Nasal Fossa of Mouse and Dwarf Lemurs (Primates, Cheirogaleidae)†
Article first published online: 9 JUL 2008
Copyright © 2008 Wiley-Liss, Inc.
The Anatomical Record
Volume 291, Issue 8, pages 895–915, August 2008
How to Cite
Smith, T. D. and Rossie, J. B. (2008), Nasal Fossa of Mouse and Dwarf Lemurs (Primates, Cheirogaleidae). Anat Rec, 291: 895–915. doi: 10.1002/ar.20724
- Issue published online: 10 JUL 2008
- Article first published online: 9 JUL 2008
- Manuscript Accepted: 4 APR 2008
- Manuscript Received: 23 JAN 2008
- nasal cavity;
- Top of page
- MATERIALS AND METHODS
- LITERATURE CITED
- Supporting Information
Dimensions of the external midface in mammals are sometimes related to olfactory abilities (e.g., “olfactory snouts” of strepsirrhine primates). This association hinges on the largely unexplored relationship between the protruding midface and internal topography of the nasal fossae. Herein, serially sectioned heads of embryonic to adult cheirogaleid primates (mouse and dwarf lemurs) and a comparative sample were studied. To assess the anteroposterior distribution of olfactory epithelium (OE) within the nasal fossa, the surface area of OE and non-OE was measured in two mouse lemurs (one adult, one infant). Prenatally, ethmoturbinal projections appear in an anteroposterior sequence. Fetal mouse lemurs, tenrecs, voles, and flying lemurs have four ethmoturbinals that project toward the nasal septum. Major distinctions among these mammals include the number of turbinals in recesses and the extent of the olfactory recess. Surface area measurements in the adult mouse lemur reveal that 31% of the entire nasal fossa is lined with OE. The majority is sequestered in a posterior recess (70% OE). Anterior to this space, only 28% of the nasal fossa is lined with OE. Ethmoturbinal I is lined with relatively less OE (35%) compared with more posterior ethmoturbinals (46–57%). Age comparisons support the idea that OE increases less than non-OE between ages. Regionally, results suggest that most growth in surface area occurs in turbinals. But in all ethmoturbinals, surface area of non-OE differs between ages more than that of OE. This study shows that the anterior part of the nasal fossa is mostly nonolfactory in Microcebus murinus. Anat Rec, 291:895–915, 2008. © 2008 Wiley-Liss, Inc.
Among all vertebrates, mammals have evolved the nasal cavities with the greatest internal complexity. The lateral nasal wall is complicated by projections called turbinals (turbinates, conchae). These invade the nasal airway space and increase surface area for both olfactory and respiratory mucosae (Negus, 1958; Hillenius, 1992, 1994). In morphology, these projections may vary from simple ridges to highly elaborated scrolls. Anatomists first understood the intricate contours of the nasal fossae by the study of hemisected skulls (e.g., Zuckerkandl, 1887; Seydel, 1891; Kollmann and Papin, 1925; Cave, 1973), but coronal sections of the rostrum of mammals provided a far clearer picture, because the most median turbinals often overlay other turbinals and recesses (Negus, 1958). The advent of computed tomography now allows nondestructive access to the nasal cavity and the ability to three-dimensionally reconstruct the internal structures and spaces (Rowe et al., 2005; Rossie, 2006; Craven et al., 2007). Such studies reveal the actual space through which inspired air and volatile chemicals travel (Craven et al., 2007). While the available information on internal nasal morphological adaptations continues to increase, knowledge of the mucosa that lines the surfaces is far less detailed for most mammals (Smith et al., 2007a, b).
In the mammalian nasal cavity, four types of epithelia have been said to line the internal boundaries. These include respiratory, olfactory, stratified, and a more inconsistent “transitional” epithelium (Adams, 1986). These epithelia, combined with underlying elements of the lamina propria that support them, are the basis for physiological properties of internal structures in the nasal region. Mucosal characteristics of the inner contours of the nasal fossae (each comprising half of the nasal cavity) are only known in a generalized manner for most mammals. In addition, the terminology used to describe structures varies greatly. These factors are limitations in the endeavor to understand functional specializations and the evolutionary modifications of thenasal fossa in different mammalian taxa, particularly in groups with highly diverse nasal morphology (Smith et al., 2004; Smith and Rossie, 2006; Smith et al., 2007a).
Detailed mucosal “maps” are available for some small-bodied mammals (Adams, 1972; Clancy et al., 1994). The percentage of mucosa found on individual elements (e.g., turbinals) has been provided for the opossum (Rowe et al., 2005) and some bat species (Bhatnagar and Kallen, 1975). For larger bodied mammals, internal distribution of nasal mucosa has been generally described (e.g., goats, horses—Kumar et al., 1993, 2000). Quantitative data are available for rabbits, cats, and dogs, although without specific associations between osseous structures and mucosal coverings (see Negus, 1958; Moulton and Biedler, 1967). In sum, a generalized topographic association of internal nasal structures with epithelial types can be gleaned from the literature summarized above (and see Moore, 1981, for review). The anteroinferior portions of the nasal fossa, including turbinals therein, are lined with nonolfactory epithelium (mostly of respiratory and stratified types). Turbinals of the ethmoid bone and adjacent surfaces of the midline septum bear olfactory epithelium in all mammals described to date. However, descriptions of diverse taxa (ungulates, carnivores, bats, insectivores, primates, and marsupials) indicate that some ethmoidal turbinals are partially covered by respiratory mucosa (Read, 1908; Negus, 1958; Loo, 1974; Bhatnagar and Kallen, 1975; Kumar et al., 1993, 2000; Rowe et al., 2005; Smith et al., 2007b). This variation in the mucosal distribution along ethmoidal turbinals and adjacent structures requires more detailed investigation (Smith et al., 2007a, b).
Turbinals and other structures that bear nasal mucosa vary enormously among mammalian taxa (Paulli, 1900; Moore, 1981). The evolutionary history of the lateral nasal wall is primarily inferred from comparative studies, which would indicate that marsupials have the primitive condition of five ethmoturbinals (Maier, 1993a). Moore (1981) suggests that, in carnivores and ungulates, the number of turbinals has increased by a splitting of the more posterior turbinals. However, Moore also questions whether the first ethmoturbinal (endoturbinal II in his terminology) is formed by means of union of two “originally quite separate endoturbinals” (1981, p 250). If certain turbinals have fused during evolution of the mammalian lateral nasal wall as suggested by Paulli (1900) and Moore (1981), using the primary lamina as criteria for nomenclature may be arbitrary. Due to postnatal elaboration of the ethmoidal labyrinth (Maier, 1993a), comparative studies of adult crania appear to hold little promise for understanding whether splitting or fusion occurred to produce the varying configurations among mammals. Although the sole use of developmental data to infer homology can be misleading (Hall, 1994), postnatal transformations of the nasal fossa in mammals are extensive and lead to divergent adult morphologies (Witmer, 1995). Thus, an understanding of the process by which the turbinals form during late embryonic and fetal stages is essential to clarify whether ethmoturbinals are autonomous elements during development. A neonatal mammalian “bauplan” has been described by Maier (1993a, b), who described several fetal strepsirrhines (1993b). At present, however, detailed, cross-sectional ontogenetic studies of the turbinals are lacking.
Here, we begin to address the need for further developmental and histological data on the primate nasal fossa. Species from the family Cheirogaleidae (mouse and dwarf lemurs) are studied. These primates may have ecological and behavioral similarities of the earliest primates (Cartmill, 1974). Each of these species feeds primarily in a fine-branch milieu to obtain insect and/or plant products. Furthermore, nocturnal cheirogaleids rely on olfaction as a crucial means of interspecific communication (Perret, 1992), and detection of certain food items (Siemers et al., 2007). The present study begins to address several uncertain aspects of primate nasal anatomy. First, ontogenetic transformations of the lateral nasal wall are assessed using a cross-sectional embryonic/fetal sample of Microcebus. A comparative sample of fetal nonprimate mammals is also studied to determine whether Microcebus spp. have a similar cartilaginous template from which the nasal fossa, particularly the ethmoturbinal complex, develops. A second focus of this study is on the distribution of nasal mucosa and structural associations in postnatal primates. Dimensions of the external midface in mammals are sometimes related to olfactory abilities, for example, the so-called “olfactory snouts” of strepsirrhine primates (Napier and Napier, 1967). Such an association hinges on the largely unexplored relationship between the protruding midface and internal topography of the nasal fossae. The present study provides a detailed account of mucosal distribution over internal osseous structures in a strepsirrhine primate, Microcebus murinus.
MATERIALS AND METHODS
- Top of page
- MATERIALS AND METHODS
- LITERATURE CITED
- Supporting Information
The present study describes development and mucosal lining of the nasal fossa in three genera from the family Cheirogaleidae, which are small bodied primates that possess moderately prognathic midfaces (Fig. 1a). Serially sectioned heads of mouse lemurs (Microcebus spp.; four adults, one neonate, nine embryos and fetuses) and dwarf lemurs (Cheirogaleus medius: two adults, two neonates; Mirza coquereli, two neonates) were studied. A fetal sample of two common tenrecs (Tenrec ecaudatus), one rodent (Microtus ochrogaster), and one dermopterid (Cynocephalus volans) were compared with fetal Microcebus to assess similarities and distinctions in the cartilaginous template for the nasal capsule.
