Tectal plate gliomas Part III: Apparent lack of auditory consequences of unilateral inferior collicular lesion due to localized glioma surgery

Acta Neurochir (Wien) (1994) 127:161-165

:Acta- . N&rochlrurgica g~Springer-Verlag 1994 Printed in Austria

Tectal Plate Gliomas Part III: Apparent Lack of Auditory Consequences of Unilateral Inferior Collicular Lesion Due to Localized Glioma Surgery L. Bognar 1, C. Fischer2, F. Turjman3, F. Michel 4, E. Villanyi 1, C. Mottolese 1, J. Guyota(, and Cl. Lapras 1 Departments of 1Neurosurgery,2Electrophysiology,3Radiology,and 4Neuropsychology,Hospital Pierre Wertheimerof Lyon, Lyon, France

Summary The authors present one of their cases operated on for intrinsic tectal plate glioma. The completeresection of the right inferior colliculus (I.C.) had no apparent auditory consequences, The pre- and post-operativetonal and vocal auditory tests were normal. The brain-stem auditory evoked potentials (BAEPs) and middlelatencypotentials(MLPs)wererecordedpre-, post- and intraoperatively. At the end of surgery all waves were present with a marked delay of wave V and a slight delay of the Pa component. The dichotic test showed a significant right ear extinction but admittedly much less important than expected. The role of inferior colliculus (I.C.) in hearing is discussed. Keywords: Brain-stemauditory evokedpotentials (BAEPs);middle latencypotentials(MLPs);inferiorcolliculus(I.C.); Dichotictest; tectal plate astrocytoma.

Introduction Since the far-field scalp averaging technique for measuring the BAEP was introduced by Jewett (1970), tlhe BAEP has been widely used clinically as a measure of brain-stem integrity and maturity 9 and also as a diagnostic tool in identification of specific brain-stem pathology< 2< 22 Efforts to identify the generators of the BAEP have been made in animals by either using depth electrodes I' 12, 13, 15, 24, 25 or making lesions 2. Lesion experiments and clinical studies in patients with midbrain lesion strongly suggest the inferior colliculus (I.C.) as the generator for wave form V 2' 64, 2o, 22. Hashimoto et aL (1981) concluded from their study with directly recorded brainstem potential that the wave V is generated in the I.C. On the contrary Funai found in rats that the central nucleus of the I.C. is not essential for generating the V wave 4. In a previous study Buchwald stated that the V wave generated in the I.C.

is activated primarily by crossed projections 2. Caird etal. stated that in cats P 5 and the following slow negative wave were reduced by I.C. lesions. When only one I.C. was ablated, this reduction was greater when the ear contralateral to the lesion side was stimulated 3. Hashimoto 8 recorded a large negative wave at the latency of Na (18ms) at the level of I.C. in man 8. Aspiration of the I.C. in the guinea pig resulted in reduction of the slow negative component following the BAEP. Thus both human and animal studies indicate that the I.C. contributes to the auditory middle latency response (MLR) such as the V wave of BAEP 14. The effects of lidocain injection into different auditory nuclei on surface potentials and on local activity support the concept that the M L R is produced by multiple contributing sources from distinct anatomical pathways 14. Early anatomical I8 and electrophysiologica121 studies have described a medial projection system for processing auditory information which function parallel with the more laterally situated primary auditory pathway. This so called extralemniscal pathway projects from the mesencephalic reticular formation through the medial tegmentum to the medial thalamus particularly to nuclei centralis lateralis (CL) and center median (CM). Bilateral I.C. resection enhanced the appearance of the CL and CM midlatency responses which suggests that these systems are functionally parallel but interactive. This medial system is anatomically much more diffuse than the lemniscal system 1~ Several earlier anatomical studies of human brainstem nuclei suggest that the assumption of total similarity of human and other mammalian auditory centers is not entirely valid 16' 17, 23. Precise information of the

162

sources of each BAEP and MLP component in man would be of the utmost importance. One central issue is the question of which of the multiple auditory centers and pathways remain prominent in the human brain. In this paper special interest is given to the role of the I.C. Here we present the first case in the neurosurgical literature where the surgical lesion was limited to only one (the right) I.C. The BAEP and MLP recordings were performed pre- and post-operatively.

Case Report A 12-year-old girl was admitted in December 1990 with one month history of headache. On examination she was found to be a vague, slow-moving girl unable to give a clear history. She had bilateral papilloedema with decreased visual acuity (4/10) in the left eye. Her pupils were equal and brisk with full extraocular movements and there was no Parinaud's syndrome. The lower cranial nerves were normal. The audiometry was normal. A C T scan showed markedly dilated lateral and III ventricles with normal IV ventricle and posterior fossa. A diagnosis of late onset aqueductal stenosis was made and a medium pressure ventriculoperitoneal shunt was inserted at the end of December 1990. MRI performed 3 months later revealed an intrinsic tectal lesion (Fig. 1). The BAEPs and MLPs were normal. On December 11, 1991 a right occipital eraniotomy was performed. A 2 crn incision was made in the tentorium starting at the level of the hiatus approximately 1 cm lateral to the straight sinus. Under the operating microscope the distorded, bulging quadrigeminal plate was exposed. Intra-operative monitoring of BAEPs and MLPs was performed. Before incision of the bulging part of the tectal plate local surface electrodes were also used for recording. The lesion was macroscopically totally resected without a real plane of cleavage. At the end of the intervention the aqueduct was

