34. [13] Paulus W, Straube A, Brandt TH. Visual postural performance after loss of somatosensory and vestibular function. J Neurol Neurosurg Psychiatry 1987;50:1542–5. [14] Collin C, Wade D. Assessing motor impairment after stroke: a pilot reliability study. J Neurol Neurosurg Psychiatry 1990;53: 576–9. [15] Winward CE, Halligan PW, Wade DT. Rivermead Assessment of Somatosensory Performance Manual. Thames Valley Test Company Limited; 2000. [16] Benson AJ, Brown SF. Visual display lowers detection threshold of angular, but not linear, whole-body motion stimuli. Aviat Space Environ Med 1989;60:629–33.
[17] Clark B, Graybiel A. Perception of the postural vertical following prolonged bodily tilt in normals and subjects with labyrinthine defects. Acta Otolaryngol 1964;58:143–8. [18] Riccio GE, Martin EJ, Stoffregen TA. The role of balance dynamics in the active perception of orientation. J Exp Psychol Hum Percept Perform 1992;18(3):624–44. [19] Zochodne DW. Autonomic involvement in Guillain-Barre syndrome: a review. Muscle Nerve 1994;17:1145–55. [20] Brown JL. Orientation to the vertical during water immersion. Aerospace Med 1961;32:209–17. [21] Nelson JG. Effect of water immersion and body position upon perception of the gravitational vertical. Aerosp Med 1968;39:806–11. [22] Do MC, Breniere Y, Bouisset S. Compensatory reactions in forward fall: are they initiated by stretch receptors? Electroencephalogr Clin Neurophysiol 1988;69(5):448–52. [23] Mittelsteadt H, Fricke E. The relative effect of saccular and somatosensory information on spatial perception and control. Adv OtoRhino-Laryng 1988;42:24–30. [24] Mittelsteadt H. Somatic graviception. Biol Physiol 1996;42:53–74.
The peripheral nervous system and the perception of verticality G. Mazibrada a,*, S. Tariq b, D. Pe´rennou c, M. Gresty c, R. Greenwood b,e, A.M. Bronstein d a
Sobell Department of Neurophysiology, Institute of Neurology, Queen Square, London, UK b Regional Neurological Rehabilitation Unit, Homerton University Hospital, London, UK c Service de Re´e´ducation Neurologique, CHU 23, rue Gaffarel BP 77908, Dijon cedex, France d Academic Department of Neuro-otology, Division of Neuroscience, Imperial College London, Charing Cross Hospital, London, UK e Acute Brain Injury Unit, The National Hospital for Neurology and Neurosurgery, Queen Square, London, UK Received 26 July 2005; received in revised form 14 March 2007; accepted 19 March 2007
Abstract Orientation of the body with respect to gravity is based on integration of visual, vestibular and somatosensory signals. Here, we investigated the subjective postural vertical (SPV) and visual vertical (SVV) in three patients with bilateral somatosensory deafferentation and a group of age-matched normal subjects. Our hypothesis was that the patients with bilateral somatosensory deafferentation may show tilt induced bias in the construction of their SPV, with a normal SVV. Patient 1 had a severe Guillain Barre´ syndrome and almost complete absence of peripheral sensation, the two other patients had a thoracic spinal injury with a sensory loss from T6-7 down. On initial testing, compared with normal subjects and the patients with spinal injury, Patient 1 had a significant bias in SPV towards the side of a preceding tilt in both directions. Several months later, after significant improvement of sensation, this tilt-induced bias in SPV had resolved completely. In addition, Patient 1 had a significantly enlarged ‘‘cone of verticality’’, which did not change following improvement in peripheral sensation, reflecting persisting disturbance in the perception of body verticality. In the two patients with spinal injury, bias towards the side of a preceding tilt was not significant. These findings confirm the importance of somatosensory input from the trunk to the perception of SPV in the seated position. # 2007 Elsevier B.V. All rights reserved. Keywords: Subjective postural vertical; Subjective visual vertical; Somatosensory input; Guillain Barre´ syndrome