Ontogenetic primate samples are challenging to obtain, and therefore most specimens were obtained opportunistically when neonatal (ages 1 to 2 days) or adult animals died of natural causes in captivity (Table 1). However, it must be mentioned that the precise fertilization age of “neonates” remains unknown. Some variations may be due to ontogenetic changes within a perinatal window. Likewise, precise ages for specimens in the comparative sample remain unknown, although all were previously estimated to be of fetal (Bhatnagar and Wible, 1994; Shimp et al., 2003) or perinatal ages (Smith et al., 2007c). The vole neonate was previously judged to be of perinatal size based on its crown-rump length (Smith et al., 2007c).
|Specimen no.||Figure(s)||Species||CRL (mm)||stage||source|
|MiSer. 7||4||Microcebus myoxinus (pygmy mouse lemur)||8||E15||B|
|MiSer. 19||M. myoxinus||9||E16||B|
|MiSer. 1*||4||M. myoxinus||13||E22/23||B|
|MiSer. 24||M. myoxinus||31||F||B|
|MiSer. 45*||13||M. myoxinus||32||F||B|
|MiSer. 71||Microcebus murinus (gray mouse lemur)||11||E20||B|
|MiSer. 54||5, 6||M. murinus||16||F||B|
|MiSer. 55*||6, 8, 12||M. murinus||28.5||F||B|
|MiSer. 53||M. murinus||33||F||B|
|P886/CM 116661||7, 8, 10, 11||M. murinus||41.4||N||DLC/CM|
|P384//CM 116670||Mirza coquereli (Coquerel's dwarf lemur)||69.4||N||DLC/CM|
|P623||Cheirogaleus medius (fat-tailed dwarf lemur)||57.2||N||DLC|
|InSer. 20*||12||Tenrec ecaudatus (Madagascar hedgehog)||22||F||B|
|InSer. 2*||13||T. ecaudatus||23.5||F||B|
|DUCEC804||12||Cynocephalus volans (colugo)||88||F||DU|
|VP104||12||Microtus ochrogaster (meadow vole)||25.3||N||SRU|
|P1845||2, 8, 10, 11||Microcebus murinus||4 y||DLC|
|P870||M. murinus||7 y||DLC|
|P1180/CM 116664||M. murinus||9 y||DLC/CM|
|P859/CM 116660||M. murinus||DLC/CM|
|P1442||Cheirogaleus medius||5 y||DLC|
Embryonic and fetal Microcebus specimens of the Bluntschli collection were studied at the American Museum of Natural History (Lozanoff and Diewert, 1989; Shimp et al., 2003). This collection included data cards with measures such as “total overall length,” which was roughly equivalent to crown-rump length (CRL) based on archived photographs of embryos/fetuses. The archived photographs revealed details about limb morphology (shape, presence of digital rays, etc.). Based on this information and internal features the Microcebus embryos were assigned Carnegie stages (O'Rahilly and Müller, 1987; Table 1).
The assessment of early nasal capsule maturation below is mostly based on the sample of Microcebus myoxinus, which comprises a greater number of embryonic stages. For comparison of nonprimates to primates, fetal specimens that possessed a completely chondrified capsule were selected to assess similarities and differences in the cartilaginous template or bauplan. In addition to images shown in the results section below, serial sectional levels can be viewed in primates and nonprimates at http://www.interscience.wiley.com/jpages/1932-8486/suppmat.
These specimens exist in several collections including those serially sectioned by the first coauthor and colleagues (Smith et al., 2007b, c), some of which are now housed at the Carnegie Museum of Natural History (Table 1). Selected specimens of the Bluntschli collection and one specimen from Duke University (Bhatnagar and Wible, 1994) were used to describe developmental aspects. Throughout the text, descriptions of the primate nasal structures apply to all species unless otherwise indicated. Otherwise, full genus and species names are frequently specified to avoid confusion at the genus level.
All specimens were previously paraffin-embedded and serially sectioned (10 to 40 μm). A variety of staining procedures were used, including Azan blue, hematoxylin-eosin, Gomori trichrome, Mallory's trichrome, and Alcian blue-periodic acid-Schiff. The details of preparation for serial sectioning were previously published (Lozanoff and Diewert, 1989; Shimp et al., 2003; Smith et al., 2004).
Structural Relations and Terminology of Nose and Nasal Fossa
Cheirogaleids, like most mammals, possess a moist hairless patch of skin that surrounds the nostrils, the rhinarium (Fig. 1a). The rhinarium has been related to primate chemoreception based on the continuity of a midline rhinarial groove with a passage leading to vomeronasal organ duct (Schilling, 1970; Martin, 1990; Rossie and Smith, 2007). The anatomy of the external nose and the vomeronasal organ in Microcebus has been carefully described in previous publications (Schilling, 1970; Smith et al., 2007a), and will not be considered further.
Comparative studies of the turbinals are made difficult by the numerous schemes of terminology used by different authors. For instance, one system of terminology identifies the turbinals closest to the septum as endoturbinals, and those positioned more laterally and deep to the endoturbinals as ectoturbinals (Paulli, 1900; Moore, 1981; or frontoturbinals—Maier, 1993a, b). Other authors have dispensed with the term endoturbinal and name the turbinals after the bones from which they project. These names reflect anatomical articulation in adults: The maxilloturbinal articulates with the maxilla and premaxilla, the nasoturbinal articulates with the nasal bone (and with the more posterior ethmoid to a variable extent), and one or more turbinals arise from the ethmoid—the ethmoturbinals. Authors differ in their treatment of the nasoturbinal, some referring to it as “endoturbinal I or ethmoturbinal I” (Paulli, 1900; Moore, 1981; Martin, 1990), whereas other authors consider the next, more posterior, turbinal as ethmoturbinal I (e.g., Le Gros Clark, 1959; Maier, 1993a).
In part, these differences in terminology vary according to fields of study, with human and veterinary anatomy each possessing its own standardized nomenclature (Warrick and Brookes, 1989 ; Nomina Anatomica Veterinaria, 2005). To facilitate a comparison of our findings with other published reports, Figures 1b and 2 and Table 2 explicitly assign the terminology used herein to internal structures of the nose. The major, that is, most medially projecting turbinals of the lateral wall of strepsirrhines present six distinct laminae, schematically shown in Figures 1b and 2. In Figure 2, the most dorsal and anterior turbinal (nasoturbinal) is arbitrarily denoted as “1,” and the remainder are numbered in a posterior direction. The reader is referred to Table 2 for nomenclature relating to these and other elements by various authors, and should refer to column 2 of Table 1 in regard to the present study. In particular, the reader should note numerous discrepancies exist for elements of the ethmoid complex (Table 2).
|Reference number (see Figure 2)||Terminology|
|Structure name (this study)||Humana||Other synonyms|
|1||nasoturbinal (entire)||see below||concha nasalis dorsalis (NAVb); endoturbinal I (Moore, 1981, Fig. 84)|
|1a||nasoturbinal, mucosal part||agar nasi||pars rostralis (NAV); nasoturbinal (Moore, 1981—p 49); nasoturbinate, anterior crus/cardinal concha IA (Pedziwiatr; 1972); agar nasi region of nasoturbinal (Kollmann and Papin, 1925)|
|1b||nasoturbinal, osseous part||semicircular crest and uncinate process are remnants||pars caudalis (NAV); ethmoturbinal I (Martin, 1990); nasoturbinate, posterior crus/cardinal concha IB (Pedziwiatr, 1972); endoturbinal I (Paulli, 1990); nasoturbinal, region of uncinate process (Kollmann and Papin, 1925)|
|2||maxilloturbinal||inferior nasal concha||concha ventralis (NAV) ; maxilloturbinate; ventral concha|
|3||ethmoturbinal I||middle nasal concha||concha media (NAV); ethmoturbinal II (Martin, 1990); endoturbinal II, upper lamella (Paulli, 1990; Moore, 1981); cardinal concha II (Pedziwiatr, 1972); endoturbinal I (Allen, 1882)|
|4||ethmoturbinal II||superior nasal concha||concha ethmoidalis(NAV); ethmoturbinal III (Martin, 1990); endoturbinal II, lower lamella (Paulli, 1990; Moore, 1981); cardinal concha III (Pedziwiatr, 1972)|
|5||ethmoturbinal III||?||concha ethmoidalis(NAV); ethmoturbinal IV (Martin, 1990); endoturbinal II (Paulli, 1990; Moore, 1981); cardinal concha IV (Pedziwiatr, 1972)|
|6||ethmoturbinal IV||?||concha ethmoidalis(NAV); ethmoturbinal V (Martin, 1990); endoturbinal III (Moore, 1981); cardinal concha V (Pedziwiatr, 1972)|
|7||semicircular crest||same||continuous with, and part of, structure 1b|
|8||frontoturbinal||ethmoid bulla||concha frontalis (Pedziwiatr, 1972); ectoturbinal (Moore, 1981)|
|9||frontomaxillary septum||–||lateral root of ethmoturbinal I (Rossie, 2006); anterior root of ethmoturbinal I (de Beer, 1937); horizontal lamina (Maier, 1993a)|
|10||interturbinal (after Maier, 1993b)||ectoturbinal (Paulli, 1900; Moore, 1981); accessory turbinal (Dieleux, 1906)|
|11||transverse lamina||ossiculum Bertini?||lamina terminalis (Kollmann and Papin, 1925; Hill, 1953)|
|w||lateral recess||recessus anterior (de Beer, 1937); maxillary sinus (Rowe et al., 2005, see Fig. 5 therein)|
|x||frontal recess||superior maxillary recess (Negus, 1958, p 313)|
|y||maxillary recess||inferior maxillary recess (Negus, 1958, p 313)|
|z||olfactory recess||sphenoethmoidal recess ethmoturbinal recess (Maier, 1993a); cupular recess (van Gilse, 1927); sphenoidal recess (Loo, 1973)|
Terminology of Development
We have argued elsewhere in support of a system that we believe most accurately reflects the homology of nasal structures (Rossie, 2003, 2006; Smith and Rossie, 2006). Subsequent to the formation of a nasal sac in the embryo, the walls of the nasal fossae first condense as mesenchyme, and then chondrify (Moore, 1981). De Beer (1937) considers this to occur in four regions: the anterior cupula, the posterior cupula (also called orbitonasal lamina), the paranasal cartilage (which joins the anterior and posterior cupulae), and the nasal tectum. Collectively, the elements of the lateral wall are referred to as the paries nasi (Fig. 3). The nasal tectum comprises superior, laterally projecting processes of the median cartilaginous septum and forms the “roof” of the nasal capsule. The bilateral paranasal cartilages and orbitonasal laminae have their own centers of condensation. The tectum, a bilateral projection of the median septal cartilage, is initially continuous with the anterior cupula (together, this is the parietotectal cartilage), but later forms bridges to the paranasal cartilage and posterior cupula. As chondrification proceeds, the articulation of these centers produces discrete elements. The posterior edge of the anterior cupula overlaps the paranasal cartilage internally producing a ridge within the nasal fossa—the semicircular crest. Similarly, the anterior edge of the posterior cupula overlaps the paranasal cartilages internally. The anterior projecting edge of the posterior cupula forms the first ethmoturbinal. Numerous authors consider the next turbinal in the posterior direction to be the ventral lamina of ethmoturbinal I (Seydel, 1891; Moore, 1981; Maier, 1993a, b; see Table 2 for alternate terminologies). The basis for this terminology is that the two scrolls anchor to a common primary lamina (Dieulafe, 1906; Moore, 1981). More posteriorly, additional ethmoturbinals arise and project medially from the ventromedial margin of the posterior cupula (de Beer, 1937). Accessory ethmoturbinals arise among (and are hidden by) the ethmoturbinals that reach the medial row. Interturbinals and epiturbinals are examples of these accessory scrolls (see below for definitions—Maier, 1993a, b). Conventionally, the entire ethmoturbinal complex of adults is considered to be a derivative of the posterior cupula of the nasal capsule (de Beer, 1937; Smith and Rossie, 2006). The nasoturbinal is considered as a distinct element that project anteriorly, but also overlaps the ethmoturbinal complex dorsally (a portion of the adult ethmoid bone forms the posterior part of the nasoturbinal—Moore, 1981). The maxilloturbinal forms as a remnant of the inferior part of the paries nasi.