L. Bognar et al.: Tectal Plate Gliomas. Part III opened and the right I.C. was excised as seen on the post-operative MR images (Fig. 2). The patient's post-operative course was benign. Papilloedema had resolved. She has a normal school life. The histological examination showed a juvenile type astrocytoma. She is without any post-operative treatment. The MRI after 11 months shows no tumour recurrence. The post-operative tonal and vocal audiometry were normal. Diehotie Test The patient was tested in April and November 1992 with dichotic tasks (i.e., repetition of verbal items simultaneously presented to both ears). Patient had to repeat 30 pairs of words and 10 pairs of sentences. Results showed:

Words Sentences

Right ear

Left ear

97% 95%

72% 65%

Auditory Evoked Potentials BAEPs and MLPs have been recorded between the vertex (FZ) and the ear lobe ipsilateral to the stimulus (A 1 or A 2), using clicks of 100 microsecond-duration. The contralateral ear was masked by a white noise. Prior to surgery (December 9, 1991), BAEPs and MLPs were normal. Intra-operative monitoring has been carried out with BAEPs and MLPs being continuously recorded during surgery under propofol anaesthesia. At the end of surgery all waves were present with a marked delay of the V wave and a slight delay of the Pa component (Table 1). Weeks after surgery a reduction in the V wave amplitude was present when stimuling the left ear.

Fig. 1. Pre-operative MRI. (a) Sagittal SE: 600/15 MR image shows the bulbous distorded tectal plate. (b) Transverse section, Gadolinium injected SE: 500/20 MR image shows a hyposignal area in the tectum. (c) Transverse SE: 2400/50 MR image shows a localized hypersignal lesion in the tectal plate

L. Bognar etal.: Tectal Plate Gliomas. Part III

163

Fig. 2. Post-operative MRI. (a) Sagittal SE: 520/22 MR image shows the resection of the right I.C. (b) Transverse SE: 600/15 MR image shows the resection of the right I.C. (c) Coronal (view) or section, Gadolinium injected SE: 600/15 MR image shows the complete resection of right I.C..(d) Coronal (view), Gadolinium injected SE: 600/15 MR image shows the preservation of the S.C.

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L. Bognar etal.: Tectal Plate Gliomas. Part III

Table I I

III

V

Na

Pa

Before surgery/left ear Before surgery/right ear

1.7 1.6

4.1 3.8

5.7 5.7

18.2 16

30.7 30

End of surgery

1.8

4.3

6.6

18.4

32.7

After surgery/left ear After surgery/right ear

1.8 1.6

3.9 3.9

6.3a 5.7

18.2 18.4

32.5 32.7

a Amplitude reduced. All latencies in milliseconds. Discussion

In this p a t i e n t the right I.C. has been surgically r e m o v e d as r e p o r t e d b y direct o b s e r v a t i o n o f the surgeon d u r i n g the o p e r a t i v e p r o c e d u r e a n d b y the posto p M R i m a g e s (Fig. 2). A t the d i c h o t i c test one i n d e e d observes a significant right e a r e x t i n c t i o n b u t a d m i t t e d l y m u c h less i m p o r t a n t t h a n expected. A c o m p l e t e d e a f f e r e n t a t i o n n o r m a l l y leads to a c o m p l e t e c o n t r a l a t e r a l extinction. A b n o r m a l i t i e s o f M L P s (either a m p l i t u d e r e d u c t i o n or at least l a t e n c y shift) m i g h t have been expected. A t the end o f the surgical p r o c e d u r e , far-field r e c o r d e d N a a n d P a were u n e q u i v o c a l l y r e c o r d e d . F r o m n u m e r o u s studies in m a n we k n o w t h a t farfield r e c o r d e d B A E P s are present, w h i c h e v e r e a r is stimulated, a n d r e c o r d i n g s m i g h t even be n o r m a l , as far as the lesion o f the a u d i t o r y p a t h w a y s are u n i l a t e r a l a n d n o t bilateral. M o r e o v e r r e c o r d i n g s f r o m b r a i n s t e m t u m o u r s have d e m o n s t r a t e d t h a t m e d i a l l y far-field r e c o r d e d B A E P s m i g h t be n o r m a l w h e n the t u m o u r is a s y m m e t r i c a l . T a k i n g into a c c o u n t t h a t the a u d i t o r y a s c e n d i n g p a t h ways have several c o n n e c t i o n s within the b r a i n s t e m , one is n o t s u r p r i s e d t h a t a lesion strictly limited to one colliculus with the o t h e r colliculus being intact, the V wave as well as P a c o u l d be r e c o r d e d . T h e afferent i n p u t c o u l d have m o v e d f r o m b o t h c o c h l e a r nuclei to b o t h cortices v i a one single colliculus. V w a v e a m p l i t u d e r e d u c t i o n was p r o o f o f a slight d y s f u n c t i o n at the collicular level. Bilateral d e s t r u c t i o n o f b o t h I.C. with M L P s being p r e s e n t m i g h t be q u e s t i o n a b l e a n d then the role o f the e x t r a l e m n i s c a l a u d i t o r y p a t h w a y s w o u l d be discussed. References

