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Comparative Morphology of the Accessory Olfactory Bulb in Bats

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Comparative Morphology of the Accessory Olfactory Bulb in Bats J. Anat. (1980), 130, 2, pp. 349-365 349 With 14 figures Printed in Great Britain Comparative morphology of the accessory olfactory bulb in bats HEIKO D. FRAHM AND KUN WAR P. BHATNAGAR Max-Planck-Institut fur Hirnforschung, Neurobiologische Abteilung, Deutschordenstrasse 46, D-6000 Frankfurt/M.-71, Federal Republic of Germany and Department of Anatomy, University of Louisville, Schools of Medicine and Dentistry, Health Sciences Center, Louisville, Kentucky 40232, U.S.A. (Accepted 9 April 1979) INTRODUCTION A few investigations in the past have dealt with the anatomy of the accessory olfactory bulb (Nebenbulbus) in vertebrates. Such studies have involved am- phibians, reptiles, and mammals (Allison, 1953; Stephan, 1975). An accessory olfactory bulb in bats was first mentioned by Kappers & Theunissen (1908). Humphrey (1936) denied its presence in Tadarida mexicana. Schneider (1957, 1966) examined a wide spectrum of Chiroptera but did not report an accessory olfactory bulb. Mann (1961, 1963) described this structure in several phyllostomatids in significant detail. Brief descriptions of the accessory bulb in some phyllostomatids and in Miniopterus schreibersi were provided by Bhatnagar & Kallen (1974) and by Cooper & Bhatnagar (1976). Frahm (1978), reporting data on the volumetric analysis of the accessory olfactory bulb in 26 chiropteran species, pointed out a correlation between the presence of this brain component and dietary preferences. Bats as a group are highly diverse both morphologically and behaviourally (Wimsatt, 1970, 1977), and offer stimulating models for the neurologist. In recent years interest has been renewed in the morphology, projections, and functional aspects of the vomeronasal organ in various mammals (Cooper & Bhatnagar, 1976; Winans & Powers, 1977; Bhatnagar, 1979). However, no study has dealt with the projections of the vomeronasal organ in bats. To facilitate such investigations in these flying mammals, to rectify erroneous statements in the literature on the chiropteran accessory olfactory bulb, and to correlate our studies on the vomero- nasal organ with its primary relay centre in the brain, it seemed highly appropriate to begin by exploring the morphology of the accessory bulb in a large number of species. In this paper we report the histomorphology of the accessory olfactory bulb in 26 chiropteran species out of a total of 76 species investigated. MATERIALS AND METHODS This study was based on 148 bats belonging to 76 species, 48 genera and 8 families. Much of this material was collected by Stephan in the Congo and Colombia, and by Stephan and Frahm in Indonesia and Malaysia. In the field, immediately after capture, the animals were weighed, then perfused with physiological saline solution followed by Bouin's fluid. The brains were removed within 2 hours of fixation 0021-8782/80/2828-7320 $00.20 © 1980 Anat. Soc. G.B. & I. 350 H. D. FRAHM AND K. P. BHATNAGAR (Stephan, 1960). After 4 days the brains were transferred to alcohol. In the laboratory, the usual paraffin-Paraplast embedding procedures were followed. Serial sections, usually 20 pum thick, were prepared of the entire brain and stained for cyto- and fibre architectonics (using cresyl violet, Delafield's haematoxylin, Hansen's iron haematoxylin and Heidenhain-Woelcke). Investigations were carried out on the accessory olfactory bulb (AOB, Table 1). To localize its position in the main bulb (MOB), the latter was divided into three equal parts (medial, middle and lateral) by lines running perpendicular to the axis created by its greatest diameter. Several parameters were measured (Table 2), namely: total length, and length of different layers from their first occurrence through to the end; width (measured with an ocular micrometer on the section where it had its largest extension); glomerular diameter (mean of ten large, well circum- scribed glomeruli); mitral and granule cell nucleus diameter (mean of ten rep- resentative mitral and granule cell nuclei). All measurements were taken in the three Glossophaga soricina series. Since variation proved to be small, measurements in other species were limited to only one series of sections. However, the histological observations were based upon exami- nation of all available series. RESULTS AND DISCUSSION The typical mammalian accessory olfactory bulb has been described by Stephan (1965, 1975) as made up of six layers, namely: layer of the vomeronasal nerve fibres; glomerular layer; external plexiform layer; mitral cell layer; internal plexiform layer; and internal granular layer (including the periventricular and ependymal layers). In bats, an AOB was observed primarily in the family Phyllostomatidae, with other examples provided by the mormoopid bat, Pteronotus parnellii, and the vespertilionid, Miniopterus schreibersi. In Miniopterus, the only vespertilionid bat