Spatially, the cartilaginous wall of the nasal fossae may be divided into three segments, the pars anterior, pars intermedia, and pars posterior. This is a useful construct for discussion because it combines the nasal tectum with the lateral elements. Our discussion uses these descriptors, but we differ slightly from Moore (1981, p 252) who emphasized the use of the posterior projection of the anterior cupula (crista semicircularis) and the anterior projection of the posterior cupula (ethmoturbinal I) as “landmarks” separating the three parts. Herein, the three contributions of the paries nasi are emphasized as defining the tripartite organization (Fig. 3).
Histological Observations and Computerized Three-Dimensional Reconstructions
Due the small size of the animals and fragile nature of the internal nasal fossa, three-dimensional reconstructions and histological cross-sections were used to ascertain the general morphology of the internal nose. An adult and neonatal Microcebus murinus were selected for computer-based three-dimensional reconstructions and quantification of olfactory mucosa distribution. Both exhibited well-preserved epithelia, enabling the identification of transition points from olfactory to nonolfactory mucosa. Observations of Bowman's glands in the lamina propria and/or olfactory nerves were made to initially locate olfactory mucosa. Then, the rows of round nuclei of olfactory receptor neurons were identified and the transition point to a shorter, ciliated respiratory epithelium was identified under high magnification. The entire contour of the nasal mucosa was observed because patches of nonolfactory epithelium sometimes occurred, interrupting the continuity of olfactory mucosa. Examination of adults and neonates was made at high magnifications using a Leica photomicroscope (Leica Microsystems: Wetzlar, Germany) at ×400 to ×630. Fetal specimens were studied using a Microstar compound microscope (American Optical).
To acquire sections for reconstruction, the serial sections of each nasal chamber were digitally photographed using a Leica stereomicroscope at low magnification. Images were transferred to Adobe Photoshop 7.0 and saved as JPEG files. To reconstruct the nasal fossa of two of the fetal specimens from the Bluntschli collection, images were acquired using a digital camera with its lens held against the eyepiece of a Brock monocular microscope (Brock Optical, Sarasota, FL). Subsequently, individual files for every 20th (in adults) or 10th section (in infants) were marked according to fiducial landmarks (specific structures or contours) that delimit the olfactory mucosa. At the anterior and posterior ends, intervening sections were also marked in adults so that accuracy was comparable to that used for infants. The marked digital images were then aligned for reconstruction as described in detail by Smith et al. (2004).
Reconstructions of the nasal wall were made using Scion Image software (release 4.02, NIH). Four specimens of M. murinus (two fetal, one neonatal, and one adult animal) were selected to assess age related changes in the contours of the nasal fossa. To illustrate the lateral nasal wall, the septum was manually erased throughout the sequence of images using Scion Image. In one fetal specimen, deeper recesses were examined by erasing the anterior projection of ethmoturbinal I.
Four reconstructions of the neonatal and adult specimen were made. First, the entire nasal fossa and the nasal septum were reconstructed as two separate views. Next, only the olfactory portions of each were reconstructed using the same rotation coordinates in Scion Image. Images generated from these reconstructions were saved and then superimposed using Adobe Photoshop software to identify mucosal transitions for pictorial comparisons (see Smith et al., 2007b, or Rehorek and Smith, 2007, for more details). Next, selected reconstructed images were traced and rendered by hand to clearly emphasize contours while excluding artifactual imperfections of the sectioned tissues (e.g., folds or tears) that distort parts of the image.
Mucosal “Mapping” and Quantitative Methods
To obtain a measurement of olfactory SA in the neonatal and adult M. murinus, the perimeter of olfactory epithelium was measured in each section after calibrating to a digital image of a stage micrometer photographed at the same magnification. The initial cross-sectional level used for perimeter measurements was the first section in which a completely enclosed nasal fossa was found. For the posterior end-point, the last section containing the olfactory recess was used. Below the olfactory recess, the nasopharyngeal meatus continues as bilateral nasopharyngeal ducts for a variable distance in primates (Smith and Rossie, 2006). These ducts are at least partially separated by mucosa alone. Every perimeter measured was recorded in millimeters, and multiplied by the distance in millimeters to the next section, yielding a segment of olfactory surface area between sections. All segmental measurements were then summed and recorded as total olfactory surface area. The same process was repeated on the entire perimeter of the nasal fossa to obtain total surface area. Olfactory surface area was subtracted from total surface area to obtain nonolfactory surface area.
- Top of page
- MATERIALS AND METHODS
- LITERATURE CITED
- Supporting Information
General Structure of the Internal Nose
Three-dimensional reconstructions of the internal topography in adults reveal that the internal nose is most complex along the lateral wall, where six distinct mucosal folds or bulges project to a position adjacent to the midline septum (Figs. 1b, 2a–h). The internal nasal skeleton passes between the large, well-separated orbits (Fig. 2e–h). In combination, Figure 2 and Table 2 offer a detailed, illustrated list of the terminology used in this study. Only a brief summary of this morphology follows, because some of this anatomy has been previously reported in osteological descriptions (Kollmann and Papin, 1925; Hill, 1953; Cave, 1973; Ankel-Simons, 2007).
On the medial side of each nasal fossa is the nasal septum, nearly vertical in its contour except for small budges inferiorly in the anterior half (Figs. 2c–1e), corresponding to the vomeronasal complex. Also, there is a more posterior projection from the septum, supported by a portion of the vomer. At this level, the vomer projects laterally to join a medially projecting shelf of the ethmoid bone (Fig. 2h). This is the transverse lamina, which divides a solely respiratory pathway (the nasopharyngeal duct) from the more dorsal space (olfactory recess, in which olfactory mucosa predominates) (Fig. 2h; see below). The lateral wall is much more irregular. The most medially projecting elements comprise the maxilloturbinal, nasoturbinal, and four scrolls from the ethmoid complex: the ethmoturbinals. The nasoturbinal is not a continuously pronounced ridge from its anterior to posterior extent (see Fig. 2c–f). However, at both anterior and posterior ends, this turbinal corresponds to the lateral extent of the cartilaginous nasal tectum, which retreats from the nasoturbinal fold anteriorly and ossifies posteriorly in the adult (see below for related developmental observations).
Prenatal Development of the Internal Nose
Mesenchymal condensations are the earliest signs of the cartilaginous capsule, as shown in the smallest embryonic specimen examined (8 mm CRL Microcebus myoxinus; Fig. 4). The paries nasi of the capsule are continuous with the tectum anteriorly, but they are discontinuous posteriorly. A separation first appears at the anterior limit of the primary choanae, where the paries nasi is separated from the tectum (Fig. 4a). The tectum itself is continuous with the median condensation for the nasal septal cartilage until the level of the pars intermedia (this position is marked by the presence of the primitive frontal recess [Fig. 4b]). From this point posteriorly, there is no distinct condensation of the tectum, although the median septal (mesethmoid) condensation continues (Fig. 4b,c). Condensations for the pars posterior are indistinct in the 8-mm CRL Microcebus myoxinus (Fig. 4c), but have commenced in the 9-mm CRL specimen (MiSer. 19). In both 8-mm and 9-mm CRL M. myoxinus, some lateral bridging exists between the pars anterior and pars intermedia. In a larger specimen (13 mm CRL M. myoxinus, Fig. 4d–f) chondrification is complete in the nasal septum, paries nasi, and the nasal tectum. Lesser-developed elements are found internally, where the semicircular crest and anterior tip of ethmoturbinal I are represented by condensed mesenchyme (Fig. 4d). A cartilaginous nasal tectum and paries nasi are continuous from the level of the pars anterior (not shown) to the intersection of pars intermedia and pars posterior (Fig. 4e). Ethmoturbinals II through IV are incompletely developed. Ethmoturbinal II is represented by a mucosal fold supported by a moderately pronounced medial bulge in the paries nasi (Fig. 4e). Ethmoturbinal III exists as condensed mesenchyme in this specimen (Fig. 4f), and no trace of Ethmoturbinal IV is observable.
Figure 5 shows a three-dimensional reconstruction of the nasal capsule and surrounding structures in a 16-mm CRL Microcebus murinus. The pars anterior, pars intermedia, and pars posterior, are difficult to delineate externally, except that the pars intermedia is an external bulge of the capsule (Fig. 5a–d). The pars posterior is directly adjacent to the orbits (Fig. 5a). Figure 5e emphasizes the close relationship of the ethmoturbinals of the pars posterior to the cribriform plate.