1. Achor LJ (1975) Auditory brain stem responses in neurological disease. Arch Neurol 32:761-768 2. Buchwald JS, Huang CM (1975) Far-field acoustic response: origins in the cat. Science 189:382-384

3. Caird David M, Klinke R (1987) The effect of inferior colliculus lesions on auditory evoked potentials. Electroencephalogr Clin Neurophysiol 68:237-240 4. Hiroaki F, Sotaro F (1983) Experimental study on the effect of inferior colliculus lesions upon auditory brain stem response. Audiology 22:9-19 5. Hamilton AE (1976) Correlation between confirmed sites of neurological lesions and abnormalities of far-field auditory brainstem responses. Electroencephalogr Clin Neurophysiol 41: 594--608 6. Hashimoto I, Ishiyama Y, Tozuka G (1979) Bilaterally recorded brainstem auditory evoked responses: their asymmetric abnormalities and lesions of the bralnstem. Arch Neurol 36:161-167 7. Hashimoto I, Ishiyama Y, Yoshimoto T, Nemoto S (1981) Brainstem auditory evoked potentials recorded directly from human brain-stem and thalamus. Brain 104:841-859 8. Hashimoto I (1982) Auditory evoked potentials from the human midbrain: slow bralnstem responses. Eleetroencephalogr Clin Neurophysiol 53:652-657 9. Hecox K, Galambos R (1974) Brainstem auditory evoked responses in human infants and adults. Arch Otolaryngo199: 3033 10. Hinman CL, Buchwald JS (1983) Depth evoked potential and single unit correlates of vertex mJdlatency auditory evoked responses. Brain Res 264:57-67 11. Jewett DL (1970) Volume-conducted potentials in response to auditory stimuli as detected by averaging in the cat. Electroencephalogr Clin Neurophysiol 28:609-618 12. Legatt AD, Arezzo JC, Vaughan Jr HG (1986) Short-latency auditory evoked potentials in the monkey II intracranial generators. Electroencephalogr Clin Neurophysiol 64:53-73 13. Legatt AD, Arezzo JC, Vaughan Jr HG (1988) The anatomic and physiologic bases of brain stem auditory evoked potentials. Neurol Clin 6:681-704 14. McGee T, Kraus N, Comperatore C, Nicol T (1991) Subcortical and cortical components of the MLR generating system. Brain Res 544:211-220 15. Moller AR, Burgess J (1986) Neural generators of the brainstem auditory evoked potentials (BAEPS) in the rhesus monkey. Electroencephalogr Clin Neurophysiol 65:361-372 16. Moore JK, Moore RY (1971) A comparative study of the superior olivary complex in the primate brain. Folia Primatol 16: 35-51 17. Moore JK, Osen KK (1979) The cochlear nuclei in man. Am J Anat 154:393-418 18. Nauta WJH, Kuypers HG: Some ascending pathways in the brainstem reticular formation. In: Jasper HH, Proctor LD, Knighton RS, Noshay WC, Costello RT (eds) Little Brown, Boston, pp 3-30 19. Tozuka G (1979) Bilaterally recorded brainstem auditory evoked responses: their asymmetric abnormalities and lesions of the brainstem. Arch Neurol 36:161-167 20. Starr A, Hamilton AE (1976) Correlation between confirmed sites of neurological lesions and abnormalities of far-field auditory brainstem responses. Electroencephalogr Clin Neurophysiol 41:549-608 21. Starzl TE, Taylor CW, Magoun HW (1951) Collateral afferent excitation of reticular formation of brainstem. J Neurophysiol 15:479-496

L. Bognar etal.: Tectal Plate Gliomas. Part III 22a.Stockard JJ, Rossiter VS (1977) Clinical and pathologic correlates of brainstem auditory response abnormalities. Neurology 27:316-325 22b.Buchwald JS, Huang CM (1975) Far-field acoustic response: origins in the cat. Science 189:382-384 23. Strominger NL, Hurwitz JL (1976) Anatomical aspects of the superior olivary complex. J Comp Neurol 170:485-498 24. Velasco M, Velasco F, Pacheco T, Martinez A, Olvera A (1982) Subcortical correlates of the auditory brainstem potentials in the monkey: referential responses. Int J Neursci 17:199-208

165 25. Velasco M, Velasco F, Romo R, Almanza X (1984) Subcortical correlates of the auditory brainstem potentials in the monkey: bipolar EEG and multiple unit activity responses. Int J Neurosci 22:235-252

Correspondence: L. Bognar, M.D., Service de Neuro-Chirurgie, H6pital Neurologique et Neuro-Chirurgical Pierre Wertheimer, 59 Boulevard Pinel, F-69394 Lyon, France.