1. Introduction Spatial orientation in relation to gravity is crucial for the maintenance of upright posture, gait and most motor activities. Three different sensory systems regulate these complex behaviours, the vestibular, the visual and the somatosensory systems [1]. The afferent information is then integrated and processed, at both brain stem and hemispheric level [2]. Damage to the central integrating system or disturbance of the central or peripheral vestibular system, can lead to abnormal perception of the body’s orientation in space, and abnormal perception of various modalities of the vertical [3–5]. Patients after hemispheric stroke, for * Corresponding author at: Queen Elizabeth Hospital, Edgbaston, Birmingham B15 2TH, UK. Tel.: +44 7867697958. E-mail address: [email protected] (G. Mazibrada). 0966-6362/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.gaitpost.2007.03.006
example, can have a bias in the behavioural postural vertical towards the affected contralesional side [3,4], a contralesional bias of the subjective postural vertical (SPV) [7], and a bias of the subjective visual vertical (SVV) [5,6], with a possible dissociation between these modalities [8,9]. By contrast, patients with a brain stem lesion can have a large ipsilesional bias in SVV [10] but preserved perception of somatosensory (haptic) verticality [11]. Similarly, patients with a peripheral vestibular lesion [12] show an ipsilesional bias in SVV without a bias in SPV. Although there is a consensus that somatosensory input plays a major role in the formation of SPV and body verticality, it is not yet clear how a peripheral disturbance of somatosensory signals affects the perception of the postural vertical. Anastasopoulos et al. [7] analysed patients with hypoesthesia in whom the deafferentation was not complete. They reported a 4–58 bias in SPV towards the side of the
G. Mazibrada et al. / Gait & Posture 27 (2008) 202–208
sensory loss in two patients with moderate to severe hemihypoesthesia caused by hemispheric lesions. However, they did not find a significant bias in patients with spinal ischemia or polyneuropathy. In addition to the existence of a bias, some patients can show a large cone of verticality reflecting an uncertainty in the construction of their subjective vertical. This has been mainly shown in avestibular patients [12]. In contrast, the subjective postural and visual vertical of patients with bilateral somaesthetic deafferentation has only occasionally been investigated [13,23]. The aim of this study was to assess and compare the subjective postural and visual vertical in patients with a somaesthetic deafferentation of the limbs and trunk. The first patient, Patient 1, with severe Guillain Barre´ syndrome initially had almost complete bilateral sensory loss below the neck; two other patients had thoracic spinal cord injuries with severe sensory disturbance below the level of the lesion. Their results were compared with a group of normal subjects. 2. Methods SPV and SVV were assessed in normal subjects, Patient 1 with Guillain Barre´ syndrome, and two other patients (Patients 2 and 3), with a thoracic spinal injury. Motor weakness and sensory function were assessed using standardised assessment scales (see below). All subjects gave their informed consent to the study according to the guidelines of the local ethics committee. 2.1. Normal subjects Twenty normal subjects (12 males, 8 females), age 22–72 years (42, S.D. 13) participated in the study. None of the subjects had a history of stroke, peripheral vestibular disorder or any other disorder affecting the central or peripheral nervous system. The SPV and SVV results from our group of normal patients have not been reported before. 2.2. Patients Patient 1 was a 44-year-old male with a severe Guillain Barre´ syndrome. Clinical examination 8 months after onset of the illness revealed a severe bilateral facial weakness and flaccid quadriparesis with inability to lift the arms or legs against gravity, superficial sensory loss from the neck down and a Barthel Index of 4 (Table 1). Electromyography (EMG) performed 1 month after the onset of the illness showed absent radial sensory action potentials and no recordable response to stimulation in the arms or legs. Repeated testing 8 months after the onset of the illness showed a small response following ulnar nerve stimulation and active reinnervation of the proximal and distal arm and leg muscles (clinical recovery is described in Table 1). Patients 2 and 3, both males aged 29, were assessed 6 and 9 months after a spinal cord injury. Patient 2 had a traumatic spinal cord injury resulting in complete sensory loss below the level of T7. Patient 3 had spinal tuberculosis resulting in an incomplete sensory loss bellow the level of T6.
