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The Connections of the Inferior Colliculus and the Organization Of THE JOURNAL OF COMPARATIVE NEUROLOGY 201:25-49 (1981) The Connections of the Inferior Colliculus and the Organization of the Brainstem Auditory System in the Greater Horseshoe Bat (Rhinolophus ferrumequinum) HERMANN SCHWEIZER Arbeitskreis Neuro- und Rezeptorphyszologte, Fachbereich Biologie (Zoologre), J W Goethe Unzuersttaet, D 6000 FrankfurtlM Federal Republic of Germany ABSTRACT The connections of the inferior colliculus, the mammalian mid- brain auditory center, were determined in the greater horseshoe bat (Rhinolophus ferrumequinum), using the horseradish peroxidase method. In order to localize the auditory centers of this bat, brains were investigated with the aid of cell and fiber-stained material. The results show that most auditory centers are highly developed in this echo- locating bat. However, the organization of the central auditory system does not generally differ from the mammalian scheme. This holds also for the organization of the superior olivary complex where a well-developed medial superior olivary nucleus was found. In addition to the ventral and dorsal nuclei of the lateral lemniscus a third well-developed nucleus has been defined which projects ipsi- laterally to the inferior colliculus and which was called the intermediate nucleus of the lateral leminiscus. All nuclei of the central auditory pathway project ipsi-, contra-, or bilaterally to the central nucleus of the inferior colliculus with the exception of the medial nucleus of the trapezoid body and the medial geniculate body. The tonotopic organization of these projections and their possible functions are discussed in context with neurophysiological investigations. Insectivorous bats are mammals that hunt are the higher auditory centers, the medial at night with the help of an active sonar sys- geniculate body, and the auditory cortex? tem. They emit ultrasonic calls and extract The most detailed anatomical study of the from the returning echoes information about auditory system in bats is the early work of their environment and their prey with the aid Poljak ('26a,b) in Rhinolophus ferrumequinum of a highly developed auditory system. Since and Nyctulus noctulu. Poljak concluded that the discovery of this specialized orientation the organization of the central auditory path- system in bats many neurophysiological ex- way in these bats does not differ significantly periments have been performed on acoustic from that of other mammals. However, his processing in the central auditory system of studies of fiber connections were done only these animals. The neurophysiological data with myelin-stained material. show that the auditory system of echolocating In contrast to Poljak's findings, Harrison and bats is highly specialized and adapted to their Irving ('661, Irving and Harrison ('671, and specific orientation behavior (e.g., Neuweiler, Masterton and Diamond ('67) emphasized '80; Pollack, '80; Suga and O'Neill, '80). some differences in the central auditory system Surprisingly, only a few anatomical data of bats, especially concerning the organization exist for the central auditory system in bats of the superior olivary complex. They advo- (for review see Henson, '70). Most anatomical cated that bats do not have a medial superior investigations show that some of the auditory olivary nucleus. Therefore it was generally centers are highly developed. But, two main agreed that the organization of the auditory questions arise from earlier investigations: system of echolocating bats differed from that How is the auditory pathway organized up to of other mammals, and not until the auditory the inferior colliculus and how well-developed pathways of bats were recently investigated 0021-996'718112011-0025$07.00 @ 1981 ALAN R. LISS, INC. 26 H. SCHWEIZER with modern neuroanatomical tracing tech- 40-60-pm-thick frontal sections. The sections niques (Schweizer, '78; Schweizer and Radtke, were collected in cold 0.1 M phosphate buffer '80; Zook, '79; Zook and Casseday, '78; Zook (pH 7.2) and were processed the same day for and Casseday, '80) did this concept begin to the HRP reaction. change. Three different procedures for HRP reaction This paper presents data on the structure of were used: The DAB method (Graham and the lower auditory centers and the connections Karnovsky, '66), the DAB cobalt chloride of the inferior colliculus of the greater horse- method (Adams, '771, and the TMB method shoe bat, Rhinolophus ferrumequinum, and (Mesulam, '78). After washing, the sections tries to clarify the question of whether there were mounted on gelatinized slides, air dried, are fundamental differences in the anatomical counterstained in cresylviolet (for DAB-re- organization of the central auditory system of acted sections) or in a 194 acidified neutral red echolocating bats in comparison to that of solution (for TMB reacted sections), dehy- other mammals. drated in graded ethanol, cleared in xylene, and coverslipped. METHODS The sections were examined with a Zeiss In order to examine the cytoarchitecture of photomicroscope under