ORIGINAL ARTICLE
Inferior cerebellar peduncular lesion causes a distinct vestibular syndrome J.-H. Choia, J.-D. Seob, Y. R. Choic, M.-J. Kimc, H.-J. Kimd, J. S. Kime and K.-D. Choic a
EUROPEAN JOURNAL OF NEUROLOGY
Department of Neurology, Pusan National University School of Medicine, Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan; bDepartment of Neurology, Bonhospital; cDepartment of Neurology, Pusan National University Hospital, Pusan National University School of Medicine and Biomedical Research Institute, Busan; d Department of Biomedical Laboratory Science, Kyungdong University, Goseong; and eBiomedical Research Institute and Department of Neurology, Seoul National University Bundang Hospital, Seongnam, Korea
Keywords:
acute vestibular syndrome, body lateropulsion, inferior cerebellar peduncle, ocular tilt reaction, stroke Received 5 August 2014 Accepted 6 February 2015 European Journal of Neurology 2015, 22: 1062– 1067 doi:10.1111/ene.12705
Background and purpose: The inferior cerebellar peduncle (ICP) contains various fibres to and from the cerebellum relating to the integration of the proprioceptive and vestibular functions. However, the full clinical features of isolated unilateral ICP lesions have not been defined in humans. Methods: Eight consecutive patients with isolated unilateral ICP lesions at the pontine level (six with stroke, one with multiple sclerosis and one with brainstem encephalitis) received bedside neurological and neuro-otological evaluations and underwent laboratory tests including measurements of the subjective visual vertical (SVV) and ocular torsion, bithermal caloric tests and pure tone audiometry. Results: All patients developed isolated acute vestibular syndrome (AVS) with ipsilesional spontaneous nystagmus (n = 7) and contralesional ocular tilt reaction (OTR) and/or SVV tilt (n = 7). In view of the normal head impulse test in all patients and skew deviation in one, our patients met the criteria for AVS from central lesions. Five patients showed a directional dissociation between the OTR/SVV tilt and body lateropulsion that fell to the lesion side whilst the OTR/SVVtilt was contraversive. Conclusions: A unilateral ICP lesion at the pontine level leads to the development of isolated AVS. However, a negative head impulse test and directional dissociation between OTR/SVV tilt and body lateropulsion may distinguish lesions involving unilateral ICP at the pontine level from those affecting other vestibular structures.
Introduction The inferior cerebellar peduncle (ICP) connects the medulla oblongata with the cerebellum, and has the shape of a thick rope-like strand between the caudal pons and rostral medulla [1]. The ICP contains various fibres to and from the cerebellum, which mainly function to integrate the proprioceptive and vestibular functions [1]. Since the vestibulocerebellum receives mossy fibre inputs from the vestibular nuclei and nerve, Correspondence: K.-D. Choi, Department of Neurology, College of Medicine, Pusan National University Hospital, 1-10 Ami-dong, Seogu, Busan 602-739, Korea (tel.: 82 51 240 7317; fax: 82 51 245 2783; e-mail: [email protected]).
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and projects efferent fibres to the vestibular nuclei via the ICP [1], a lesion involving the ICP may give rise to postural imbalance with vertigo and nystagmus. In monkeys, experimental sectioning of a unilateral ICP has shown a fall towards the lesion side without nystagmus [2]. However, the full clinical features of isolated unilateral ICP lesions have not been defined in humans. Clinical and laboratory findings of eight patients with isolated unilateral ICP lesions are reported.