203
3. Assessments 3.1. Sensory–motor examination The severity of motor weakness was recorded using the Motricity index [14], a brief assessment scale of motor function of arm, leg and trunk. Somatosensory function was assessed by subtests of the Rivermead Somatosensory test (RST) [15]. This included pinprick sensation assessing small myelinated sensory fibres and light touch, deep pressure and joint position (proprioception) sensation assessing large myelinated sensory fibres. The maximum RST score is 300. Bilateral caloric vestibular stimulation was also performed. Finally, overall functional independence was assessed using the modified Barthel Index. 3.2. Subjective postural vertical The assessment was carried out in a darkened room with the subjects’ eyes covered. They were seated on a chair mounted in a cylindrical frame with head, shoulders, hips and legs restrained and feet supported. The frame was slowly rolled manually by the examiners at less than 1.58 s 1, a velocity which does not provoke significant semicircular canal stimulation [16]. Immediately after a random offset in the roll (coronal) plane from the starting position to the left or right side, the subject was rolled back at the same speed (less than 1.58 s 1) towards the vertical position. This avoided adaptation to a tilted posture [17,18]. The subject’s task was to indicate as soon as s/he started to feel upright. This position was recorded as an entry point into the ‘‘cone of verticality’’, as defined by Bisdorff et al. [12]. The motion was then continued in the same direction and the subject was asked to indicate as soon as s/he started to feel tilted again which was recorded as an exit point from the ‘‘cone of verticality’’. The rotation was interrupted both when the patient felt ‘‘vertical’’ or ‘‘tilted’’ to allow minor adjustment to the left or right. This paradigm determined the SPV and the ‘‘cone of verticality’’ during motion from left to right and right to left, and is illustrated in Fig. 1. Ten tilts to the left and 10 tilts to the right were executed with a different angle of inclination (tilt) varying from a maximum of 508 (left) to 508 (right). The axis of rotation was at mid-abdominal level. The angle of inclination away from gravitational vertical was measured by an inclinometer attached to the back of the tilting frame. Patient 1 was tested three times initially (Test 1) and three times after 7 months (Test 2). The patients with spinal injury were assessed twice initially (Test 1), and twice after 2 months (Test 2). Patients were tested two or three times in each session to ensure test–retest reliability and results were averaged. 3.3. Subjective visual vertical A luminous line (15 cm long) was displayed on a computer screen 1.2 m away from the subject, at eye level, in
204
G. Mazibrada et al. / Gait & Posture 27 (2008) 202–208
deviation) for the 10 trials. For the control group (n = 20), the average value as well as the intersubject standard deviation were calculated in order to express the data of each patient as Z-scores and analyse his/her individual results with respect to normality ranges. A Z-score above 2 by definition means an abnormality with the alpha risk of 0.05. A non-parametric (Mann–Whitney) test was used to compare SPV orientation, uncertainty and ‘‘size of the cone’’ between the leftwards and rightwards trials in normal subjects and patients. The normal range for the cone of verticality and cone size of SPV and SVV orientation were defined as normal subjects group mean 2S.D. measurement error. Measurement error for the SPV was estimated at 0.58 as the inclinometer scale measured a minimum difference of 18. Measurement error for the SVV was 0.28, the accuracy corresponding to the step of the angular displacement of the luminous line. Throughout the manuscript data are given as mean standard deviation.
5. Results 5.1. Normal subjects 5.1.1. Subjective postural vertical Fig. 1. Diagram illustrating the SPV measurements obtained during the right to left tilt cycle.
a completely dark room. The luminous line was randomly deviated to the right or left and the subject asked to set the line ‘‘vertical to the earth’’ whilst seated upright in the circular frame. The line was moved with the left/right arrow on a computer keyboard by the examiner on instruction by the subject. A computer measured the angle of inclination away from the earth vertical. Ten adjustments were performed. SVV in the patients was tested once only during Test 1.
The mean SPV orientation was 0.4 0.88 that gave a normality range from 2.58 to 1.78. The mean and the standard deviation of the uncertainty across the normal subjects was 1.8 0.48. For leftwards trials, the mean orientation was 1.4 1.08 that gave normality range from 3.98 to 1.18 and the uncertainty was 1.7 0.58. For the rightwards trials, the mean orientation was 0.6 1.58 that gave a normality range from 2.98 to 4.18 and the uncertainty was 1.8 0.58. The mean size of the cone of verticality was 3.1 1.18when the 10 trials per subject were considered, 3.2 1.38 for the leftwards trials and 3.0 1.18 for the rightwards trials. Normal range for the orientation of the cone of verticality was 5.88 for all trials; 6.38 for the leftwards and 5.78 for the rightwards trials. Mann–Whitney testing between left and right trials showed no significant difference in orientation ( p = 0.4), size of cones of verticality ( p = 0.8), or uncertainty ( p = 0.6).