Divisions between the portions of the tripartite capsule are best visualized internally. Figure 6a displays a transverse view of the nasal capsule in the same fetus as in Figure 5. The capsule appears to be in a more advanced state of maturation compared with the specimen described in Figure 4d–f, because the semicircular crest and ethmoturbinals II and III have fully cartilaginous projections within the mucosal folds. In this specimen, ethmoturbinal IV is visible, although only as a mucosal bulge. Figure 6a also illustrates the intersection of the three anteroposterior “segments” of the capsule. The pars anterior folds inwardly relative to the pars intermedia, and projects posteriorly as the semicircular crest. Similarly, the pars posterior folds inward relative to the pars intermedia, and projects anteriorly as ethmoturbinal I. Note that the semicircular crest and the anterior free margin of ethmoturbinal I form the medial wall of the lateral recess (Fig. 6a). Larger fetuses, such as the 28.5-mm CRL M. murinus, possess a full set of turbinals (Fig. 6b), which all have internal cartilaginous support (Fig. 7a–d). Figure 6b is a drawing based on a computer three-dimensional reconstruction of the lateral wall of this specimen, after the anterior projection of ethmoturbinal I was digitally “dissected away” using Scion Image software. The intersection of the three parts of the nasal capsule is mostly revealed. The semicircular crest obscures the anterior limit of the anterolateral recess (i.e., the portion of the lateral recess bordered medially by overlap with the pars anterior). More posteriorly in the lateral recess, the cut edge of the frontomaxillary septum (“lateral root” of ethmoturbinal I) is seen. This horizontal shelf effectively divides the lateral recess into a frontal recess (superiorly) and maxillary recess (inferiorly). Here, this portion of the lateral recess is termed the posterolateral recess (i.e., the portion of the lateral recess bordered medially by overlap with the pars posterior).
Morphology of the Nasal Capsule in Three Neonatal Cheirogaleids
Neonates of three cheirogaleids (Microcebus murinus, Mirza coquereli, and Cheirogaleus medius) are similar anteriorly, throughout the pars anterior (not shown). The anterolateral recess (the portion of the lateral recess bordered medially by overlap with the pars anterior) similarly has a thick glandular lamina propria ventrally in all species (Fig. 7a,e,f). A major distinction among species is the number of frontoturbinals in the frontal recess. Microcebus murinus has one, whereas Mirza coquereli and C. medius each have two (Fig, 7b,f,i). These differences are also seen in comparisons of adult Microcebus murinus and C. medius. Frontoturbinal 1, the nasoturbinal, and ethmoturbinal I are all more robust in neonates of Mirza coquereli and C. medius compared with Microcebus murinus. In the neonatal Mirza coquereli, there is a third, dorsally positioned bulge in the mucosa and underlying cartilage, suggestive of a rudimentary frontoturbinal. All three species are similar throughout the pars posterior (Figs. 7c,d,g,h,k,l).
Prenatal to Postnatal Transformations of the Lateral Nasal Wall
Figure 8 shows renderings drawn from three-dimensional computer reconstructions of the right side of the nasal fossa in a fetal to adult series of Microcebus murinus. Anteriorly, reconstructions begin at the level of the marginoturbinal. Posteriorly, the reconstructions end just anterior to the end of the olfactory recess. The median nasal septum is removed to reveal the medial surface of the lateral wall. Figure 8a shows a reconstruction of a 28.5-mm CRL fetus. In this specimen, all ethmoturbinals are supported internally by cartilage (Fig. 7a–d). The nasoturbinal is a pronounced ridge anteriorly and posteriorly, but is poorly defined in the region of the anterolateral recess (cf. Fig. 12a). Here, the semicircular crest continues into the posterior part of the nasoturbinal. The maxilloturbinal is largest anteriorly, and tapers to a small ridge at the level of ethmoturbinal II. The frontal recess is small, with a single prominent frontoturbinal. All four ethmoturbinals project anteriorly from their ventral attachments to the lateral nasal wall. Ethmoturbinal IV is proportionally enlarged relative to the size of the same turbinal in the 16-mm CRL fetus (cf. Fig. 5e), and is the sole visible structure in the olfactory recess (demarcated by the floor of this space, the transverse lamina, Fig. 8a). Figure 8b shows the same view in a neonatal Microcebus murinus. The most notable distinction of this specimen compared with the smaller fetus is the proportional elongation of ethmoturbinal I. In the adult nasal fossa (Fig. 8c; 4-year-old M. murinus), the anterior third of the nasal fossa is spatially packed with proportionally larger turbinals. The maxilloturbinal and ethmoturbinal I are the major elements in this region, while the nasoturbinal remains a small ridge. Relative to the neonatal specimen (Fig. 8b), all ethmoturbinals are proportionally larger on their anterior margin, but ethmoturbinals I and IV appear to be the most enlarged. In the adult, ethmoturbinal I projects to overlap the majority of the maxilloturbinal and also obscures all but a small aperture of the frontal recess. Ethmoturbinal IV is elongated in both anterior and posterior directions from its dorsal attachment. Relative to fetal and neonatal specimens, the adult maxilloturbinal is enlarged dorsally, to lie closely adjacent to the nasoturbinal and ethmoturbinal I. The maxilloturbinal is also enlarged posteriorly relative to younger specimens. Note that this turbinal is proportionally elongated to overlap at least part of all turbinals. In part, this is related to a free posterior projection, which tapers toward the nasopharyngeal duct (cf. Fig. 2g).
Distribution of Olfactory and Nonolfactory Mucosae Along the Walls of the Nasal Fossae
Figures 9 to 11 provide a pictorial summary of the distribution of mucosa along the walls of the nasal fossa in C. medius and Microcebus murinus. At the level of the marginoturbinal (Fig. 9a, adult C. medius), mostly stratified epithelia is found but small patches of ciliated epithelium are found associated with subepithelial glands (Fig. 9b,c). The marginoturbinal is continuous posteriorly with the maxilloturbinal (Fig. 9d). Septal and lateral nasal gland masses are associated with the nasal septum and nasoturbinal, respectively (Fig. 9d). These glands are PAS+/Alcian blue−. At this level (approximately 1.5 mm posterior to Fig. 9a), respiratory epithelium (ciliated, pseudostratified, or simple columnar) covers most of the septum, lateral nasal wall, and portions of the maxilloturbinal. Alcian blue+ goblet cells are numerous in this epithelium (Fig. 9d). Aside from the floor of the nasal fossa (not shown), which is mostly covered with stratified epithelium, respiratory mucosa covers most of the anterior third of the nasal fossa.
Olfactory epithelium first appears as small patches along the roof and/or septum of the nasal fossa and the dorsal rim of ethmoturbinal I (Fig. 9e,f; at the level of the anterolateral recess). The patch along the roof or septum extends somewhat more anteriorly than the olfactory mucosa of ethmoturbinal I, especially at birth (Figs. 10, 11, Microcebus murinus). The first 0.5 to 0.8 mm of the anterior projection is entirely nonolfactory in adult Microcebus murinus.
The anterolateral recess is mostly filled with glandular lamina propria, covered with ciliated epithelium with goblet cells (Fig. 9g,h). A small patch of olfactory epithelium extends into the apex of the anterolateral recess, just anterior to the beginning of the frontal recess. The proportionally extensive anterior distribution of respiratory mucosa on ethmoturbinal I was previously described in cheirogaleids (Smith et al., 2007b). The adjacent maxilloturbinal is only partly ciliated. Generally, the convex surface of the scroll is nonciliated and highly vascular, whereas it concave aspects are covered with ciliated epithelium with goblet cells (Fig. 9i).
In the posterior half of the nasal fossa, olfactory mucosa covers the majority of surfaces of all turbinals excluding the maxilloturbinal (Figs. 9j–o; 10a,b). The frontal recess of C. medius houses two frontoturbinals (Fig. 9j,k). A portion of all frontoturbinals and ethmoturbinals is lined with at least some nonolfactory mucosa, even within the olfactory recess (Figs. 9l,o).
Olfactory Mucosa Distribution
Table 3 and Figures 10 and 11 provide quantitative and pictorial accounts, respectively, of the olfactory versus nonolfactory mucosa that lines the nasal fossae in one neonatal (Figs. 10a, 11a) and one adult (Figs. 10b, 11b) Microcebus murinus. Calculations of surface area (SA) of olfactory and nonolfactory mucosae, as well as three-dimensional reconstructions indicate that the nasal fossa is lined with proportionately more olfactory mucosa in the neonatal specimen (38%) compared with the adult (31%). This difference is more evident in the nasopharyngeal chamber, where the neonatal nasal fossa had approximately 41% olfactory SA, compared the 25% in the adult. Based on three-dimensional reconstructions, half or more of the nasal septal mucosa is olfactory. Passing toward the olfactory recess, the extent of olfactory mucosa is greater, ending at the level where the vomer projects its bilateral choanal processes (Fig. 11).
|Structure/ space for surface area (SA) measurement||Adult SA (mm2)||Neonatal SA (mm2)||Adult/neonate ratio|
|Total nasal fossa||372.6||65.09||5.7|
|Total OE in nasal fossa||113.8||24.8||4.6|
|olfactory recess OE||19.6||2.1||9.4|
|nasopharyngeal chamber total area (incl. recesses)||294.6||55.5||5.3|
|nasopharyngeal chamber OE||73.6||22.7||3.2|
|lateral recess, total area||64.2||11.5||5.6|
|OE in lateral recess||27.3||5.5||4.9|
|ET I: total area||40.4||3.2||12.7|
|ET I: OE||14.2||2.4||6.0|
|ET I: Non-OE||26.2||0.8||32.0|
|ET II: total area||13.2||1.3||9.9|
|ET II: OE||7.0||1.1||6.6|
|ET II: Non-OE||6.2||0.3||22.4|
|ET III: total area||11.0||1.3||8.0|
|ET III: OE||6.1||1.0||6.0|
|ET III: Non-OE||4.6||0.3||14.7|
|ET IV: total area||18.3||1.2||15.9|
|ET IV: OE||8.4||08||10.8|
|ET IV: Non-OE||9.9||0.4||26.4|
|maxilloturbinal: total area||79.1||5.7||13.8|
|frontoturbinal: total area||12.7||1.2||10.7|
Olfactory mucosa covers dorsoposterior portions of the nasoturbinal and ethmoturbinals. The nasoturbinal was not quantified separately because it is indistinct for a portion of its anterior half (see Fig. 2e). Three-dimensional reconstructions revealed that the most anterior glandular portion is entirely covered with nonolfactory mucosa, whereas the part posterior to the semicircular crest is entirely olfactory (Fig. 10). All turbinals possess some nonolfactory mucosa and a greater proportion of nonolfactory SA is found in adults (Fig. 10b). Quantitative results support this observation (Table 3). Moreover, the maxilloturbinal has the greatest overall adult/neonatal ratio in SA of the turbinals outside the olfactory recess (Table 3).
