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2.17 Evolution of Vertebrate Olfactory Subsystems 2.17 Evolution of Vertebrate Olfactory Subsystems H L Eisthen and G Polese, Michigan State University, East Lansing, MI, USA ª 2007 Elsevier Inc. All rights reserved. 2.17.1 Introduction 355 2.17.1.1 What is Olfaction? 355 2.17.1.2 Components of the Vertebrate Olfactory System 357 2.17.2 Evolutionary Changes in the Vertebrate Olfactory System 360 2.17.2.1 Chordates and Basal Craniates 360 2.17.2.2 Lampreys 361 2.17.2.3 Cartilaginous Fishes: Sharks, Skates and Rays, and Chimaeras 363 2.17.2.4 Ray-Finned Fishes 365 2.17.2.5 Lobe-Finned Fishes: Lungfishes and Coelacanths 370 2.17.2.6 Tetrapods: Amphibians, Reptiles, and Mammals 372 2.17.3 Conclusions 386 2.17.3.1 Evolutionary Changes in the Organization of the Olfactory Epithelium 386 2.17.3.2 Evolutionary Changes in the Organization of the Olfactory Bulbs 387 2.17.3.3 Evolutionary Changes in the Organization of Central Olfactory Projections 389 2.17.3.4 Evolution of Vertebrate Olfactory Subsystems 390 Glossary in the respiratory, circulatory, and digestive systems that detect gasses, ions, and nutrients. In general, these olfactory The olfactory system in any animal is the chemosensory systems consist of isolated sensory cells system primary sensory system that responds to that project to the spinal cord or hindbrain. These chemical stimuli emanating from a dis- systems will not be discussed here. tant source. In this article, we will consider three interrelated pheromone A chemical cue that, when released by an olfactory subsystems: the main olfactory system, or individual, elicits specific behavioral or physiological responses from olfactory system proper; the vomeronasal system; conspecifics. and the terminal nerve. The main olfactory system terminal The most anterior cranial nerve in verte- comprises receptor neurons located in a specialized nerve brates. The terminal nerve releases sensory epithelium in the nasal cavity, as well as the compounds into the nasal epithelia, central projections of these neurons. The receptor modulating activity of sensory receptor cells of the olfactory epithelium develop from the cells. nasal placode, and the ingrowing fibers of the devel- vomeronasal A discrete olfactory subsystem present in oping sensory neurons are involved in development system tetrapods that differs morphologically of the olfactory bulb at the rostral pole of the pro- from the olfactory system. Its function spective telencephalon (Gong and Shipley, 1995; is unclear. Graziadei and Monti-Graziadei, 1992; Long et al., 2003). 2.17.1 Introduction The vomeronasal system, or accessory olfactory system, also develops from the nasal placode, and is 2.17.1.1 What is Olfaction? present as a discrete sensory system only in tetrapods The term olfaction is commonly applied to chemosen- (see The Evolution of the Vomeronasal System). The sory systems that detect chemicals emanating from a vomeronasal epithelium is sequestered in the vomer- distant source. Other chemosensory systems generally onasal organ, also known as Jacobson’s organ require physical contact with the source for detection, (Figure 1). The sensory epithelium contains and this sensory modality is called gustation. The some what different cell types than does the vertebrate olfactory and gustatory systems are anato- main olfactory epithelium, and the vomeronasal mically distinct; the latter is discussed in a separate receptor neurons terminate in microvilli, whereas article (Evolution of Taste). Fibers of the trigeminal olfactory receptor neurons can terminate in cilia nerve also detect chemical stimuli, as dochemosensors or microvilli or both. In some vertebrates, 356 Evolution of Vertebrate Olfactory Subsystems ob aob en ns ob vno aob en vno ns Figure 1 Illustration of the locations of the olfactory epithelium, inside the nasal sac (ns), and of the vomeronasal organ (vno) in a frog and a snake. The nasal sac opens to an external nostril (en) on the dorsal surface of the snout, whereas the vomeronasal organ opens to the nasal sac in frogs and oral cavity in snakes. The axons of the olfactory receptor neurons project to the olfactory bulb (ob), and those of the vomeronasal receptor neurons project to the accessory olfactory bulb (aob). the axons of the vomeronasal receptor neurons refer to this structure simply as the ‘olfactory bulb’ form a separate cranial nerve, the vomeronasal to facilitate comparisons across vertebrates. nerve, but in others these axons run alongside the The terminal nerve, or nervus terminalis, is the olfactory nerve and the two cannot be distin- most anterior of the cranial nerves. It extends guished using conventional light microscopy. between the nasal cavity and basal forebrain, and, Vomeronasal receptor cell axons project to the because of its anatomy, has