Olfaction in Mammals. Department of Biology, Clark University, Worcester, Massachusetts

Transcription

1 A.\r. ZOOLOGIST, 7: (1967). Olfaction in Mammals DAVID G. MOULTON Department of Biology, Clark University, Worcester, Massachusetts SYNOPSIS. This paper centers on selected and particularly, little recognized problems in mammalian olfaction: (1) With certain exceptions the spacing of the external nares in most mammals does not favor orientation in an odor gradient by simultaneous comparisons of odor intensities (tropotaxis). (2) The mammalian nose is rich in both dynamic and static devices for conditioning and controlling the How of inspired air. (3) A well-developed vomeronasal organ is widely distributed but its function is obscure. (4) Nerve impulse traffic telemetered from the olfactory bulb of freely moving rats shows a varying pattern of discrete bursts of units with each inspiration and more sustained discharges. (5) Olfaction in species showing adaptations tor lite in water, air, and underground is reviewed. (6) Because of its rich olfactory-trigeminal innervation the snout of pigs, moles, etc., may be considered as a "chemotactile" organ. The ability to detect, analyze, and exploit odors appears to reach its highest degree of development among mammals. For reasons that are not entirely selfevident, this evolution is paralleled by marked increases in the number of olfactory receptors and their supporting structures. In particular, the ethmoturbinals generally form a complex series of convolutions, congesting the olfactory chamber, and, in some species such as the badgerextending into the frontal sinuses and the sphenoid recess. This development allows the dog to accommodate an estimated 2.8 X 10 8 receptors (Wieland, 1942). It would not be surprising if the number approached half a billion in certain other species. Even the retina contains fewer receptors. But effectiveness in exploiting odors need not be due to the extensiveness of the olfactory apparatus alone. Mammals are especially flexible and efficient in deploying their sensory resources and tend to make more use of all available cues. Unless this plasticity is taken into account and rigorous analyses of the sensory components of mammalian behavior are fewclaims that olfaction is the dominant modality in a particular species, or in con- This research was supported in part by a research grant, NB , from the National Institutes of Health, and by grants, AF-AFOSR and AF-AFOSR , from the U. S. Air Force. (421) trolling a particular behavioral pattern, should be viewed with caution. On the other hand, there is much evidence to suggest that many mammals do, in fact, exploit odors extensively in trail-following, recognition of territory, of young, of mates, and of other social groups, as well as in the detection of food and predators. Furthermore, it is becoming increasingly evident that odors may control certain reproductive functions in mice and doubtless other species of mammals, by acting as pheromones (Whitten, 1966a). In what follows we shall examine a few selected aspects of mammalian olfaction, and where appropriate, stress the existence of problems that are given little attention or are generally unrecognized. RELATIVE SIZE OF OLFACTORY STRUCTURES IN DIFFERENT SPECIES Most mammals retain an extensive cortical commitment to olfaction, despite marked diversity in the relative degree of elaboration of the olfactory bulb. But it is among the more primitive groups, such as the echidna, opossum, ant eater, and armadillo, that olfactory structures are most prominent. The platypus is particularly interesting since the salient features of its olfactory organs more closely resemble those found in the reptile than in the mammal. According to Smith (1895)

