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LEMNISCUS and ~ COLLICULUS on the ABR in GUINEA Pig L 352 Electroencephalography and clinical Neurophysiology, 1983, 56:352-366 Elsevier ScientificPublishers Ireland, Ltd. GENERATION OF AUDITORY BRAIN STEM RESPONSES (ABRs). IlL EFFECTS OF LESIONS OF THE SUPlglIK~ OLIVE, LA~ LEMNISCUS AND ~ COLLICULUS ON THE ABR IN GUINEA PiG l SHIN-ICHI WADA 2 and ARNOLD STARR 3 Department of Neurology, University of California at Irvine, Irvine, Calif. 92717 (U.S.A.) (Accepted for publication: April 15, 1983) While there is consensus that the ABR recorded stem contralateral to the ear stimulated. In this at the scalp represents the far-field activity of final article of the series we made fairly discrete brain stem structures comprising the auditory lesions in the superior olivary complex, lateral pathway (Jewett 1970; Buchwald 1982), there is lemniscus and inferior colliculus to further define uncertainty as to the precise localization of the the locus of the generator site(s) for the ABR generators for some of the components. While components. waves I (PI, N1), and perhaps II (P2, N2), reflect activity in the VllIth nerve both within the cochlea and proximally near the brain stem (Moiler et al. Methods 1981), wave III (P3, N3) has been localized only roughly to the region of the pans (Starr and Ham- Subjects ilton 1976; Stockard and Rossiter 1977), perhaps Twenty-six adult guinea pigs weighing between contralateral to the stimulated ear (Buchwald and 0.7 and 1.1 kg were subjected to lesions of the Huang 1975), and IV and V (P4, N4) to the region pans and midbrain. of the midbrain (Starr and Hamilton 1976; Stimulus generation, ABR recording and data Hashimoto et al., 1981; Moiler and Jannetta 1982) analyses were the same as in the first two studies perhaps bilaterally (Buchwald and Huang 1975). (Wada and Starr 1983a, b). Furthermore, it is not known whether each wave is generated primarily by one brain stem structure or Surgery whether activity in several different sites combine The animals were deeply anesthetized with to account for the appearance of that wave (Jewett sodium pentobarbital. Following a tracheotomy 1970; Buchwald and Huang 1975; Achor and Starr and fixation of a small screw at a point 3 mm 1980a). posterior to the bregma to serve as the 'active' In the first two articles of this series on the role electrode for recording the ABR, 3 different surgi- of the trapezoid body in the generation of the cal approaches were employed to make the brain ABR (Wada and Starr 1983a, b) we demonstrated stem lesions. A ventral approach was similar to that components P1, NI, P2 and P4 are generated that described in the first two papers and was used in the brain stem ipsilateral to the ear stimulated, to lesion the superior olivary complex. A dorsal whereas N2, P3 and N3 are generated in the brain approach consisting of removal of the occipital bone and aspirating the cerebellum was used for lesions of the midbrain and lateral lenmiscus. A This research was supported by Research Grant NS-11876 lateral approach through the bulla and temporal from the National Institute of Health. 2 Present address: Department of Neurosurgery, Kumamoto bone was used to expose the lateral aspect of the UniversityMedical School, 1-1-1 Honjo, Kumamoto860, Japan. brain stem for unilateral lesions of the superior 3 To whom all correspondenceshould be addressed. olivary complex or lateral lemniscus. This last 0013-4649/83/$03.00 © 1983 Elsevier Scientific Publishers Ireland, Ltd. GENERATION OF ABRs. III 353 approach damaged the cochlea so that the ABR of the ventral acoustic stria entering the ipsilateral only to contralateral input could be tested. superior olivary complex. Fig. 1 shows the recon- struction of the lesion and the corresponding ef- Experimental lesions and histology fects on the ABR in guinea pig GX. The lesion Electrolytic lesions were made in 19 animals by involved the lateral aspect of the lateral superior placing a 100 #m stainless steel wire, insulated olive and dorsal part of the ventral acoustic stria, except for the bare cut end, into the appropriate and extended dorsally into the pons. Changes in structure guided by the potentials recorded from the ABR were primarily to stimulation of the ear that electrode to clicks. Discrete lesions (1-4.5 ipsilateral to the lesion (labeled 'R' in Fig. 1); mm) were then made by passing 1 mA of cathodal component P4 decreased in amplitude by 39% and current for varying times (5-50 see). In 6 animals, was delayed in latency by 0.2 msec; component the brain stem was sectioned transversely with a N4 decreased in amplitude by 35% and was also blunt spatula just caudal to the inferior colliculus delayed in latency (0.25 msec). In contrast, compo- without damaging the basilar artery. A unilateral nent N3 increased in amplitude by 25%. The other section was made in 4 and bilateral sections in the components, P1 through P3, were unchanged. The other 2 animals. In one other