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Descending Projections to the Dorsal and Ventral Divisions of the Cochlear Nucleus in Guinea Pig

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Hearing Research, 52 (1991) 255-268 2% 0 1991 Elsevier Science publishers B.V. 0378-5955/91/$03.50 HEARES 01529 Descending projections to the dorsal and ventral divisions of the cochlear nucleus in guinea pig Susan E. Shore I, Robert H. Helfert 2, Sanford C. Bledsoe, Jr. 2, Richard A. Altschuler 2 and Donald A. Godfrey ’ ’ Department of Otolaryngologv, Medical College of Ohio, Toledo, Ohio, and ’ Kresge Hearing Research Institute, University of Michigan, Ann Arbor, Michigutz, U.S.A. (Received 6 August 1990; accepted 17 October 1990) The origins of extrinsic projections to the guinea pig dorsal and ventral cochlear nuclei were identified by examining the retrograde transport of horseradish peroxidase conjugated to wheatgerm agglutinin following its injection into each of these divisions. Major projections originated in periolivary regions of the superior olivary complex, the contralateral cocblear nucleus and the inferior colliculus. There was no contribution from the nuclei of the lateral lemniscus to these pathways. The heaviest projection from the periolivary regions to both divisions of the co&ear nucleus arose bilaterally in the ventral nucleus of the trapezoid body. The ipsilateral lateral nucleus of the trapexoid body also projected heavily to dorsal and ventral cc&ear nucleus. In addition, the ventral co&ear nucleus received a substantial projection from the dorsal aspect of the ipsilateral dorsomedial periolivary nucleus. Projections originating bilaterally in the central nucleus of the inferior colliculus terminated in the deep layers of dorsal cochlear nucleus. These projections appear to be more strongly ipsilateral and specific than those reported in the cat. Horseradish peroxidase; Ventral cochlear nucleus; Dorsal cochlear nucleus; Superior olivary nuclei; Inferior colliculus Inaction Rasmussen, 1960, 1967; Osen et al., 1984; Van Noort, 1969; Adams, 1983; Elverland, 1977). Many Previous studies have shown that in addition to of the non-cochlear synaptic endings in the synaptic endings from the VIIIth nerve (for re- cochlear nucleus originate in neurons of the super- views see Cant and Morest, 1984; Caspary, 1986), ior olivary complex, nuclei of the lateral lemnis- most neurons in the co&ear nucleus receive in- cus, the inferior colliculus, and the contralateral nervation from non-co&ear sources (Cant, 1981; co&ear nucleus (Van Noort, 1969; Adams and Kane and Firm, 1977; Kane and Conlee, 1979; Wan, 1976; Kane, 1977; Elverland, 1977; Cant and Gaston, 1982; Adams, 1983; Spangler et al., 1987; Covey et al., 1984; Winter et al., 1989; Abbreviations: AVCN = Anteroventral cochlear nucleus; CN = Benson and Potashner, 1990). Cochlear nucleus; CPO = Caudal periolivary region; DCN = The manner in which periolivary cell groups Dorsal cochlear nucleus; DMPO = Dorsomedial periolivary and other auditory areas project to specific nucleus; DPO = Dorsal periolivary nucleus; IC = Inferior col- cochlear nucleus neuronal targets is critical to the liculus; LNTB = Lateral nucleus of the trapezoid body; LSO = Lateral superior olivary nucleus; MNTB = Medial nucleus of ability of these neurons to process complex signals the trapezoid body; MS0 = Medial superior olivary nucleus; and operate over a wide dynamic range. This OCB = Olivocochlear bundle; PVCN = Posteroventral co&ear study addresses the question of interspecies dif- nucleus; SOC = Superior olivary complex; VCN = Ventral ferences in the organization of olivary projections cochlear nucleus; VNTB-Ventral nucleus of the trapezoid to specific regions of the cochlear nucleus. The body. Correspondence to: S.E. Shore, Medical College of Ohio, De- methodology differs from other studies in the partment of Otolaryngology, Toledo, OH 43699, U.S.A. guinea pig by examining and quantifying the ret- 256 rograde transport of horseradish peroxidase con- set; 80 mg/kg) and xylazine (Rompun; 4 mg/kg) jugated to wheatgerm agglutinin from different administered intramuscularly. Periodic supple- regions of the cochlear nucleus to other brainstem mentation was used to maintain anesthetic levels nuclei. In the cat, these projections terminate in all t~ou~out the procedure. The left co&ear regions of the cochlear nucleus, with some nucleus was visualized, after a posterior fossa nucleotopic organization: The rostra1 periolivary surgical approach, by aspirating a small part of regions project more heavily to rostra1 cochlear the overlying cerebellum. A glass micropipette nucleus while the caudal periolivary groups pro- filled with 2% wheat germ agglutinin conjugated ject more heavily to caudal co&ear nucleus (Van to horseradish peroxidase (WGA-HRP), in phos- Noort, 1969; Adams, 1983; Spangler et al., 1987). phate buffered saline (pH 7.4), was placed under The tree shrew, on the other hand, shows a more visual control on the surface of the dorsal or specific dist~bution pattern, with the dorsomedial ventral co&ear