The posterior part of the upper nasal fossa is separated from the nasopharyngeal ducts by the transverse lamina (posterior 25% of the nasal fossa in neonate and posterior 22% in adult Microcebus murinus); a partial separation is created anteriorly by the choanal process of the vomer. Only ethmoturbinal IV is completely enclosed within the olfactory recess. This turbinal has proportionally the greatest amount of olfactory SA at both ages and has the greatest overall adult/neonatal ratio in SA of all ethmoturbinals (Table 3).
The posterolateral recess has olfactory mucosa in the enclosed frontal recess, and more anteriorly before the frontomaxillary septum attaches (not shown; cf. Fig. 9j,k). The percentage of olfactory SA in the entire lateral recess is somewhat lower in the adult (43%) compared with the neonatal Microcebus murinus (48%). The single frontoturbinal of the Microcebus murinus has an adult/neonatal ratio in SA that exceeds ethmoturbinals II and III.
These SA data include some surfaces that would not be discernable in osseous specimens, such as the first enclosed cross-sections of the nasal fossa as well as the posterior-most cross sections of the nasopharyngeal ducts. Each of these regions has some borders formed by soft tissue alone. To generate results that could be applied to osseous specimens, surface areas were also calculated in the adult Microcebus murinus using osseous landmarks. For this measurement, the start point of the nasal fossa is the first section in which the right nasal passageway is completely enclosed by bone. The end point is the last section in which the nasopharyngeal ducts are completely divided by the vomer. Using these landmarks, the total mucosal SA of the nasal fossa is 362.1 mm2, of which 113.8 mm2 (31%) is olfactory mucosa.
Comparative Morphology of the Internal Nose During Late Fetal/Neonatal Development
A comparison of sectioned material from late fetal/neonatal mammals is provided in Figure 12, including coronal sections of a Microcebus murinus (Fig. 12a–e), Cynocephalus volans (Fig. 12f–j), Tenrec ecaudatus (Fig. 11k–o), and Microtus ochrogaster (Fig. 12p–t). A basic similarity exists in organization of the ethmoturbinal complex among these species. Specifically, ethmoturbinal I projects anteriorly to overlap the pars intermedia, and posteriorly three additional cartilaginous elements (ethmoturbinals II–IV) project to a position adjacent to the nasal septum. In contrast to ethmoturbinal I, which represents an anterior projection of the orbitonasal lamina itself, the posterior three elements each have an attachment to the ventral margin of the pars posterior. Ethmoturbinals III and IV also have more posterior attachments to the roof of the capsule in all species, and ethmoturbinal II has a mucosal root near the intersection of the nasal tectum and ethmoturbinal I. Ethmoturbinal I shows subtle variations in contour (Fig. 12b,g,j,q). All species have two frontoturbinals except Microcebus spp., which possesses a single scroll within the frontal recess (Fig. 12a–c). All possess interturbinals lateral to ethmoturbinal III (Fig. 12d,i,n,s). Major distinctions exist between the Microtus ochrogaster and the other three mammals. In Microtus ochrogaster, the transverse lamina more extensively overlaps the ethmoturbinal complex, encapsulating ethmoturbinals III and IV within the olfactory recess (Fig. 12s,t). In Microcebus murinus, Cynocephalus volans, and Tenrec ecaudatus, only ethmoturbinal IV is completely enclosed in the olfactory recess (Fig. 12e,j,o). More anterior distinctions include a relatively smaller maxilloturbinal in Microtus ochrogaster (not shown, also see Adams, 1972). Additionally, the anterior part of the nasoturbinal has cartilaginous support in Microtus ochrogaster (not shown here), while in the other mammals it is only a mucosal, glandular bulge (as in the adult Microcebus murinus, Fig. 2c).
Figure 13 shows roughly horizontal sections through fetal heads of a 32 CRL Microcebus myoxinus (Fig. 13a–d) and a 23.5 CRL Tenrec caudatus (Fig. 13e–h). Each series of sections progresses from ventral to dorsal through the ethmoturbinal complex. The nasal capsules are in a similar state of maturation, in that all ethmoturbinals have fully developed cartilaginous supports. This view reveals that ethmoturbinal I is a direct continuation of the orbitonasal lamina (i.e., the lateral wall of the pars posterior) that projects anteriorly, overlapping the semicircular crest (Fig. 13a–c,e–g). In this view, the more posterior ethmoturbinals are seen to be growths from the medial aspect of the orbitonasal lamina. Each species can be seen to have two interturbinals between ethmoturbinals II and III, although they are somewhat smaller in Microcebus murinus (Fig. 13b,f). Figure 13d,h is near the cribriform plate, a proportionally larger frontal recess is seen in Tenrec ecaudatus (Fig. 13h) compared with Microcebus murinus (Fig. 13d).
- Top of page
- MATERIALS AND METHODS
- LITERATURE CITED
- Supporting Information
Functional interpretations of superficial (e.g., midfacial prognathism) and minute details (e.g., turbinal size and number) of extant and fossil primate noses hinge, in part, on a detailed knowledge of the inner mucosal lining (Smith et al., 2007a). Recent studies show that evolutionary patterns related to chemosensory structures can be inferred from fossil material (Hillenius, 2000; Bush et al., 2004; Kay et al., 2004; Rossie, 2005). Although evidence is sometime indirect, osteological morphology can yield estimates of the size of soft tissue structures (Bush et al., 2004; Kay et al., 2004). Observations on the nasal fossa of fossil primates are hampered by the paucity of well-preserved material. However, some adequate material exists (see Smith and Rossie, 2006; Smith et al., 2007a), and more data will likely be uncovered (Kay et al., 2006). The details provided here, on the association between internal osseous nasal structures and mucosa in two cheirogaleids primates, are intended to inform such future studies.
Ontogeny of the Nasal Template
The prenatal Microcebus sample of the Bluntschli collection was opportunistically collected more than 70 years ago, and no information on precise ages of the embryos and fetuses can be gleaned. However, this collection has been used to demonstrate graded characteristics of the solum nasi (Lozanoff and Diewert, 1989) and nasopalatine ducts (Shimp et al., 2003) of specimens with differing CRL. Because Microcebus myoxinus dominates this sample, the bulk of interpretations of early stages of development are based on this species. Because the 13 mm CRL M. myoxinus (MiSer. 1) was previously assessed as a Carnegie Stage 22/23 embryo (also see Lozanoff and Diewert, 1989), it can be used to approximate that state of maturation at the end of the embryonic timeframe. Figure 14a,b is a schematic diagram illustrating the maturation of the tectum and paries nasi, respectively. The top row is based on observations of 8- and 9-mm CRL Microcebus myoxinus (Stage 15–16 embryos). The middle row represents the stage of maturation at the transition from embryonic to fetal periods. The bottom row is based on the fully chondrified capsules in fetuses of both M. murinus and M. myoxinus.
The tripartite organization of the mammalian paries nasi, beginning with three separate centers of mesenchymal condensation, is a common theme of morphogenesis (de Beer, 1937) with few known exceptions (Zeller, 1987). Because the ensuing maturation and growth of these centers varies among higher taxa (Zeller, 1987), early nasal capsule development of the mouse lemur is of interest. The specimens examined in this study suggest several spatial trends in development of the nasal capsule. The nasal tectum develops in an anteroposterior and mediolateral direction (Fig. 14a, top, middle). A bridging of the tectum to the paries nasi is first apparent anteriorly, as the parietotectal cartilage condenses (Fig. 14a, middle), as described for amniotes generally (de Beer, 1937). More posteriorly, it appears that the paranasal cartilages begin to form laterally and then progress toward the tectum, based on comparison of embryos of different sizes. The mesenchymal condensations of the orbitonasal lamina and paranasal cartilages begin to overlap relatively early by virtue of the extension of ethmoturbinal I (14a,b, middle row). A schematic view of the full roof is shown in 14a (bottom).
In Figure 14b the paries nasi is shown with the tectum removed. The nasal capsules of the smallest Microcebus myoxinus suggest that the condensations for the orbitonasal lamina appear after those for the paranasal cartilages. The pars intermedia becomes overlapped internally by the anterior margin of the par posterior and the hind edge of the pars anterior by virtue of additions of condensing mesenchyme. Ethmoturbinal I and the semicircular crest are formed in this manner, by means of advancing streams of condensing mesenchyme (Fig. 14b, middle). Ethmoturbinals II to IV form in an anteroposterior sequence, as inferred from prenatal Microcebus myoxinus and Microcebus murinus (see Figs. 4f and 6a, respectively). Specimen MiSer. 54 (Microcebus murinus) had a slightly more advanced maturation of the pars posterior, with a chondrified ethmoturbinal III, but only a mucosal bulge for ethmoturbinal IV.
Ontogeny of the Lateral Wall
Two clear ontogenetic trends are suggested by the cross-sectional sample of fetal, neonatal and adult Microcebus murinus. First, there is a disproportionate increase in dimensions of the anterior part of the nasal fossa, with expansion of the maxilloturbinal and the adjacent nasal fossa wall (mostly the viscerocranial maxillary and nasal bones). Based on reconstructions in Figure 8, ethmoturbinal I may advance in anterior length at an even faster pace. This differential growth may begin in the late fetal period. Three-dimensional “maps” of the mucosa and quantitative findings indicate that this expansion of surface area involves mostly nonolfactory portions (Fig. 10). Whereas this study did not quantify respiratory mucosa, the preponderance of respiratory mucosa on nonolfactory parts of ethmoturbinal I (Smith et al., 2007b) and the mucosa of the maxilloturbinal (see below) suggests that the growth in these anterior regions augments air-conditioning capacity.
The second trend is seen posteriorly. While all ethmoturbinals become anteriorly elongated, the first and fourth increase disproportionately. This is evidenced most plainly by the posterior elongation of ethmoturbinal IV, wherein a free projection elongates in tandem with a posteriorly expanding olfactory recess (see Fig. 8).