2 422 DAVID G. MOULTON OlftKtery N«oc«rt» 61 «SiS^gJ #* 36 Q 5? 74 FIG. 1. Volumes of subdivisions of the telencephalon as a per cent of total telencephalon (data from Stephan and Andy, 1964). there is no cribriform plate, and the bulb is invaginated to form a cup-like depression. This invagination is similar to that found in certain Ophidia and, as in Ophidia, is associated with a highly-developed vomeronasal nerve. The vomeronasal organ is also well-developed in the opossum in which the main bulb is relatively enormous. But a well-developed olfactory apparatus is present in most carnivores, pterissodactyls, rodents, and chiroptera; and it is mainly in the higher primates and aquatic mammals that any severe reduction occurs. In the case of the higher primates this reduction is the culmination of a progressive evolutionary trend (Fig. 1). Both the olfactory bulbs and the hippocampus are prominent in the primitive insectivores the group generally thought to have given rise to several orders of placental mammals, including primates. The gradual diminution in the size of the olfactory bulbs parallels the dramatic rise of the neocortex. Figures given by Stephan and Andy (1964) suggest that the olfactory bulb is the only telencephalic structure showing obvious regression in evolution. The olfactory and limbic systems seem independent of one another. Unfortunately, it is difficult to find meaningful indices for comparing the degree of development of the olfactory bulb or organ in different species. As shown in Table 1, one suggested criterion is the ratio of the area of the nasal respiratory mucosa to that of the olfactory epithelium. It might be deduced from this table that man, monkey, and sheep are "microsmatic," while dog, cat, rat, and guinea pig are "macrosmatic." However, it is difficult to accept the position of sheep in this classification, if it is taken as an index of olfactory powers. Furthermore, wide individual variations within the same species can occur: in the extreme case of the dog, the area of the olfactory epithelium in pekinese was found to be cm 2, while in a German sheepdog it extended over cm 2 (Lauruschkus, 1942). Unless this intraspecific variability is considered and the necessary figures are seldom recorded interspecific comparisons should be viewed with caution. Unfortunately, more meaningful data are not available. ARCHITECTURE OF THE MAMMALIAN NOSE The external nares It is well known that the pairing of the eyes and ears assists in determining the direction of the source of a stimulus. Does the pairing of the external nares serve a comparable function? If such a mechanism exists it could depend on the detection of differences in the intensities of odorants reaching each nostril (tropotaxis). The farther apart the nostrils the greater the effective differences in concentration are likely to be. Sharks have widely separated external nares, and there is some evidence that the hammerhead shark, in particular, may orientate in an odor gradient by tropotaxis (Jones, 1960). However, in most mammals the nostrils TABLE 1. Absolute and relative areas of olfactory and respiratory mucosa in various species of mammals. Sheep Guinea pig Rat Cat Dog Monkey Man Respiratory surface (in cm 2 ) (From Dieulafe, 1906) Olfactory surface (in cm 2 ) Ratio

3 OLFACTION JN MAMMALS 423 are relatively close together, as in the carnivores. This does not exclude the possibility that orientation may be based on simultaneous comparisons of odor intensities, [or time of arrival of odorous molecules at the receptors, as von B k6sy (1964) argues] since sensitive receptors might still detect minute differences, but it is not an arrangement which favors such a mechanism. In any case, for highly mobile species the successive spatio-temporal comparisons made possible by swinging the head or body from side to side as do dogs, hagfish, and dogfish may be more effective than simultaneous comparison of intensities. Nevertheless, there are certain mammals in which the external nares are more widely separated, notably the larger ungulates (e.g., giraffe, hippopotamus, and moose). The most striking example is the tubenosed bat, Harpyia major, in which each nostril is extended into a tube-like structure projecting anteriorly and dorsolaterally from the tip of the snout. Whether these species do, in fact orientate by tropotaxis remains to be investigated. Internal structure of the nose The mammalian nose is particularly rich in both static and dynamic devices which alter the flow, or condition of the inspired air. Dynamic mechanisms can be under either voluntary or autonomic control. For example, in some species, voluntary movements of the nasal alae can close the external nares. Negative pressure may then be built up in the nasal cavity, facilitating a sudden intake of air at each sniff. Since the mammalian nasal fossae accommodate both the olfactory organ and the respiratory air stream, the adaptive value of a particular structure is not always clear. The maxillo-turbinals are a case in point. That they are involved in warming cold air might be deduced from their extensive development in seals and other mammals inhabiting cold environments: here the surface area is so increased by branching that this body has a sieve-like structure. But even carnivores living in less extreme environments have maxillo-turbinals sufficiently elaborate to impede airflow markedly: thus Negus (1960) found pressures in the dog's trachea as high as mm H 2 O, as compared with a value of 12 mm H 2 O in man [for an airflow of 500 cc/sec. (Craig, et al., 1965)]. In fact, there is evidence that the maxillo-turbinals are involved in heating or cooling, humidifying, and filtering of inspired air, and may function in a countercurrent heat-exchange mechanism. For example, Negus (1960) has compared the temperature and humidity of air before and after it had passed through dog turbinals. Upon reaching the trachea, air delivered at 39 C or -(-48 O C was close to body temperature, while air delivered at 0% relative humidity was saturated with moisture. The degree of engorgement of the nasal mucosa doubtless contributes to these effects since it is said that when exposed to warm air the mucosa swells, while with cold air it shrinks. The properties of the inspired air are not the only factors influencing the degree of mucosal engorgement. Indeed any agent which alters the excitability of the autonomic nervous system may be effective, since this system controls the vasomotor functions of the mucosa. At the level of the 'maxillo-turbinals these changes can be dramatic, resulting at one extreme in the almost complete closure of the nasal airways (Fig. 2). These various results indicate the nature of the modifications imposed on inspired air by passage through the maxillo-tur- FIG. 2. Coronal sections through maxillo-turbinal regions of cats after perfusion with adrenaline and histamine showing extreme constriction (A) and engorgement (B). The normal condition more closely approximates (A) than (B). Drawn from pliotographs appearing in a paper by Negus

