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Comparative Anatomy of the Facial Motor Nucleus in Mammals, with an Analysis of Neuron Numbers in Primates

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Comparative Anatomy of the Facial Motor Nucleus in Mammals, with an Analysis of Neuron Numbers in Primates THE ANATOMICAL RECORD PART A 287A:1067–1079 (2005) Comparative Anatomy of the Facial Motor Nucleus in Mammals, With an Analysis of Neuron Numbers in Primates CHET C. SHERWOOD* Department of Anthropology and School of Biomedical Sciences, Kent State University, Kent, Ohio ABSTRACT The facial motor nucleus (VII) contains motoneurons that innervate the facial muscles of expression. In this review, the comparative anatomy of this brainstem nucleus is examined. Several aspects of the anatomical organization of the VII appear to be common across mammals, such as the distribution of neuron types, general topography of muscle representation, and afferent con- nections from the midbrain and brainstem. Phylogenetic specializations are apparent in the proportion of neurons allocated to the representation of subsets of muscles and the degree of differentiation among subnuclei. These interspe- cific differences may be related to the elaboration of certain facial muscles in the context of socioecological adaptations such as whisking behavior, sound localization, vocalization, and facial expression. Furthermore, current evidence indicates that direct descending corticomotoneuron projections in the VII are present only in catarrhine primates, suggesting that this connectivity is an important substrate for the evolution of enhanced mobility and flexibility in facial expression. Data are also presented from a stereologic analysis of VII neuron numbers in 18 primate species and a scandentian. Using phylogenetic comparative statistics, it is shown that there is not a correlation between group size and VII neuron number (adjusted for medulla volume) among primates. Great apes and humans, however, display moderately more VII neurons that expected for their medulla size. © 2005 Wiley-Liss, Inc. Key words: facial motor nucleus; comparative neuroanatomy; facial expression; mammals; primates; stereology; motoneuron Therian mammals are characterized by well-differenti- these basic mammalian adaptations within particular lin- ated superficial facial muscles (also known as muscles of eages, subsets of facial muscles have increased in com- facial expression) derived from the second branchial arch. Compared to nonmammalian vertebrates whose facial muscle actions are limited to opening and closing the apertures encircling the mouth, eyes, and nostrils, mam- Grant sponsor: the National Science Foundation; Grant num- mals are capable of a much more varied range of facial ber: BCS-0121286; Grant sponsor: the Leakey Foundation; Grant movements (van Hooff, 1967). Greater mobility of the lips sponsor: the Wenner-Gren Foundation for Anthropological Re- and cheeks may have evolved in stem mammals to facili- search; Grant sponsor: Mount Sinai School of Medicine; Grant sponsor: Kent State University. tate neonatal suckling and more extensive chewing of food *Correspondence to: Chet C. Sherwood, Department of Anthro- (Huber, 1930). Additionally, with the evolution of in- pology, Kent State University, 226 Lowry Hall, Box 5190, Kent, creased energetic demands related to homeothermy in OH 44242. Fax: 330-672-2999. E-mail: [email protected] mammals, facial muscles may have become differentiated Received 16 August 2005; Accepted 17 August 2005 to facilitate mobility of the external ears and whisking DOI 10.1002/ar.a.20259 movements of tactile vibrissae to explore more actively the Published online 2 October 2005 in Wiley InterScience environment for food items (van Hooff, 1967). Building on (www.interscience.wiley.com). © 2005 WILEY-LISS, INC. 1068 SHERWOOD Fig. 1. Motoneurons located in the lateral sub- division of the VII of an orangutan (Pongo pyg- maeus) stained for (A) Nissl substance and (B) nonphosphorylated neurofilament protein (NPNFP) with SMI-32 antibody. Scale bar ϭ 100 ␮m. plexity and expanded concomitantly with socioecological phorylated neurofilament protein (Tsang et al., 2000), and adaptations. For example, the mass of musculature sur- calcineurin (Strack et al., 1996). Morphological and tract rounding the blowhole in odontocete cetaceans alters the tracing studies in rats and cats suggest that the VII con- shape of the spermaceti organ during the emission of tains few, if any, interneurons (Courville, 1966a; McCall biosonar (Cranford et al., 1996). In anthropoid primates, a and Aghajanian, 1979). Injection of horseradish peroxi- number of tractor muscles (e.g., zygomaticus major, zygo- dase (HRP) into the main trunk of the facial nerve, for maticus minor, levator labii superioris, depressor anguli instance, results in retrograde labeling of 98% of neurons oris, depressor labii inferioris, and risorius) surround the in