Materials and methods Eight patients with isolated unilateral ICP lesions (five with cerebral infarction, one with cerebral haemor-
© 2015 EAN
INFERIOR CEREBELLAR PEDUNCULAR LESION
rhage, one with multiple sclerosis and one with brainstem encephalitis) were prospectively recruited at the Dizziness Clinic of Pusan National University Hospital from November 2011 to July 2013. The diagnosis of an isolated ICP lesion was based on magnetic resonance imaging (MRI) findings. The location of the ICP on the MRI was defined using the anatomic diagrams of Neuroanatomy: Text and Atlas [3], and isolated involvement of the ICP was determined when the MRI lesions were restricted to the lateral wall of the fourth ventricle in the caudal pons or the dorsolateral portion in the medulla oblongata. The patients included three men and five women with ages ranging from 18 to 83 years (mean age 53.6 21.4 years) (Table 1). All patients received bedside neurological and neuro-otological evaluations including horizontal head impulse tests, prism cross-cover test for ocular alignment and an assessment of balance. Imbalance was graded from 0 to III based on the following criteria: grade 0 (normal), able to stand on tandem Romberg with eyes open for 3 s; grade I (mild), unable to stand on tandem Romberg with eyes open for at least 3 s; grade II (moderate), unable to stand on Romberg with eyes open for at least 3 s; and grade III (severe), unable to stand or sit without support [4]. Eye movements were recorded binocularly at a sampling rate of 60 Hz using three-dimensional video-oculography (SensoMotoric Instruments, Teltow, Germany). Spontaneous nystagmus was recorded both with and without fixation. Gaze-evoked nystagmus
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was induced with horizontal (30°) and vertical (20°) target displacements. Head-shaking nystagmus (HSN) was induced using a passive head-shaking manoeuvre and the presence of HSN in the patients was defined only when the maximal slow phase velocity of the induced nystagmus exceeded the values (mean + 2 SD) observed in normal controls after subtracting the slow phase velocity of spontaneous nystagmus (≥3°/s) and when the nystagmus lasted more than 5 s [5]. For positional nystagmus, patients bent down, straightened and turned their heads to either side whilst supine. Patients were also subjected to Dix Hallpike manoeuvres and the straight head hanging test. Laboratory tests included measurements of the subjective visual vertical (SVV) and ocular torsion, bithermal caloric tests and pure tone audiometry. To measure the tilt of SVV, subjects were seated upright in a dark room and were asked to align a rod (80 cm long and 0.3 cm wide) vertically. The rod was presented randomly at various angles from the vertical, at a distance of 130 cm from the subjects’ eyes. The SVV value for each subject was examined by calculating the average of five adjustments. In order to express trial-to-trial variability, the coefficient of variation (CV, standard deviation divided by the mean) of the SVV values was also calculated. There was no time restraint in performing the tests. The erect position of the head was ensured by the examiner manually or through the use of a head rest attached to the chair when necessary. Pathological SVV tilt in the
Table 1 Neuro-otological findings of eight patients with isolated unilateral inferior cerebellar peduncular lesion at the pontine level SN without fixation (°/s)
OT (°)b
Patient Sex/age Lesion no. (years) side
H
V
1 2
F/83 M/73
L R
L4 R7.3
– – U3.4 –
L –
– –
3 4 5 6 7 8
M/67 M/57 F/47 F/52 F/18 F/32
L R R L R R
– R2 R6.6 L5.2 R10.3 R4
– – –
L – – – – –
– – – – – –
T
– – CW3 CCW2 D3.4 CW3.6 – –
RE
LE
Body Caloric SD lateropulsion tests PTA
13.6 27.9
17.3 0.7
4.1 23.7
– L
L (III) NO
No CP No CP
17.9 1.4 9.4 16.8 5.1 3.6
14.6 0 9.23 7.82 7.9 2.7 11.4 4.3 4.8 18.7 9.1 4.8
– – – – – –
L (III) NO R (I) L (I) R (I) NO
No No No No No No
SVV HSN HIT (°)a
CP CP CP CP CP CP
Other signs
Normal – Normal Apogeotropic horizontal positional nystagmus Normal – Normal – Normal – Normal – Normal – Normal –