animal the inferior ABR evoked by stimulation of the ear con- colliculus was removed bilaterally by aspiration. tralateral to the lesion (labeled 'L' in Fig. 1) Following the lesions, recordings of the ABR were showed no significant amplitude and latency continued for at least 2 h. changes except for components N1 and P5 which At the end of the experiment, the animals were decreased slightly in amplitude (by 21% and 29% perfused through the heart with normal saline respectively) while P4 increased slightly by 13%. In followed by a 10% buffered formalin solution. The the other 3 animals with a lesion in this area the entire brain was removed, blocked and stored in major effect on the ABR was a decrease in ampli- 10% buffered formalin for at least 1 week prior to tude (29-70%) and a prolongation of the latency sectioning. Serial reconstruction of the extent of of components P4 and N4 to ipsilateral stimula- the lesion was made from 60 pm frozen sections tion similar to the example in Fig. 1. In addition, stained with cresyl violet. Lesions made by tran- in these 3 guinea pigs, components P3 and N3 also section were confirmed both by visual inspection decreased slightly (13-35%) in amplitude. In and by examining serial sections from the lesion summary, lesions of the lateral aspect of lateral sites. superior olive that did not involve the trapezoid body affected the ABR evoked by stimulation of the ear ipsilateral to the lesion with a decrease in Results amplitude and prolongation of latency particularly of components P4 and N4. The effects of lesions of the region of the super- ior olivary complex, the lateral lemniscus (uni- (B) Lesions of the superior olivary complex lateral and/or bilateral) and inferior colliculus on In 3 animals the lesions were restricted to the the amplitude and latency of the ABR are sum- superior olivary complex without significant marized in Tables I and II. damage to other auditory structures. Fig. 2 shows the reconstruction of the lesion and the corre- (A) Lesions adjacent to the lateral aspect of the sponding effects on the ABR in guinea pig PF. superior ofivary nucleus The lesion involved almost the entire medial super- In 4 animals the lesion was dorsolateral to the ior olivary nucleus and approximately the dorsal superior olivary nucleus contacting the lateral 2/3 of the lateral superior olivary nucleus without aspect of the lateral superior olivary nucleus. The impinging on the trapezoid body. The ABR to lesions, in common, involved a portion of the stimulation of the ear contralateral to the lesion lateral superior olivary nucleus, the dorsal and (labeled 'L' in Fig. 2) had a decrease in amplitude intermediate acoustic stria, as well as those fibers for components N1 (22%), P3 (68%), N3 (57%) 354 S.-I. WADA, A. STARR POSTERIOR<D Fig. 1. Reconstruction of a lesion of the lateral region of the pons in guinea pig GX and corresponding effects on the ABR to monaural stimulation. In this and all subsequent figures the ABR in the control period is in the solid line and following the lesion is in the interrupted line. The lesion involved the lateral aspect of the lateral superior olive, the periolivary region including the dorsal and intermediate acoustic striae and the dorsal aspect of the ventral acoustic stria. Note that components P4 and N4 are both delayed and attenuated to ipsilateral stimulation (R) whereas contralateral stimulation (L) is without effect. The following abbreviations are used in this and subsequent figures. TB = trapezoid body; LSO = lateral superior olive; MSO = medial superior olive; LL = lateral lemniseus; IC - inferior eollicuhis; IV vent = fourth ventricle. and N4 (48%), and amplitude increments for com- ( C) Lesions of both the superior olivary complex and ponents P1 (14%) and N2 (22%). (The changes in the trapezoid body P I and N1 appear to be due to a baseline shift In 3 animals, the lesions involved both the since the composite wave I was unchanged.) In superior olivary complex and a significant part of contrast, the ABR to ipsilateral stimulation the trapezoid body. Fig. 3 shows the reconstruc- (labeled 'R' in Fig. 2) showed components P4 and tion of the histology and the corresponding effects N4 to decrease in amplitude by 11% and 64% on the ABR in guinea pig PE. The lesion began respectively. In the other 2 animals, the lesions within 2 mm of the dorsum of the brain stem also involved the entire medial superior olivary extending ventrally to involve almost the entire nucleus and the dorsomedial side of the lateral medial superior olivary nucleus, approximately 3/4 superior olivary nucleus. The changes in the ABR of the lateral superior olivary nucleus in its medial to eontralateral stimulation were comparable with side, and approximately 60% of the fibers in the a marked attenuation of component P3 and N4 to trapezoid body just ventral to the superior ofivary contralateral stimulation without consistent effect complex.
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