5.2. Subjective visual vertical 4. Data analysis SPV data in normal subjects and patients were expressed as: (1) orientation of the cone of verticality, defined as the mean of the entry and the exit point of the cone of verticality for each of the 10 trials performed in each subject, SPV orientation was also measured from right to left and left to right motion separately (2) uncertainty, defined as the dispersion (standard deviation) of the 10 orientation values and (3) size of the cone of verticality, defined as the mean angular sector between the entry and exit points of the cone of verticality. These three variables were expressed in degrees. SVV data were expressed as orientation, defined as the mean of the 10 trials performed in each subject and uncertainty, defined as the data dispersion (standard
SVV orientation was 0.1 1.08 (normality range from 2.18 to 2.28) and uncertainty was 0.3 1.08.
6. Patients 6.1. Clinical sensory–motor examination Patient 1 was assessed 8 months after the onset of the illness and after a further 7 months when his neurological condition had significantly improved. The first and second clinical assessments are summarised in Table 1. In both assessments, bilateral cold-water (4 8C) caloric vestibular stimulation produced a normal response.
G. Mazibrada et al. / Gait & Posture 27 (2008) 202–208
205
Table 1 Patient 1, 1st and 2nd clinical assessment 1st assessment
2nd assessment
Motricity index Arm Leg Side
Left 53 34 43.5
Proprioception
Normal bilaterally at the elbows and wrists Absent bilaterally at the thumbs, fingers, ankles and toes
Normal bilaterally apart from toes –
Rivermead Somatosensory test (max = 300)
Minimal sensation to pin prick in the left and right hand, otherwise no superficial sensation in the trunk and limbs Total score 22
Normal sensation in the trunk. Superficial sensation in the limbs improved in all modalities apart from two point discrimination No sensation below the knees Total score 130
Barthel score (max = 20) Mobility
4 Hoist required for transfers
18 Able to walk with a Zimmer frame
Patient 2 had a complete sensory loss below the level of T7. His motricity scores were normal in the arms (100/100); in the legs the score was 73/100, giving a total score of 86.5/ 100 bilaterally. Patient 3 had an incomplete sensory loss bellow the level of T6. Surface pressure touch was moderately impaired on the left and severely on the right side. Proprioception was normal in the left ankle and decreased in the right ankle. Motricity scores were normal in the arms (100/100); the left leg score was 58/100, the right leg score was 53/100 giving a total score of 79/100 left and 76.5/100 right. Clinical examination of patients 2 and 3 was the same at both time points. Both patients had a normal response to bilateral cold-water caloric vestibular stimulation. 6.2. Subjective postural vertical
Right 43 39 41.5
Left 81 67 79
Right 81 67 79
Orientation for the leftwards and rightwards trials, Z-scores were 5.1 and 4.9, respectively. Z-scores for the size of the cone including cone size for the leftwards and rightwards trials were 4.5, 3.8 and 4.4, respectively. Z-scores for mean orientation, including orientation for leftwards and rightwards trials of SPV in Patients 2 and 3 were within the normal range (0.3–1.3). The cone size for leftwards trials in Patient 2 was just outside the normal range, the cone size for the leftwards and rightwards trials together was at the upper limit of normal. Z-scores for cone size were 2.5, 2.7 for leftwards trials and 2 for the rightwards trials. The cone size in Patient 3 was within the normal range with Z-scores for the cone size, leftwards and rightwards trials ranging from 0.1 to 0.8. Non-parametric (Mann–Whitney) comparison between the left to right and right to left sided trials in orientation (absolute values), uncertainty and size of the cone showed no significant differences in Patient 1 ( p = 0.7, 0.2 and 0.1, respectively), Patient 2 ( p = 0.06, 0.1 and 0.5, respectively) and Patient 3 ( p = 0.2, 0.1 and 0.1 respectively).
6.2.1. Test 1 SPV orientation estimation from the left and right as well as leftwards and rightwards cone size were all outside the normal range in Patient 1. Patient 1 Z-score for mean orientation was 0.8.
6.2.2. Test 2 The SPV orientation, uncertainty and cone size in normal subjects and patients in Tests 1 and 2 are shown in Table 2.