The quantitative comparisons support these impressions of differential growth, because ethmoturbinals I and IV have the highest of the adult/neonatal specimen ratios (see Table 3). If the neonatal specimen is typical in dimensions for a newborn Microcebus murinus, and the adult is typical for its age, the differences suggest clear trends in postnatal growth. First, the disproportionate growth of nonolfactory portions of ethmoturbinal I in Microcebus murinus (Smith et al., 2007b) appears to be part of a trend throughout the entire nasal fossa. There is a decrease in olfactory SA of nearly 10% between neonatal and adult ages. Second, when the nasal fossa is divided into two regions, the olfactory recess and the remainder, the changes in SA indicate reverse trends in growth. The olfactory recess increases its olfactory SA by nearly 45%, while the remainder of the nasal fossa decreases by more than 15% in olfactory SA. In the intermediate region of the nasal fossa, quantitative observations and three-dimensional reconstructions suggest that the anterolateral recess and ethmoturbinals II and III expand at a rate more commensurate with overall nasal fossa growth. These apparent patterns are interpreted as growth trends with caution, because these represent the first detailed quantifications of the entire nasal fossa and its components in a primate. Future analyses of other taxa are sorely needed.
Internal, Osseous Nasal Structures and Spaces: Identification and Physiological Associations
The terminology in this report, largely derived from Maier (1993a, b) is specifically useful for ontogenetic and evolutionary analyses of the mammalian nasal fossa. The most numerous irregularities in terminology in Table 2 relate to turbinals. While some terms may be interchangeable with little chance of confusion (e.g., frontoturbinal/ectoturbinal), some specific practices have been problematic
First, the use of Maier's terminology (1993a, b) is advocated with respect to the “accessory” ethmoidal turbinals. Frontoturbinals or ectoturbinals are those nested within the frontal recess. Accessory ethmoturbinals arising more posteriorly include interturbinals and epiturbinals. The former arise from the medial wall of the orbitonasal lamina, between (and covered medially by) ethmoturbinals. Epiturbinals are accessory scrolls of the ethmoturbinals themselves. Developmentally, frontoturbinals are products of the pars intermedia while interturbinals and epiturbinals derive from the pars posterior. This system resolves confusion in terms of simple descriptive anatomy and potential issues regarding homology. A drawback in the practice of collectively referring to all of these elements as “ectoturbinals” (Paulli, 1900) is that they are clearly not serial homologues.
Second, it is argued here that the practice of describing ethmoturbinal I as a bipartite structure (see Table 2) is arbitrary. Ethmoturbinal I is the most anterior medially positioned scroll of the ethmoid bone, and at the same time, the most anterior limit of the orbitonasal lamina. The next ethmoidal scroll in posterior procession is an independent element arising from the ventromedial margin of the orbitonasal lamina, as discussed further below. Historically, this issue has already been raised, for different reasons. Kollmann and Papin (1925), citing Seydel (1891), also found the practice of combining the first two medial scrolls into a composite structure as problematic. Based on embryology of the human nasal fossa (“...il y a plus d'ethmoïdaux chez l'Hommme qu'on croyait...” —p 5), they argued that that the practice of combining these elements is an unnecessary construct, used to render easier the comparisons of some anthropoids to lemurs. Accordingly, Kollmann and Papin considered the series of (ethmo) turbinals as separate elements (“...suffisamment invidividualisée.” —p 5).
The nasoturbinal is among the most problematic internal structures in terms of nomenclature (see Table 2). This may partially relate to differing preferences among authors, but taxonomic variation may also contribute. For example, the anterior portion of this turbinal encloses elements of the lateral nasal gland, which create a visible mucosal fold. There is no well-defined osseous ridge supporting this fold in any species under study (e.g., see Figs. 2c, 9a). However, in some other primates, the nasal bone projects a turbinal crest inward in the region of this mucosal fold (e.g., lorisoids—Kollmann and Papin, 1925). In at least some insectivores, an osseous turbinal is adjacent to the lateral nasal gland duct (see Fig. 1 in LaRochelle and Baron, 1989). More problematic is the large anteriorly positioned osseous turbinal in rodents, commonly identified as the nasoturbinal (Adams, 1972 ; Clancy et al., 1994; Jurcisek et al., 2003), which is directly continuous with the ossified nasal tectum. The homology of these structures with the glandular part of the nasoturbinal, as defined here, is uncertain. It is beyond the purpose of this study to resolve this issue, and we are following Moore (1981) who used the entire structure defined here as synonymous with the nasoturbinal. However, a careful reconsideration of the variation and development of different segments of the nasoturbinal is needed
In cheirogaleids, the nasoturbinal may be traced in development by following the lateral margin of the nasal tectum. Anteriorly, the lateral nasal gland mass is located on the medial margin of the tectum. The tectum has disappeared from this position in adults (Fig. 2c). Passing posteriorly, the lateral part of the tectum continues as the semicircular crest (see Fig. 7a), which then becomes attenuated dorsally (see Fig. 7b). These structures ossify as dorsolateral walls of the ethmoid bone. The mucosal characteristics show that the glandular part of the nasoturbinal bears respiratory mucosa. In the osseous part, the dorsal part of the semicircular crest and the entire posterior part of the nasoturbinal bear olfactory mucosa. An extension of mucosa from the ventral part of the semicircular crest that is unsupported by bone (see Figs. 7a, 9g) reveals mucosal surfaces that would be difficult to infer from osseous structures alone. This creates extra mucosal surface, and contains glands of the lateral recess.
The maxilloturbinal ossifies from the inferior margin of the paries nasi, as described previously in other mammals (de Beer, 1937; Moore, 1981). Observations of the mucosal covering indicate that the medial convex surface is important for regulating temperature during respiration, based on the presence of numerous venous sinuses. A ciliated epithelium with unicellular glands is mostly restricted to the lateral concave surface, which may be more important for air filtration
The ethmoid bone ossifies from portions of all three components of the fetal capsule, the pars anterior (semicircular crest), pars intermedia (walls of the frontal recess, frontomaxillary septum, frontoturbinal[s]), and the pars posterior (ethmoturbinal complex, posterior nasal tectum, lateral part of transverse lamina)
The ethmoturbinal complex is the primary derivative of the orbitonasal lamina of the pars posterior. Ethmoturbinal I is a rostrally prolonged extension of the orbitonasal lamina of the pars posterior. The remaining ethmoturbinals project ventromedially from the orbitonasal lamina. Progressing posteriorly, the lamina transversalis posterior forms the lateral part of the transverse lamina. It resembles the ethmoturbinals as the posterior-most ventromedial projection in the sequence. As such, the lamina transversalis posterior could be the homolog of the last ethmoturbinal of metatherians. In fact, the last ethmoturbinal in the opossum forms part of the floor of the olfactory recess (see “ethmoid plate,” Fig. 6, in Rowe et al., 2005). It is not precisely clear at this time how the ethmoturbinals of the opossum correspond with that of Microcebus. A bipartite “endoturbinal I” was described by Rowe et al. (2005; Fig. 10), corresponding to the sequence assigned as ethmoturbinals I and II here. Although this may indicate six ethmoturbinals in the opossum, the scroll identified as “endoturbinal III” by Rowe et al. (2005, Fig. 6) does not appear to occupy the medial row, and may correspond to an interturbinal according to the terminology of Table 2. Further comparative work is required to establish developmental equivalence of ethmoturbinals between metatherian and eutherian mammals.
Notwithstanding that all turbinals do derive from the nasal capsule (a basis for more inclusive terminology per Rowe et al., 2005), all ethmoturbinals have two common characteristics. First, all develop from the pars posterior (which also does provide partial origin for the nasoturbinal). Second, all of these turbinals are distinctly and wholly part of the adult ethmoid bone. Therefore there is both a developmental and anatomical basis for referring to the four posterior turbinals in the medial row as “ethmoturbinals.”
Our preference to consider the first two ethmoturbinals as sequentially distinct elements is based on the developmental observation that the so-called ventral lamina of ethmoturbinal I is one of three or more invaginations from the inner surface of the pars posterior. This agrees with Maier's (1993b) descriptions of individual fetuses of Microcebus and Galago. In Daubentonia, ethmoturbinal I projects farther into the nasal fossa at birth compared with these species (Maier, 1993b). Maier's diagram of the ethmoidal labyrinth appears to show a distinct division of this turbinal into two laminae, but without a series of prenatal stages, it is difficult to discern whether this turbinal divides or is at a more advanced stage of morphogenesis compared with his descriptions of Microcebus and Galago. We argue that the mammalian bauplan described by Maier (1993a) similarly shows that the “ventral lamina of ethmoturbinal I” is simply the first of a sequence of turbinals that grow from the inner face of the pars posterior. This argument may seem semantic, but it resolves some problems in comparative morphology. Although the second ethmoidal turbinal does partially merge (postnatally) with the most anterior ethmoidal turbinal and share a common primary lamina (a distinct lateral root—the frontomaxillary septum), it also diverges from this lamina to anchor into the lateral wall of the nasal fossa by its own distinct root. In cheirogaleids, this separate root is posterior to its union with the first ethmoturbinal (after the latter merges with the roof of the nasal fossa—Fig. 2g). In rodents, the second ethmoturbinal is distinct anterior to its union with the first ethmoturbinal (Adams, 1972; Clancy et al., 1994).
The notion of a bipartite ethmoturbinal I is rendered questionable by the above information. In summary, the second ethmoidal turbinal can be termed ethmoturbinal II based on the following points. First, it is developmentally identified as one of three distinct structures on the medial face of the pars posterior. Second, ethmoturbinal I is distinct from ethmoturbinals II–IV because it is the continuation of the orbitonasal lamina of the pars posterior. Last, although ethmoturbinal II has the most anterior emergence from the pars posterior, its association with the first ethmoturbinal in the sequence is variable.