known to possess an AOB, this structure is clearly less developed. Position and size of the main and accessory olfactory bulbs The AOB is found in the posterior part of the main bulb. In most species it is situated mid-dorsally on the MOB in such a way that it cannot be seen from the lateral side without removing the overlying forebrain. Rostrally it is usually rounded, but caudally it (especially its internal granular layer) often stretches out laterally. When a well developed MOB is present the AOB tends to be situated laterally (Figs. 4, 10), whereas with a poorly developed MOB its position is more dorsal (Figs. 1, 12). The MOB is remarkably long in Phyllostomus, Sturnira and in some Stenoderminae. Small MOBs occur in Anoura caudifera, and in the mormoopid bat Pteronotus parnellii. Minimum values for both length and width are found in Miniopterus schreibersi. The longest AOBs occur in Phyllostomus hastatus, P. discolor, and in Desmodus rotundus. Smaller ones can be observed in Diphylla ecaudata and M. schreibersi. No precise measurements were possible in the stenoderminid bat Sphaeronycteris, which has an AOB only 20-25 ,tm long. Usually the width of the AOB exceeds the length. This ratio is reversed in a few species, for example, Sturnira lilium, Uroderma, P. parnellii and, in an extreme way, in P. hastatus. The accessory and the main bulbs often end together. However, in P. parnellii, and in the sub- families Carolliinae, Sturnirinae and Stenoderminae, the AOB ends 400 ,tm or more before the MOB ends. Accessory olfactory bulb in bats 351 The sizes of the main and accessory bulbs are independent, for example in the sub-family Sturnirinae the main bulbs are relatively large but the AOBs are relatively small (Table 2). Layers of the accessory olfactory bulb On account of the great variability in the size of the AOB in different species of bats, all six layers of the typical AOB are not present in all species (Table 1). Bats with a well developed AOB show clear lamination into six layers. In most species, however, the internal plexiform layer is not well represented. Further reduction of the AOB affects the external plexiform and the internal granular layers. Even in a minute AOB some glomeruli and mitral cells at least can always be observed. Vomeronasal nerve fibre layer (I) In bats the vomeronasal nerve always approaches the AOB over the medial surface of the MOB. In the vicinity of the AOB it is a single bundle of fibres. The vomero- nasal nerve fibre layer is very pronounced in Phyllostomus discolor, Anoura geoffroyi (Fig. 14b) and in Artibeus jamaicensis. The vomeronasal nerve, originating in the union of numerous filaments (McCotter, 1912) beneath the sensory epithelium of the vomeronasal organ, takes an ascending and posterior course on the nasal septum in separate strands (Bhatnagar & Kallen, 1974) which join together as these approach the cribriform plate of the ethmoid. The medial course of the vomeronasal nerve appears to be common in mammals. However, in most prosimians (with the exception of Tupaia glis and Lemurfulvus) the vomeronasal nerve runs on the lateral surface of the MOB to reach the AOB from the lateral side (Stephan, 1965). In Avahi and Propithecus both possibilities have been reported: in some specimens the vomeronasal nerve was found to enter the AOB from the medial, and in others from the lateral side. In simians, where the AOB is present only in New World monkeys (Platyrrhini), the vomeronasal nerve enters from the medial side, as in insectivores, bats and most mammals. The laminations of the AOB tend to bend either medially (as in bats, e.g., Fig. 6) or laterally, in the direction of the incoming vomeronasal nerve (Stephan, 1965). Mann (1961) stated the vomeronasal nerve of Phyllostomus hastatus to be 'myelinated'. This erroneous statement has since appeared sporadically in the literature. We examined this nerve in a P. hastatus series stained for nerve fibres (Fig. 13 d) as well as in all the other species reported here, and concluded that it is unmyelinated in bats as it is in other mammals (Negus, 1958). Often a prominent blood vessel was seen in the groove between the olfactory bulb and the frontal lobe (Artibeus cinereus, Fig. 9, and A. jamaicensis, Fig. 10) and this was subsequently seen penetrating the AOB in close connection with the entry of the vomeronasal nerve. As stated by Stephan (1975), one main difference between the olfactory nerve fibres and the vomeronasal nerve as they approach their respective destinations is that the latter shows shorter and thicker branchings, and the branching of a single vomeronasal nerve fibre is not confined exclusively to a single glomerulus as is seen in the main bulb. 23 ANA 130 352 H. D. FRAHM AND K. P. BHATNAGAR 0 0 Ct: U2 a) I- I- -a 0 0° C)Cd & 0< C) CU cn cd 0 0 0 O C) CISCU 0 2 Co 0 0-1C'S *-.s a) :t *u0 .2ci. '0 (a) CU '0 -__ 0 0 0 cts0l _ W -a) C)OCU~ ~ ~ ~ ~ ~ ~ ~~C S0 EU a) .0 '0 ~CU CtO ^ C a)Y C-iU ._ * oCU = 1- q Q '0 '0 a) '0 C Cd cis 0 0 CU _, ~CUo -ao > .0 cd '0* '0 a.) .
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