Table 2 Test 1 and Test 2, SPV orientation, uncertainty and cone size in patients and normal subjects (abnormal values in bold type) SPV orientation/ uncertainty left to right trials Normals
SPV orientation/ uncertainty right to left trials
SPV orientation/ uncertainty left + right trials 0.48/1.8
SPV cone size/ S.D. leftwards trials
SPV cone size/ S.D. rightwards trials
SPV cone size/ S.D. left + right trials
3.28/1.38
38/1.18
3.18/1.18
1.48/1.78
0.68/1.88
Test 1 Patient 1 Patient 2 Patient 3
S6.5-/4.11.18/2.48 2.28/2.48
7.9-/2.63.38/2.48 3.48/2.58
18/3.38 1.48/3.68 0.68/3.78
8.2-/1.48 6.3-/2.18 48/0.78
7.8-/0.68 58/1.58 3.18/1.28
8-/0.68 5.8-/1.98 3.68/1.18
Test 2 Patient 1 Patient 2 Patient 3
0.38/28 0.28/1.48 1.78/1.48
1.98/2.98 38/2.38 1.28/28
18/2.58 1.68/2.98 0.38/2.38
8.2-/0.48 4.88/1.48 3.28/2.18
7.2-/0.28 4.78/1.78 3.58/28
7.7-/0.28 4.88/1.58 3.48/28
206
G. Mazibrada et al. / Gait & Posture 27 (2008) 202–208
SPV orientation estimation from the left and right as well as leftwards and rightwards cone size were all within the normal range in Patients 2 and 3. Cone size, including the cone size for the leftwards and rightwards trials remained abnormal in Patient 1 with Z-scores 4.2, 4.3 and 4.2, respectively. In Patient 1, non-parametric (Mann–Whitney) comparison between orientation (absolute values), uncertainty and size of the cone for the left to right and right to left sided trials did not show significant differences ( p = 0.5, 0.1 and 0.2, respectively). Similarly, comparison of SPV orientation, uncertainty and cone size between Tests 1 and 2 in Patient 1 showed that the mean SPV orientation was not different ( p = 1.0), but orientation for the left to right and right to left sided trials was significantly different ( p = 0.002 and 0.001, respectively). Uncertainty, including uncertainty for the leftwards and rightwards trials, and cone size, including cone size for the leftwards and rightwards trials, were not significantly different ( p = 0.1, 0.6 and 0.3, and p = 1.0, 0.1 and 0.4, respectively). For Patient 1, repeated assessments within testing session 1 and within testing session 2 were not statistically different. This shows good test–retest reliability.
Fig. 2. Patient 1(A) SPV orientation in trials from left to right. (B) SPV orientation in trials from right to left. Results at 8 months (Test 1) and 15 months (Test 2) after illness onset are shown.
Patient 1 change in SPV orientation in Test 1 and Test 2 for the left to right and right to left sided trials are visually summarized in Fig. 2.
6.3. Subjective visual vertical All measures of SVV were within the normal range. SVV orientation in Patient 1 was 1.1 1.08 with an uncertainty of 1.0 0.58, in Patient 2 0.5 0.88 with uncertainty of 1.5 0.58 and in Patient 3 1.5 1.38 with an uncertainty of 1.5 0.68.
7. Discussion Normal subjects have an accurate orientation of postural vertical with a small, symmetrical cone of verticality. They also had a minimal tilt-induced directional bias in SPV orientation, represented by a slight influence of the preceding tilt on the perception of SPV. These findings are comparable with the results reported by Bisdorff et al. [12]. The size of the cone of SPV, that is the width of the sector in which our normal subjects felt vertical, was smaller than the one described by the Bisdorff et al. [12]. This could be because rotation from left to right and right to left was continuous in the study by Bisdorff et al. [12], while in our study the rotation was interrupted when the patient felt ‘‘vertical’’ or ‘‘tilted’’ to allow minor adjustments either to the left or to the right. Patient 1 with Guillain Barre´ syndrome changed in some, but not all, of his SPV measures across time, a dissociation that could be explained by changes in his recovery from peripheral somatosensory loss across time. His initial SPV orientation for the left to right and right to left tilts showed a significant directional bias, a tendency to perceive the body being vertical towards the side of the preceding tilt. This directional bias was much larger than the physiological bias found in our normal subjects, 6.58 versus 1.48 for the leftwards trials and 7.98 versus 0.68 for the rightwards trials, with Z-scores of 4.8 and 4.7, well outside the normal range defined as mean 2S.D. measurement error. As expected from the sensory examination, which showed symmetrical loss of sensation in the trunk and limbs, there was no significant asymmetry between the left to right and right to left sided trials. At Test 2, when sensation had recovered significantly in the trunk and limbs, there was a normalisation of the SPV orientation in rightwards (1.98) and leftwards ( 0.38) trials. By contrast increase in size of the ‘‘cone of verticality’’ and abnormal Z-scores in both directions of tilt shown at Test 1 remained during Test 2 despite the improvement of directional bias in SPV orientation. This dissociation could be explained by incomplete recovery of peripheral somatosensory information. The Guillain-Barre´ syndrome principally affects the myelin sheaths and, in severe cases, axons of larger diameter spinal roots and peripheral nerves. In a significant number of