brightfield or darkfield the auditory centers of the greater horseshoe illumination or between crossed polarizers (for bat, six brains were fixed in formalin, embed- the TMB method) (Illing and Waessle, '79). ded in paraplast or celloidin, and cut in the Drawings were made from frontal sections to three standard planes in 20-km-thick sections. show the cytoarchitecture of auditory nuclei Sections were stained with cresylviolet for and to show the spatial distribution of labeled cells, with hematoxyline for myelinated fibers, cells. or with cresylviolet and luxol fast blue for a combined cell and fiber stain. For visualization of unmyelinated fibers, some sections were A bbreviatrons processed according to a modified Bodian silver impregnation method (Ziesmer, '52). ALP0 Anterolateral periolivary nucleus AVCN Anteroventral cochlear nuclues The connections of the inferior colliculus BIC Brachium of the inferior colliculus were studied with the horseradish peroxidase CGM Central pray matter (HRP)method. The animals were anesthetized CN Cochlear nucleus by intraperitoneal injection of nembutal DCN Dorsal cochlear nucleus DNLL Dorsal nucleus of the lateral lemniscus (2.5-3.0 mg/100 gm body weight) and placed DPO Dorsal periolivary nucleus in a head holder. The skin and muscles over 1c lnfenor colliculus the midbrain were removed and a small hole ICC Central nucleus of the infenor colliculus was drilled into the skull. HRP (Sigma type VI ICP Pericentral nucleus of the inferior colliculus ICX External nucleus of the interior colliculus or HRP from Serva) was injected into different INLL Intermediate nucleus of the lateral lemniscus parts of the IC either by pressure or ionto- LL Lateral lemniscus phoretically. In five cases HRP was applied in LNTB Lateral nucleus of the trapezoid body solid form. LSO Lateral superior olrvary nucleus MGB Medial geniculate body Survival times varied from 4 to 96 hours, MNTB Medial nucleus of the trapezoid body but in most experiments the survival time was MSO Medial superior olivary nucleus 24 hours. The animals were then deeply an- PVCN Posteroventral cochlear nucleus esthetized with nembutal (4 mg/100 gm body SOC Superior olivary complex VMPO Ventromedial penolivary nucleus weight) and perfused through the heart with VNLL Ventral nucleus of the lateral lemniscus phosphate-buffered heparinized saline (pH 7.2) VNTB Ventral nucleus of the trapezoid body followed by the fixative solution. In most an- VOP Ventral periolivary nucleus imals the fixative consisted of 2% paraformal- dehyde + 1%'glutaraldehyde in 0.05 M phos- phate buffer (pH 7.2).After 20-30 minutes of RESULTS perfusion the brains were removed from the The presentation of the results is divided skull, covered with a thin layer of egg yolk, into two parts. Part one gives a brief descrip- and postfixed for 4-6 hours in the cold. The tion of the cytoarchitecture of the auditory cen- tissue was then washed overnight in two ters with the exception of the medial genicu- changes ofcold 0.1 M phosphate buffer (pH 7.2) late body and the auditory cortex. A detailed containing 20% sucrose. The following day the description of subdivisions of different audi- brains were cut on a freezing microtome into tory nuclei and the neurons composing these AUDITORY PATHWAYS OF BATS 27 Fig. 1. Frontal sections of the medulla oblongata and The rectangles in the right half of each section indicate the the overlying cerebellum (Ceb) (left) and of the midbrain location of the sections in figures 2 to 5. Ahhrev.: NLL- (right) showing the position of the lower auditory centers. nuclei of the lateral lemniscus. nuclei will be part of further studies. In part the lateral brain surface (Fig. 2). In the ventral two, the results of the HRP experiments are part a superficial ependymal cell layer is fol- presented. lowed medially by a molecular cell layer, a “fusiform” cell layer, and a polymorphic cell region. However, the fusiform cell layer can be Part I: Cytourchitecture of the lower auditory distinguished from the polymorphic cell region centers only by a more orderly arrangement of fusi- Figure 1 shows the position of the lower au- form cells, which are often oriented with their ditory centers in two frontal sections of the long axis running from lateral to medial, and brainstem. The description of these centers by a slightly higher density of granular cells. starts from caudal to rostra1 with the cochlear In contrast to the ventral DNC, the dorsocau- nucleus complex followed by the superior oli- dal region shows a disorderly cell arrange- vary complex, the nuclei of the lateral lemnis- ment. But the main difference is that a mo- cus, and the inferior colliculus. lecular layer is not developed in this part of The cochlear nucleus complex. As in other the DCN. mammals the cochlear nucleus complex (CN) of Rhinolophus ferrumequinum can be divided The Posterouentrul Cochlear Nucleus. The on the basis of cytoarchitectural features (cell PVCN is situated ventral to the DCN and just size, cell shape, packing density of cells) into caudal to the acoustic branch of the eighth three subnuclei (Fig.
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