M, male; F, female; SN, spontaneous nystagmus; H, horizontal; V, vertical; T, torsional; R, right; L, left; D, downbeat; U, upbeat; CCW, counterclockwise torsional (upper poles of the eyes beat toward the left shoulder); CW, clockwise torsional (upper poles of the eyes beat toward the right shoulder); HSN, head-shaking nystagmus; HIT, head impulse test; SVV, subjective visual vertical; OT, ocular torsion; RE, right eye; LE, left eye; SD, skew deviation; NO, not observed; CP, canal paresis; PTA, pure tone audiometry. a The given numbers are the mean value of subjective visual vertical testing with binocular viewing (normal range 3.0 to 3.0; a negative value indicates a counterclockwise rotation) [5]; bnegative value means intorsion, whilst positive value indicates extorsion. Pathological ocular torsion is defined when the eye shows any intorsion (
Inferior cerebellar peduncular lesion causes a distinct vestibular syndrome J.-H. Choia, J.-D. Seob, Y. R. Choic, M.-J. Kimc, H.-J. Kimd, J. S. Kime and K.-D. Choic a
EUROPEAN JOURNAL OF NEUROLOGY
Department of Neurology, Pusan National University School of Medicine, Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan; bDepartment of Neurology, Bonhospital; cDepartment of Neurology, Pusan National University Hospital, Pusan National University School of Medicine and Biomedical Research Institute, Busan; d Department of Biomedical Laboratory Science, Kyungdong University, Goseong; and eBiomedical Research Institute and Department of Neurology, Seoul National University Bundang Hospital, Seongnam, Korea
Keywords:
acute vestibular syndrome, body lateropulsion, inferior cerebellar peduncle, ocular tilt reaction, stroke Received 5 August 2014 Accepted 6 February 2015 European Journal of Neurology 2015, 22: 1062– 1067 doi:10.1111/ene.12705
Background and purpose: The inferior cerebellar peduncle (ICP) contains various fibres to and from the cerebellum relating to the integration of the proprioceptive and vestibular functions. However, the full clinical features of isolated unilateral ICP lesions have not been defined in humans. Methods: Eight consecutive patients with isolated unilateral ICP lesions at the pontine level (six with stroke, one with multiple sclerosis and one with brainstem encephalitis) received bedside neurological and neuro-otological evaluations and underwent laboratory tests including measurements of the subjective visual vertical (SVV) and ocular torsion, bithermal caloric tests and pure tone audiometry. Results: All patients developed isolated acute vestibular syndrome (AVS) with ipsilesional spontaneous nystagmus (n = 7) and contralesional ocular tilt reaction (OTR) and/or SVV tilt (n = 7). In view of the normal head impulse test in all patients and skew deviation in one, our patients met the criteria for AVS from central lesions. Five patients showed a directional dissociation between the OTR/SVV tilt and body lateropulsion that fell to the lesion side whilst the OTR/SVVtilt was contraversive. Conclusions: A unilateral ICP lesion at the pontine level leads to the development of isolated AVS. However, a negative head impulse test and directional dissociation between OTR/SVV tilt and body lateropulsion may distinguish lesions involving unilateral ICP at the pontine level from those affecting other vestibular structures.
Introduction The inferior cerebellar peduncle (ICP) connects the medulla oblongata with the cerebellum, and has the shape of a thick rope-like strand between the caudal pons and rostral medulla [1]. The ICP contains various fibres to and from the cerebellum, which mainly function to integrate the proprioceptive and vestibular functions [1]. Since the vestibulocerebellum receives mossy fibre inputs from the vestibular nuclei and nerve, Correspondence: K.-D. Choi, Department of Neurology, College of Medicine, Pusan National University Hospital, 1-10 Ami-dong, Seogu, Busan 602-739, Korea (tel.: 82 51 240 7317; fax: 82 51 245 2783; e-mail: [email protected]).
1062
and projects efferent fibres to the vestibular nuclei via the ICP [1], a lesion involving the ICP may give rise to postural imbalance with vertigo and nystagmus. In monkeys, experimental sectioning of a unilateral ICP has shown a fall towards the lesion side without nystagmus [2]. However, the full clinical features of isolated unilateral ICP lesions have not been defined in humans. Clinical and laboratory findings of eight patients with isolated unilateral ICP lesions are reported.