been thought to serve accessory olfactory bulb, a structure that is histo- sensory function (e.g., Demski and Northcutt, 1983; logically distinct from the main olfactory bulb Rossi et al., 1972). Nevertheless, recordings from (Figure 1). The secondary projections of the olfac- the terminal nerve have failed to detect sensory tory and accessory olfactory bulbs differ. The activity (Bullock and Northcutt, 1984; White and molecular, physiological, and anatomical differ- Meredith, 1995), and the terminal nerve is now ences between the vomeronasal and olfactory thought to function in modulating activity in the system suggest that the two subsystems serve dif- olfactory epithelium (reviewed in Oka, 1992; ferent behavioral functions, but the nature of this Wirsig-Wiechmann et al., 2002a). The terminal difference is unclear. Although the vomeronasal nerve usually contains a ganglion, the location of system is often presumed to be specialized for which varies across groups of vertebrates. The detecting pheromones, it responds to a variety of neurites extending outward from these bipolar odorants with differing behavioral significance in neurons sometimes comprise a separate nerve, all groups of tetrapods, and this presumption is but the fibers of the terminal nerve can also run unwarranted (see The Evolution of the within the olfactory or vomeronasal nerve, as illu- Vomeronasal System; Baxi et al., 2006; Halpern strated in Figure 2. The cells and fibers of the and Martı´nez-Marcos, 2003; Restrepo et al., terminal nerve contain neuromodulatory com- 2004; Shepherd, 2006). A different hypothesis pounds, including gonadotropin releasing posits that the vomeronasal system is specialized hormone (GnRH) and acetylcholine (reviewed in for detecting nonvolatile molecules. Although bet- Wirsig-Wiechmann et al., 2002a). The nerve can ter supported than the pheromone hypothesis, this also be immunohistochemically labeled with anti- hypothesis is still problematic (Baxi et al., 2006). sera directed against neuropeptide Y (NPY) and Throughout this article, we will refer to the nasal the molluscan cardioexcitatory neuropeptide chemosensory system present in all vertebrates as FMRFamide, but the two antisera may cross- the ‘olfactory system’ rather than the ‘main olfac- react with a single peptide (Chiba, 2000). We tory system’. Similarly, although it is common to use include the terminal nerve in this article not only the term ‘main olfactory bulb’ to refer to the pri- because of its role as a centrifugal portion of the mary target of the olfactory receptor cells in animals olfactory system, but also because the primary that possess a separate vomeronasal system, we will neurons of the terminal nerve develop from the Evolution of Vertebrate Olfactory Subsystems 357 pumping mechanisms, and nonsensory cells with motile cilia that create constant movement. Within the nasal cavity, the pseudostratified sen- sory epithelium contains three basic cell types (Figure 3b): olfactory receptor cells; sustentacular cells, a class of supporting cells; and basal cells, poa the progenitor cells that give rise to new receptor ob and sustentacular cells throughout life. The olfac- on tory receptor cells are bipolar neurons with a onf dendrite that terminates in cilia or microvilli or ns both. The membrane-bound odorant receptors are en localized to these processes, which are therefore Figure 2 Location of the terminal nerve around the nasal presumed to be the site of transduction (Menco, cavities and in the brain of a salamander. Anterior is down and 1997). The odorant receptors are part of the large to the left. The fibers of the terminal nerve extend between the preoptic area and nasal cavities, wrapping around the outside of superfamily of G-protein-coupled receptors the olfactory epithelium (lower left). en, external nostril; ns, nasal (GPCRs) that have seven membrane-spanning sac; ob, olfactory bulb; onf, olfactory nerve fascicles; on, olfac- domains (reviewed in Gaillard et al., 2004; tory nerve; poa, preoptic area. Mombaerts, 2004). The large family of odorant receptor genes has been suggested to contain two nasal placode (Schwanzel-Fukuda and Pfaff, fundamentally different classes that differ in the 1989), as do the olfactory and vomeronasal recep- size of the third extracellular loop (Freitag et al., tor neurons. 1995, 1998), although others have suggested that a larger number of groupings better describes the 2.17.1.2 Components of the Vertebrate Olfactory evolutionary history of the gene family (Niimura System and Nei, 2005). As depicted schematically in Elements of the olfactory system have been Figure 3c, the odorant receptor is coupled to an described from an evolutionary or comparative per- olfactory-specific G-protein (Gaolf), with alpha spective in several reviews
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