This plate of bone, a result of fusion between the lamina transversalis posterior and the lateral (choanal) vomerine processes, creates a blind-ended olfactory recess dorsal to the nasopharyngeal ducts. The arrangement appears to be primitive for therian mammals because the plate of bone is present in metatherians and numerous eutherians (Negus, 1958), and its presence has been asserted in at least one Triassic mammal (Kielan-Jaworowska et al., 2004). The comparative sample of this study suggests some developmental variations. Of particular note is the differing anteroposterior extent of the transverse lamina in Microtus ochrogaster compared with all others. The rodent exhibits a common condition among mammals. In cats (Negus, 1958) and dogs (Craven et al., 2007), multiple ethmoturbinals are enclosed in the olfactory recess. Negus (1958) noted that the transverse lamina (which he termed the “subethmoid shelf”) is present in marsupials, felids, and canids, among others, but is small in rodents and ungulates. He also considered it absent in primates, although numerous studies have since contradicted this (Maier, 1993b; Smith et al., 2004). The extent of this plate may relate directly to segregation of turbinal physiology. Craven et al. (2007) describe ethmoturbinals of the dog to be predominantly lined with olfactory mucosa. Furthermore, in canids and felids there is less overlap of the maxilloturbinal by the first ethmoturbinal projection (see Fig. 99 in Negus, 1958; Fig. 3 in Craven et al., 2007). By comparison, some strepsirrhine primates (e.g., cheirogaleids and galagids—Kollmann and Papin, 1925; Smith et al., 2007b), at least some bats (Bhatnagar and Kallen, 1975), and the opossum (Rowe et al., 2005) all have extensive overlap of the maxilloturbinal by ethmoturbinal I. In these animals, the transverse lamina is confined to toward the posterior part of the ethmoturbinal complex or is absent (in two bats described by Bhatnagar and Kallen, 1975). Furthermore, in at least some of these mammals, a substantial portion of the ethmoturbinal I is lined with nonolfactory epithelium (Rowe et al., 2005; Smith et al., 2007b). This suggests that a more collaborative turbinal physiology exists for some mammals, leaving an interesting unanswered question of the plesiomorphic condition
Previous studies suggest that the ethmoturbinal complex is overlapped to a variable degree by the transverse lamina in different strepsirrhines. Loo (1973) shows ethmoturbinal IV to be completely overlapped by the transverse lamina, whereas ethmoturbinals I–III are anterior to the olfactory recess (Fig. 8, therein). While this relationship is also described here for cheirogaleids, other lemuroids differ. Hill describes “typical lemurs” (referring to genera of the family Lemuridae) as having the ethmoturbinals “more completely welded to the lamina terminalis of the ethmoid than in lorisidae or galagidae....” (1953, p 277). He also reported variations in this regard among indriids. Clearly, the transverse lamina is not a reliable structure to denote the limits of the ethmoturbinal complex.
The nasal fossa provides an excellent example of an anatomical region where human vs. nonhuman or mammal vs. nonmammal anatomy is so dichotomous that certain homologies remain obscure (Witmer, 1995; Smith and Rossie, 2006). In some circumstances such as this, different schemes of terminology for anatomical structures may be partially unavoidable (see Wilson, 2006). However, paranasal recesses and sinuses have become interchanged repeatedly (see Table 2 for some details). For instance, Rae and Koppe (2003) lamented the interchange in terminology of “lateral recess” with spaces relating to the maxillary sinus or its primordium
The present study used a novel terminology for the lateral recess. Specifically, it is proposed that the lateral recess should be named regionally based on the intersection of elements of the developing nasal capsule. Ossifications or the pars intermedia form the entire lateral wall of the recess. The anterolateral recess is the portion of the lateral recess where the semicircular crest (derived from the pars anterior) forms the medial wall. Posteriorly, the first ethmoturbinal (derivative of the pars posterior) forms the medial border of the posterolateral recess. The posterolateral recess is divided further into frontal and maxillary recesses, which are transected by the horizontally oriented frontomaxillary septum. These terms explicitly relate to contours of the fetal cartilaginous capsule. In Microcebus, the frontal recess appears first (see Fig. 4b) in keeping with observations on other mammals by Dieulafe (1906). Subsequently, the shape of the lateral recess relates to the formation of the semicircular crest and differential growth of ethmoturbinal I as well as a region-specific outwardly folded paries nasi. Confusion with terms such as the maxillary or frontal sinus is specifically avoided, because these spaces form by means of the distinctive process of secondary pneumatization (Rossie, 2006).
The frontal recess is primarily related to olfaction, a primitive association (Negus, 1958). In Mirza coquereli and C. medius this space is more complex by virtue of a second frontoturbinal. The anterolateral and maxillary recesses are predominantly nonolfactory spaces (except a small strip of olfactory epithelium extending anterior to the frontal recess). These spaces demonstrate the potential incongruity of mucosa/bone surface areas. The thick glandular lamina propria would appear to impart a great difference between estimates using osteological as opposed to mucosal boundaries.
Moore (1981) reports that frontoturbinals (called ectoturbinals by Moore) vary in number from 13–20 in extant taxa. In part, this is because he follows Paulli (1900) by including structures referred to here as “interturbinals.” The terminology advocated here provides different names for turbinals that do not reach the medial row. The advantage of this practice is that it partially differentiates these accessory scrolls, which are difficult to identify and determine relationships of homology. Interturbinals then, arise from the orbitonasal lamina. “Frontoturbinals” (Maier, 1993a, b) are found in the frontal recess and articulate with the frontal bone in adults
Moore reported that “prosimians” (clearly referring only to strepsirrhines in that actual context) possess only one or two frontoturbinals, and cheirogaleids conform to this. Paulli's work (1900) shows that carnivores and ungulates have as many as sevenfold additional frontoturbinals by comparison. Whether the number is reduced in primates as suggested by Moore (1981) or the other taxa evolved additional structures awaits further study. Homologies of frontoturbinals are difficult to deduce, and an arbitrary medial to lateral numbering scheme is used. It should not be assumed that frontoturbinal 1 of cheirogaleids corresponds with frontoturbinal 1 of nonprimates. Indeed, this study found no dorsally positioned frontoturbinals, except a possible rudiment in Mirza. This is consistent with a reduction in number due, in part, to medial compression secondary to orbital convergence.
If the lamina transversalis posterior is indeed homologous with the last ethmoturbinal of opossum and other marsupials, the nasal fossa of metatherians and eutherians differs in more than ethmoturbinal number. The fundamental difference would also include the complexity and extent of the olfactory recess. A potential conundrum exists in that this homology suggests that the transverse lamina is not formed similarly among different mammals. However, this must be the case broadly speaking, because the lamina overlaps the ethmoturbinal complex to a varying degree. Broader ontogenetic studies of therian mammals are required for a definitive answer
The present study indicates that in cheirogaleid primates, ethmoturbinal IV is the sole medial projection within the olfactory recess. Although the transverse lamina itself serves as valid indicator for a space dedicated for olfactory function, it cannot be assumed to correlate closely with the complexity or size of the ethmoturbinal complex in osteological studies of extant or fossil primates.
The measurements of the olfactory recess in this study begin in the coronal section where it is completely enclosed, a highly replicable definition. In terms of olfactory air-currents, this definition is certainly somewhat arbitrary and too rigid. Nonetheless, three-dimensional mucosal maps of Microcebus illustrate that the recess, as defined herein, is predominantly an olfactory space, in contrast to the nasopharyngeal chamber. As such, it represents potentially reliable proxy for the extent of olfactory mucosa. Of concern is the unknown extent to which the nasopharyngeal part of the nasal fossa shares in the function across different primates.
Implications for Future Studies
Maier (1993a) emphasized the need for further studies on the morphogenesis of the mammalian nasal capsule. Few authors have studied or discussed prenatal ontogeny of the nasal fossa since then (but see Lozanoff et al., 1993; Rowe et al., 2005; Rossie, 2003, 2006). Results of the present study illustrate that the ethmoturbinal complex of Microcebus develops from a cartilaginous template similar to mammals of diverse other taxa. The number of ethmoturbinals occupying a medial position in mammals has been reported to range from three to six (Negus, 1958; Moore, 1981). The mechanism by which turbinals vary among mammalian groups remain unanswered to date. For example, do some mammals acquire complexity by adding turbinals or splitting existing lamellae (e.g., pigs—Parker, 1874; Hillmann, 1971)? Which turbinals are lost in taxa with reduced complexity? Such questions require a broad range of species and ages.
The observations made to date suggest that possession of four medial ethmoturbinals is a common theme, and may have evolved through reduction of the last ethmoturbinal after divergence from a common therian ancestor. If stem primates developed a nasal fossae by means of the same template, it seems likely that reduction of the ethmoturbinals is not a defining feature of the order, but occurred as a complex trend across different taxa. However, a reduction of the frontal recess, and the olfactory turbinals therein, could be.
In terms of the olfactory versus nonolfactory SA, the present study provides a broader perspective than a similar previous study on an individual turbinal (Smith et al., 2007b). An age comparison supports the idea that olfactory epithelium scales differently than other epithelia between ages. Along the surfaces of ethmoturbinal I, Smith et al. (2007b) suggested that nonolfactory mucosa increased to a lesser extent than olfactory mucosa. The present study suggests this observation may be applied more broadly across the nasal fossa. In Microcebus murinus, total olfactory SA is 3.5-fold greater in adult versus neonate, whereas nonolfactory SA is more than 5.4-fold greater.
These quantitative data are the most detailed to date in terms of structure-mucosa relationships. Thus, these findings can inform future osteological analyses that attempt to infer physiological attributes of the nasal fossa, such as olfactory SA or air flow dynamics, in living or extinct primates. It is possible that the data on olfactory SA of individual elements reflects specific characteristics of Microcebus, so interpretations are necessarily generalized at present. However, the microanatomical and quantitative findings in this study offer guidance in the osteological interpretation of extant and fossil primates.
The following generalizations can be made at present: (1) This study shows that the anterior part of the nasal fossa is mostly nonolfactory in M. murinus, and the magnitude of nonolfactory SA increases postnatally. Thus, the term “olfactory snout” may misrepresent the prognathic midface of strepsirrhines. (2) The SA of the ethmoturbinal complex must be interpreted with caution. Restricted functional associations of individual turbinals with specific physiology may apply to some mammals (e.g., rats, mice, and dogs), but at least some primates do not exhibit this clear division of labor. (3) Two spaces, the olfactory recess and frontal recess, are reliable proxies for olfactory SA in Microcebus. However, the olfactory recess in cheirogaleids is not coextensive with the ethmoturbinal complex. Variations in the transverse lamina across mammals, especially with regard to the extent that it encloses ethmoturbinals, remain obscure. (4) Structures such as the glandular portion of the nasoturbinal and the mucosal SA of the olfactory recess are difficult to infer from osseous contours.