Materials and methods Eight patients with isolated unilateral ICP lesions (five with cerebral infarction, one with cerebral haemor-
© 2015 EAN
INFERIOR CEREBELLAR PEDUNCULAR LESION
rhage, one with multiple sclerosis and one with brainstem encephalitis) were prospectively recruited at the Dizziness Clinic of Pusan National University Hospital from November 2011 to July 2013. The diagnosis of an isolated ICP lesion was based on magnetic resonance imaging (MRI) findings. The location of the ICP on the MRI was defined using the anatomic diagrams of Neuroanatomy: Text and Atlas [3], and isolated involvement of the ICP was determined when the MRI lesions were restricted to the lateral wall of the fourth ventricle in the caudal pons or the dorsolateral portion in the medulla oblongata. The patients included three men and five women with ages ranging from 18 to 83 years (mean age 53.6 21.4 years) (Table 1). All patients received bedside neurological and neuro-otological evaluations including horizontal head impulse tests, prism cross-cover test for ocular alignment and an assessment of balance. Imbalance was graded from 0 to III based on the following criteria: grade 0 (normal), able to stand on tandem Romberg with eyes open for 3 s; grade I (mild), unable to stand on tandem Romberg with eyes open for at least 3 s; grade II (moderate), unable to stand on Romberg with eyes open for at least 3 s; and grade III (severe), unable to stand or sit without support [4]. Eye movements were recorded binocularly at a sampling rate of 60 Hz using three-dimensional video-oculography (SensoMotoric Instruments, Teltow, Germany). Spontaneous nystagmus was recorded both with and without fixation. Gaze-evoked nystagmus
1063
was induced with horizontal (30°) and vertical (20°) target displacements. Head-shaking nystagmus (HSN) was induced using a passive head-shaking manoeuvre and the presence of HSN in the patients was defined only when the maximal slow phase velocity of the induced nystagmus exceeded the values (mean + 2 SD) observed in normal controls after subtracting the slow phase velocity of spontaneous nystagmus (≥3°/s) and when the nystagmus lasted more than 5 s [5]. For positional nystagmus, patients bent down, straightened and turned their heads to either side whilst supine. Patients were also subjected to Dix Hallpike manoeuvres and the straight head hanging test. Laboratory tests included measurements of the subjective visual vertical (SVV) and ocular torsion, bithermal caloric tests and pure tone audiometry. To measure the tilt of SVV, subjects were seated upright in a dark room and were asked to align a rod (80 cm long and 0.3 cm wide) vertically. The rod was presented randomly at various angles from the vertical, at a distance of 130 cm from the subjects’ eyes. The SVV value for each subject was examined by calculating the average of five adjustments. In order to express trial-to-trial variability, the coefficient of variation (CV, standard deviation divided by the mean) of the SVV values was also calculated. There was no time restraint in performing the tests. The erect position of the head was ensured by the examiner manually or through the use of a head rest attached to the chair when necessary. Pathological SVV tilt in the
Table 1 Neuro-otological findings of eight patients with isolated unilateral inferior cerebellar peduncular lesion at the pontine level SN without fixation (°/s)
OT (°)b
Patient Sex/age Lesion no. (years) side
H
V
1 2
F/83 M/73
L R
L4 R7.3
– – U3.4 –
L –
– –
3 4 5 6 7 8
M/67 M/57 F/47 F/52 F/18 F/32
L R R L R R
– R2 R6.6 L5.2 R10.3 R4
– – –
L – – – – –
– – – – – –
T
– – CW3 CCW2 D3.4 CW3.6 – –
RE
LE
Body Caloric SD lateropulsion tests PTA
13.6 27.9
17.3 0.7
4.1 23.7
– L
L (III) NO
No CP No CP
17.9 1.4 9.4 16.8 5.1 3.6
14.6 0 9.23 7.82 7.9 2.7 11.4 4.3 4.8 18.7 9.1 4.8
– – – – – –
L (III) NO R (I) L (I) R (I) NO
No No No No No No
SVV HSN HIT (°)a
CP CP CP CP CP CP
Other signs
Normal – Normal Apogeotropic horizontal positional nystagmus Normal – Normal – Normal – Normal – Normal – Normal –
M, male; F, female; SN, spontaneous nystagmus; H, horizontal; V, vertical; T, torsional; R, right; L, left; D, downbeat; U, upbeat; CCW, counterclockwise torsional (upper poles of the eyes beat toward the left shoulder); CW, clockwise torsional (upper poles of the eyes beat toward the right shoulder); HSN, head-shaking nystagmus; HIT, head impulse test; SVV, subjective visual vertical; OT, ocular torsion; RE, right eye; LE, left eye; SD, skew deviation; NO, not observed; CP, canal paresis; PTA, pure tone audiometry. a The given numbers are the mean value of subjective visual vertical testing with binocular viewing (normal range 3.0 to 3.0; a negative value indicates a counterclockwise rotation) [5]; bnegative value means intorsion, whilst positive value indicates extorsion. Pathological ocular torsion is defined when the eye shows any intorsion (