G. Mazibrada et al. / Gait & Posture 27 (2008) 202–208
cases, it also affects sympathetic and parasympathetic autonomic nerves, and small fibre sensory nerves [19]. The significant directional bias, the loss of sensitivity in SPV orientation and the increased size of the ‘‘cone of verticality’’ in both directions of tilt in our patient with Guillain-Barre´ syndrome must therefore be the result of abnormal peripheral somatosensory input caused by widespread, severe damage to the peripheral nerves and spinal roots. Results from the two spinal patients suggest that afferent input from the lower limbs is relatively unimportant to the perception of verticality in the seated position. In both spinal patients, the mean SPV orientation and uncertainty in the leftwards and rightwards trials were similar and within the normal range. In Patient 2, who had more profound sensory loss, the size of the ‘‘cone of verticality’’ was at the upper limit of normal with a Z-score of 2.5, possibly caused by impaired sensory input from the lower trunk. These results confirm the importance of peripheral somatosensory signals from the trunk in the perception of subjective postural vertical and vertical orientation of the body. Our data were obtained in the seated position where contact/pressure from trunk and shoulders was of prime importance. Presumably, inputs from the lower limbs are critical for orientation in the standing position, but patient data in this position are lacking. The findings are in line with previous studies, suggesting a role for peripheral somatosensory signals in postural orientation of the body. Brown [20] and Nelson [21] reported that reduction in proprioceptive cues by whole body immersion in water significantly impairs estimates of uprightness. Do et al. [22] found that the early motor responses contributing to recovery of balance possibly originate from receptors located at the abdominal or lumbar level and not from vestibular cues or leg proprioceptors. Bisdorff et al. [12] suggested that the perception of body verticality in seating is mainly dependent on proprioceptive and contact cues. In addition, Mittelsteadt et al. [23] suggested that gravity receptors in the trunk provide somatosensory graviceptive signals responsible for the perception of posture and body verticality. Furthermore, based on experiments on healthy subjects laying horizontally in a centrifuge with a vertical rotation axis Mittelsteadt [24] suggested the existence of at least two separate graviceptive inputs from the trunk, one entering the spinal cord at the level of the 11th thoracic dorsal root and another delivering the information to the brain presumably via the vagus or phrenic nerve. Our spinal patients perceived verticality normally without a significant directional bias in SPV orientation. Patient with a complete sensory level at T7 only had a borderline increase in size of the ‘‘cone of verticality’’ in the first test in comparison to normal subjects. It seems likely that our spinal patients had no directional bias in SPV orientation because there was a significant sensory input in a constrained sitting position from the upper trunk and shoulders. Sensory input from these areas was significantly impaired in Patient 1 during Test 1, in the
207
absence of any clinical evidence of autonomic involvement. Whilst these results confirm the importance of somatosensory input from the trunk and/or shoulders to the perception of verticality, what sensory modalities convey this information remains unclear. In addition to confirming the importance of somatosensory input from the trunk to the perception of verticality, we showed that the perception of SVV, tested in the upright position, was normal in all three patients. It is questionable whether SVV tested in such a way can predict the effect of somatosensory loss on visual verticality and its relation to the loss of sensitivity found in SPV. Testing SVV just inside and outside the patients’ cone of verticality and comparing it to the healthy subjects taking into account the standard Aand E-effects would perhaps help determine how somatosensory deficit affects visual verticality. Future studies assessing this would be helpful.
Acknowledgements The authors acknowledge 1. The Physiotherapy Department, The Regional Neurological Rehabilitation Unit, Homerton University Hospital. 2. Hilary Watt, statistician at The National Hospital for Neurology and Neurosurgery.