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- MATERIALS AND METHODS
- LITERATURE CITED
- Supporting Information
We thank E. Westwig and D. Lunde of the American Museum of Natural History for access to the Bluntschli collection of prenatal mammals and J.R. Wible for access to a fetal colugo. We also thank M.P. Mooney for access to a stereomicroscope. Lastly, many thanks to S.B. McLaren for caring for a portion of the sample studied herein, now housed at the Carnegie Museum, Section of Mammals. This is Duke Lemur Center publication # 1130.
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- LITERATURE CITED
- Supporting Information
- 1972. Olfactory and non-olfactory epithelia in the nasal cavity of the mouse, Peromyscus. Am J Anat 133: 37–50. .
- 1986. Transitional epithelial zone of the bovine nasal mucosa. Am J Anat 176: 159–170. .
- 1882. On a revision of the ethmoid bone in Mammalia, with special reference to the description of this bone in and of the sense of smell in the Chiroptera. Bull Mus Comp Zool Harvard 10: 135–164. .
- 2007. Primate anatomy: an introduction. New York: Academic Press. , . 1975. Quantitative observations on the nasal epithelia and olfactory innervation in bats. Acta Anat (Basel) 91: 272–282. .
- 1994. Observations on the vomeronasal organ of the colugo Cynocephalus (Mammalia, Dermoptera). Acta Anat (Basel) 151: 43–48. , .
- 2004. High resolution CT study of the cranium of a fossil anthropoid primate, Parapithecus grangeri: new insights into the evolutionary history of primate sensory systems. Anat Rec 281A: 1083–1087. , , .
- 1974. Rethinking primate origins. Science 184: 436–443. .
- 1973. The primate nasal fossa. Biol J Linn Soc Lond 5: 377–387. .
- 1994. The spatial organization of the peripheral olfactory system of the hamster. II: Receptor surfaces and odorant passageways within the nasal cavity. Brain Res Bull 34: 211–241. , , , .
- 2007. Reconstruction and morphometric analysis of the nasal airway of the dog (Canis familiaris) and implications regarding olfactory airflow. Anat Rec 290: 1325–1340. , , , , , , .
- 1937. The development of the vertebrate skull. Chicago: Chicago University Press. .
- 1906. Morphology and embryology of the nasal fossae of vertebrates. Ann Otol Rhinol Laryngol 15: 1–584. .
- 1994. Introduction. In: HallBK, editor. Homology. The hierarchical basis of comparative biology. San Diego: Academic Press. p 1–19. .
- 1953. Primates, comparative anatomy and taxonomy. I. Strepsirrhini. Edinburgh: Edinburgh University Press. .
- 1992. The evolution of nasal turbinates and mammalian endothermy. Paleobiology 18: 17–29. .
- 1994. Turbinates in therapsids: evidence for endothermy in mammal-like reptiles. Evolution 48: 207–229. .
- 2000. Septomaxilla of nonmammalian synapsids: soft-tissue correlates and a new functional interpretation. J Morphol 245: 29–50. .
- 1971. Anatomy of the nasal cavity and paranasal sinuses of the domestic pig (Sus Scrofa Domestica). Ph.D. dissertation. Iowa State University. .
- 2003. Anatomy of the nasal cavity in the chinchilla. Cells Tissues Org 174: 136–152. , , , .
- 2004. Observations of Tremacebus harringtoni (Platyrrhini, early Miocene, Sacanana, Argentina) based on high-resolution X-ray CT- scans. Anat Rec 281A: 1157–1172. , , , .
- 2006. Paranasal sinus pneumatization in the Miocene platyrrhine Homunculus patagonicus. Am J Phys Anthropol Suppl 42: 112. , , , .
- 2004. Mammals from the age of dinosaurs: origins, evolution, and structure. New York: Columbia University Press. , , .
- 1925. Etudes sur lémuriens. Anatomie compareé des fosses nasales et de leurs annexes. Archs Morph gé exp 22: 1–60. , .
- 1993. Histological studies on the nasal ethmoturbinates of goats. Small Rumin Res 11: 85–92. , , .
- 2000. Light and scanning electron microscopic studies of the nasal turbinates of the horse. Anat Histol Embryol 29: 103–109. , , , .
- 1989. Comparative morphology and morphometry of the nasal fossae of four species of North American shrews (Soricinae). Am J Anat 186: 306–314. , .
- 1959. The antecedents of man. Edinburgh: Edinburgh University Press. .
- 1973. A comparative study of the nasal fossa of four nonhuman primates. Folia Primatol (Basel) 20: 410–422. .
- 1974. Comparative study of the histology of the nasal fossa in four primates. Folia Primatol 21: 290–303. .
- 1989. Developmental morphology of the solum nasi in the mouse lemur (Microcebus murinus). J Morphol 202: 409–424. , .
- 1993. Computerized modelling of nasal capsular morphogenesis in prenatal primates. Clin Anat 6: 37–47. , , .
- 1993a. Cranial morphology of the therian common ancestor, as suggested by adaptations of neonate marsupials. In: SzalayF,NovacekMJ,McKennaMC, editors. Mammal phylogeny. New York: Springer-Verlag. p 165–181. .
- 1993b. Zur evolutiven und funktionellen Morphologie des Gesichtsschaedels der Primaten. Z Morph Anthrop 79: 279–299. .
- 1990. Primate origins and evolution. A phylogenetic reconstruction. Princeton, NJ: Princeton University Press. .
- 1981. The mammalian skull. London: Cambridge University Press. .
- 1967. Structure and function of the peripheral olfactory system. Physiol Rev 47: 1–51. , .
- 1967. A handbook of living primates. New York: Academic Press. , .
- 1958. The comparative anatomy and physiology of the nose and paranasal sinuses. Livingston: Edinburgh and London. .
- Nomina Anatomica Veterinaria. 2005. www.wava-amav.org/nav.htm.
- 1987. Developmental stages in human embryos. Washington: Carnegie Institute of Washington. .
- 1874. On the structure and development of the skull in the pig (Sus scrofa). Philos Trans R Soc Lond 164: 289–336. .
- 1900. Über die Pneumaticität des Schädels bei den Säugethieren. III. Über die Morphologie des Siebbeins der Pneumaticität bei den Insectivoran, Hyracoideen, Chiropteren, Carnivoren, Pinnepedien, Edentates, Rodentiern, Prosimien und Primaten. Gegenb Morpholog Jahrb 28: 483–564. .
- 1972. . Differenzierung und Systematik der Hauptmuschel bein einigen Gattungen der Säugetiere. Anat Anz 131: 378–390. .
- 1992. Environmental and social determinants of sexual function in the male lesser mouse lemur (Microcebus murinus). Folia Primatol 59: 1–25. .
- 2003. The term “lateral recess” and craniofacial pneumatization in Old World monkeys (Mammalia, Primates, Cercopithecoidea). J Morphol 258: 193–199. , .
- 1908. A contribution to the knowledge of the olfactory apparatus in dog, cat and man. Am J Anat 8: 17–47. .
- 2007. Concurrent 3-D visualization of multiple microscopic structures. In: Mendez-VilasA,DiazJ, editors. Modern research and educational topics on microscopy. No. 3. Vol. 2. Badojoz, Spain: Formatex. p 917–923. , .
- 2003. Ontogeny, homology, and phylogenetic significance of anthropoid paranasal sinuses. New Haven, CN: Yale University. .
- 2005. Anatomy of the nasal cavity and paranasal sinuses in Aegyptopithecus and early Miocene African catarrhines. Am J Phys Anthropol 126: 250–267. .
- 2006. Ontogeny and homology of the paranasal sinuses in Platyrrhini (Mammalia: Primates). J Morphol 267: 1–40. .
- 2007. Ontogeny of the nasolacrimal duct in primates: functional and phylogenetic implications. J Anat 210: 195–208. , .
- 2005. Organization of the olfactory and respiratory skeleton in the nose of the gray short-tailed opossum Monodelphis domestica. J Mamm Evol 12: 303–336. , , , .
- 1970. L'organe de Jacobson du lemurien malgache Microcebus. murinus. Mem Mus d'Hist Nat (Serie A) 61: 203–280. .
- 1891. Über die Nasenhöhle der höheren Säugethiere und des Menschen. Morphol Jahrb 18: 44–99. .
- 2003. Ontogeny of the nasopalatine duct in primate. Anat Rec 274A: 862–869. , , , .
- 2007. Sensory basis of food detection in wild Microcebus murinus. Int J Primatol 28: 291–304. , , , , , , and .
- 2006. Primate olfaction: anatomy and evolution. In: BrewerW,CastleD,PantelisC, editors. Olfaction and the brain: window to the mind. Cambridge: Cambridge University Press. p 135–166. , .
- 2004. Distribution of olfactory epithelium in the primate nasal cavity: are “microsmia” and “macrosmia” valid morphological concepts? Anat Rec 281A: 1173–1181. , , , .
- 2007a. Evolution of the nose and nasal skeleton in primates. Evol Anthropol 16: 132–146. , , .
- 2007b. Scaling of the first ethmoturbinal in nocturnal strepsirrhines: olfactory and respiratory surfaces. Anat Rec 290: 215–237. , , , , , , .
- 2007c. Growth deficient vomeronasal organs in the naked mole-rat (Heterocephalus glaber). Brain Res 1132: 78–83. , , , , .
- 1927. The development of the sphenoidal in man and its homology in mammals. J Anat 61: 153–166. .
- 1989. Nomina Anatomica. Edinburgh: Churchill Livingstone. , .
- 2006. Anatomical nomenclature of fossil vertebrates: standardized terminology or ‘lingua franca.’ J Vert Paleontol 26: 511–518. .
- 1995. Homology of facial structures in extant archosaurs (birds and crocodilians), with special reference to paranasal pneumaticity and nasal conchae. J Morphol 225: 269–327. .
- 1987. Morphogenesis of the mammalian skull with special reference to Tupaia. In: KuhnHJ,ZellerU, editors. Morphogenesis of the mammalian skull. New York: Springer Verlag. p 17–50. .
- 1887. Das periphere Geruchsorgan der Säugethiere. Stuttgart: Verlag von Ferdinand Enke. .
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- LITERATURE CITED
- Supporting Information
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