nucleus. After the electrode place- periolivary region and dorsal periolivary region ment, the brain was covered with warm mineral projecting only to the anteroventral cochlear oil to prevent tissue desiccation and reduce brain nucleus, whereas the ventral nucleus of the pulsation. Evoked potentials in response to click trapezoid body and the caudal portion of the stimulation were recorded as the electrode was lateral nucleus of the trapezoid body project only advanced ventrally (see Shore and Nuttall, 1985). to dorsal cochlear nucleus and posteroventral At a depth corresponding to the maximum-ampli- cochlear nucleus (Covey et al., 1984). In contrast tude evoked potential, a continuous, positive cur- to the tree shrew, a recent study of the superior rent (3-5 PA) was passed through the silver re- olivary projections to cochlear nucleus in the cording wire for 2-15 min. After the electrode was guinea pig showed similar results to those found removed, some neck muscle was applied to replace in the cat (Winter et al., 1989). This was surprising the volume of aspirated brain, dental cement was in view of findings that brainstem projections to used to seal the opening, and the animal was the cochlea in guinea pig and cat differ in their sutured and allowed to recover. After a 24-h organization (Robertson, 1985; Robertson et al., survival period, the animal was deeply anesthe- 1987). tized with pe~tobarbital and perfused transcar- This study has confirmed reports that major dially with 50 ml of 0.05% sodium nitrite in nor- projections to the cochlear nucleus originate in mal saline, followed by 750 ml of mixed aldehyde periolivary regions of the superior olivary com- fixative (1.25% glutaraldehyde and 1.0% for- plex, the contralateral cochlear nucleus (see Shore maldehyde in phosphate buffer, pH 7.4). Follow- et al., 1991), and the inferior colliculus. The results ing their removal from the skull and postfixation here indicate that some periolivary nuclei in the for 2-4 h in the same fixative, the brainstems were guinea pig have more specific target areas in the immersed overnight in 20% sucrose in 0.12 M co&ear nucleus than previously indicated. In par- phosphate buffer, pH 7,4. After frozen sectioning, ticular, the projections from the dorsomedial peri- the 40 pm-thick transverse sections containing the olivary regions in the guinea pig terminate prim- cochlear nucleus (CN), superior olivary complex arily in the ventral division of the co&ear nucleus. (XX), nuclei of the lateral lemniscus (NLL) and The guinea pig also receives more strongly ipsi- IC were reacted with 3.3’-5,5’ -tetramethylben- lateral projections from periolivary nuclei to the zidine (TMB) to visualize the peroxidase (Mesu- cochlear nucleus, than the cat (e.g. Adams, 1983). lam, 1978). The reacted sections were then These findings imply that information processing mounted, counterst~ned with neutral red (Mesu- in the auditory brainstem may vary si~fic~tly lam, 1978) and studied using a Leitz Dialux mi- among species. croscope equipped with a drawing tube. An esti- mate of the total number of labeled cells in the M&hods SOC was obtained by counting those in every 5th section. Labeled cell types were described in terms Fifteen pigmented guinea pigs (250-400 g) were of soma shape and size, and the location of the anesthetized with ketamine hydrochloride (Keta- nucleus when possible. Soma size was measured 257 using a calibrated eyepiece micrometer. The mea- 1991). There was a different distribution of labeled surements presented are not corrected for tissue cells in each of these major regions, depending on shrinkage which occurs during processing. whether the injection was centered in dorsal cochlear nucleus (DCN) or ventral cochlear nucleus. Injections in the cochlear nucleus produced ret- Descending projections from the superior olivaty rograde labeling in the ipsilateral and con- complex tralateral cochlear nucleus, superior olivary com- plex (SOC) and inferior colliculus. Only the pro- jections from the SOC and inferior colliculus are Definition of periolivaly regions discussed in this paper; the cochlear nucleus pro- Periolivary nuclei are defined in terms of their jections are presented elsewhere (Shore et al., positions with respect to the lateral and medial 50, 50 D 45 A 45 6888 (PVCN) 53190 (DcN) 40 40 N-201 0 N-1338 35 35 i 30 / 30 25 25 20 20 15 15 10 10 5 5 n 0 LNTB VNTB MNTB DMPO DPO CPO LSO LNTB VNTB MNTB DMPO DPO CPO LSO 50 45 3288 (PVCN) 62988 (DCN) 1 E 40 N-=1380 N-1 155 35 30 25. 20. 15. 10- 5- o- LNTB VNTB MNTB DMPO DPO CPO LSO LNTB VNTB MNTB DMPO DPO CPO LSO I IPSUATERAL 817138 (DCN+WCN) m coNTRAlATERM N-1265 40 35 32489 (PVCN+AVCN) 30 N-3370 25 25 20 20 15 15 10 10 5 5 0 0 INlB VNTB MNTB DUPO DPO CPO Lso LNlB VNTB LlNlB DMW DPO CPO LSO SUPERIOR OLIVARY REGION SUPERIOR OLIVARY REGION Fig. 1. Percentages of labeled cells in different SGC nuclei following WGA-HRP injections centered on different cochlear nucleus regions, as indicated in parentheses. (A) Animal 53190; injection centered on medial DCN.
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