the VII, indicating the virtual absence of neurons that mouth to configure the shape of the lips for vocalizations do not directly innervate facial muscles (McCall and Agha- and facial displays (Huber, 1931). Perhaps the most im- janian, 1979). In addition, size histograms of facial neu- pressive example of facial musculature specialization is rons in macaque monkeys (Welt and Abbs, 1990) and rats the elongated and highly mobile trunk of elephants, which (Martin et al., 1977) show a unimodal distribution, indi- is composed of several layers of differentially oriented cating that few small ␥-motoneurons are found in the VII. muscle bundles derived exclusively from the caninus mus- This concords with reports that muscle spindles, which cle (also known as levator anguli oris) (Endo et al., 2001). are innervated by ␥-motoneurons, occur in very low abun- Neurons within the facial motor nucleus (VII) of the dance in superficial facial muscles (Bowden and Mahran, brainstem innervate the superficial facial musculature 1956; Olkowski and Manocha, 1973; Dubner et al., 1978; and hence comprise the final common output for circuits Brodal, 1981; Sufit et al., 1984). related to various behaviors, including emotional expres- As with other motor nuclei (e.g., hypoglossal) (Sokoloff sion, vocal communication, respiration, ingestion, protec- and Deacon, 1992), the neurons of the VII are arranged in tive reflexes, and sensory exploration of the environment. subnuclei that lie adjacent to one another in longitudinal In addition to the main VII, the accessory facial nucleus cell columns. Because each subnucleus extends rostrocau- (also called the suprafacial nucleus or the dorsal facial dally for a different distance, the differentiation of subnu- nucleus) contains motoneurons of deep facial muscles (i.e., clei is most apparent in coronal sections at the middle stylohyoid and the posterior belly of the digastric). Axons third of the VII. Historically, the number of VII subnuclei of motoneurons in the main VII and the accessory facial recognized by researchers has varied considerably de- nucleus exit the brainstem together on the ipsilateral side pending on species, anatomical methods, and subjective as the facial nerve (CN VII), then leave the base of the assessment. For example, based on Nissl staining pat- skull via the stylomastoid foramen and enter the parotid terns, Welt and Abbs (1990) described six subnuclei in gland, where the main trunk of the facial nerve divides long-tailed macaques (Macaca fascicularis), Jenny and into several major branches. Saper (1987) described four subnuclei in M. fasciularis, Considering the central involvement of the VII in di- and Satoda et al. (1987) described five subnuclei in Japa- verse sensorimotor adaptations of the facial muscles nese macaques (M. fuscata). Some discrepancy may arise across phylogeny, the comparative neurobiology of the VII from the fact that facial neurons are arranged in irregular is of special interest. This article presents an overview of clusters and cytoarchitectural boundaries between subnu- phylogenetic variation in the neuroanatomical structure clei are not well defined in most species (Papez, 1927; and connectivity of the VII in mammals. Vraa-Jensen, 1942; van Buskirk, 1945; Courville, 1966a; Dom et al., 1973; Martin and Lodge, 1977; Porter et al., SIMILARITIES ACROSS PHYLOGENY 1989; Welt and Abbs, 1990; Yew et al., 1996; Sherwood et al., 2005). Nonetheless, some boundaries among subnuclei General Cytoarchitectural Plan can be more clearly delimited in tissue stained for myelin The VII is composed predominantly of multipolar ␣-mo- and nonphosphorylated neurofilament protein (Fig. 2). In toneurons (Fig. 1), which express the biochemical markers these preparations, however, there is not clear differenti- choline acetyltransferase (Ichikawa and Hirata, 1990; ation between all the subnuclei identifiable based on cy- Ichikawa and Shimizu, 1998; Tsang et al., 2000), nonphos- toarchitecture, suggesting that there may be fewer func- FACIAL MOTOR NUCLEUS IN MAMMALS 1069 Conserved Musculotopy The topographic representation of the muscles of facial expression in the VII has been studied in several species. Unfortunately, interpretation of older axotomy studies is hampered by the fact that retrograde cellular pathologic changes are somewhat unpredictable (Martin and Lodge, 1977). In addition, many retrograde cell degeneration studies involved sectioning of a single peripheral nerve branch. Individual facial nerve branches, however, may innervate a number of different muscles and a particular muscle may be supplied by more than one nerve branch (Provis, 1977). Thus, early studies that found a close cor- respondence between subnuclei of the VII and the inner- vation territories of peripheral branches of the facial nerve may have been influenced by methodological artifact (van Gehuchten, 1898; Marinesco, 1899; Yagita,
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