References [1] Anastasopoulos D, Bronstein AM. A case of thalamic syndrome: somatosensory influences on visual orientation. J Neurol Neurosurg Psychiatry 1999;67:390–4. [2] Mergner T, Huber W, Becker W. Vestibular-neck interaction and transformation of sensory coordinates. J Vestib Res 1997;7(4): 347–67. [3] Pe´rennou DA, Amblard B, Leblond C, Pe´lissier J. Biased postural vertical in humans with hemispheric lesions. Neurosci Lett 1998;252:75–8. [4] Pe´rennou DA, Amblard B, Laassel EM, Benaim C, He´risson C, Pe´lissier J. Understanding the pusher behaviour of some stroke patients with spatial deficits: A pilot study. Arch Phys Med Rehabil 2002;83:570–5. [5] Brandt T, Dieterich M, Danek A. Vestibular cortex lesions affect the perception of verticality. Ann Neurol 1994;35:403–12. [6] Kerkhoff G, Zoelch C. Disorders of visuospatial orientation in the frontal plane in patients with visual neglect following right or left parietal lesions. Exp Brain Res 1998;122:108–20. [7] Anastasopoulos D, Bronstein A, Haslwanter T, Fetter M, Dichgans J. The role of somatosensory input for the perception of verticality. Ann N Y Acad Sci 1999;871:379–83. [8] Karnath HO, Ferber S, Dichangs J. The origin of contraversive pushing: evidence for a second gravioceptive system in humans. Neurology 2000;55(9):1298–304. [9] Pe´rennou D, Playford D, Guerraz M, Mazibrada G, Gresty M, Bronstein A. Dissociation in the verticality perception after a stroke. In: Kingma H, Duysens J, editors. Proceedings of the ISPG 2001. 2001. [10] Dieterich M, Brandt T. Ocular torsion and tilt of subjective visual vertical are sensitive brainstem signs. Ann Neurol 1993;33:292–9.
208
G. Mazibrada et al. / Gait & Posture 27 (2008) 202–208
[11] Bronstein AM, Pe´rennou DA, Guerraz M, Playford D, Rudge P. Dissociation of visual and haptic vertical in two patients with vestibular nuclear lesions. Neurology 2003;61:1260–2. [12] Bisdorff AR, Wolsley CJ, Anastasopoulos D, Bronstein AM, Gresty MA. The perception of body verticality (subjective postural vertical) in peripheral and central vestibular disorders. Brain 1996;119:1523– 34. [13] Paulus W, Straube A, Brandt TH. Visual postural performance after loss of somatosensory and vestibular function. J Neurol Neurosurg Psychiatry 1987;50:1542–5. [14] Collin C, Wade D. Assessing motor impairment after stroke: a pilot reliability study. J Neurol Neurosurg Psychiatry 1990;53: 576–9. [15] Winward CE, Halligan PW, Wade DT. Rivermead Assessment of Somatosensory Performance Manual. Thames Valley Test Company Limited; 2000. [16] Benson AJ, Brown SF. Visual display lowers detection threshold of angular, but not linear, whole-body motion stimuli. Aviat Space Environ Med 1989;60:629–33.
[17] Clark B, Graybiel A. Perception of the postural vertical following prolonged bodily tilt in normals and subjects with labyrinthine defects. Acta Otolaryngol 1964;58:143–8. [18] Riccio GE, Martin EJ, Stoffregen TA. The role of balance dynamics in the active perception of orientation. J Exp Psychol Hum Percept Perform 1992;18(3):624–44. [19] Zochodne DW. Autonomic involvement in Guillain-Barre syndrome: a review. Muscle Nerve 1994;17:1145–55. [20] Brown JL. Orientation to the vertical during water immersion. Aerospace Med 1961;32:209–17. [21] Nelson JG. Effect of water immersion and body position upon perception of the gravitational vertical. Aerosp Med 1968;39:806–11. [22] Do MC, Breniere Y, Bouisset S. Compensatory reactions in forward fall: are they initiated by stretch receptors? Electroencephalogr Clin Neurophysiol 1988;69(5):448–52. [23] Mittelsteadt H, Fricke E. The relative effect of saccular and somatosensory information on spatial perception and control. Adv OtoRhino-Laryng 1988;42:24–30. [24] Mittelsteadt H. Somatic graviception. Biol Physiol 1996;42:53–74.