4 424 DAVID G. MOULTON binals, and suggest how the changes are effected. They do not, however, establish to what extent these changes facilitate olfactory functions, respiratory functions, or both. Nor has there been any systematic attempt to explore this problem in mammals. In addition to their function in conditioning the inspired air, changes in the width of the nasal airways influence the complex aerodynamical properties of this region. This, in turn, partly determines what proportion of molecules entering the nasal cavity will finally contact the receptors. There is little agreement, however, about what this proportion is likely to be in a given species. In most "macrosmatic" species, air-flow probably reaches the anterior ends of the olfactory turbinals, but additional modifications, such as the lateral ethmoidal plates in the leopard (Panthera pardus), may deflect air into the olfactory area. The geometry of the nasal fossae and associated structures also determines the extent to which olfactory input is related to input from other senses. For example, Whitten (1966) has observed in the mouse that fluid from the mouth travels up the cleft in the upper lip to enter the nasal cavity. Here, known patterns of mucus movement would carry the fluid posteriorly. Consequently, volatile constituents of food placed in the mouth may be smelled. The nasopalatine (Stenson's) canal provides further intercommunication between the olfactory and buccal cavities in some species. OLFACTORY EPITHELIUM The structure of the olfactory epithelium is remarkedly uniform throughout the vertebrates, and there is little to distinguish the epithelium of one mammalian species from that of another. However, there are some variations in thickness, ratio of supporting cells to receptors, and the number of cilia per receptor (see Moulton and Beidler, 1967). For example, the mole is unusual, if not unique among mammals, in having more supporting cells than receptors (Graziadei, 1966). Doubtless this species, in moving about its burrows at 2,5 mph, encounters concentrations of dust particles. The abundance of supporting cells might, therefore, reflect a need to protect the receptors, since there is evidence that the supporting cells have a secretory function. The initial interaction between odorant molecule and receptor presumably occurs at specialized regions of the cell surface. In mammals so far examined this surface is augmented by one or more cilia projecting from the terminal knob of the receptor cell into the secretions of Bowman's glands. In the mole many of the receptors bear only one cilium (Graziadei, 1966) as in the pike; but in other mammals it is more common to find 5-15 cilia. The odorant molecules must first penetrate the dense mat formed by these cilia before reaching the main surface of the receptor. It is tempting, therefore, to assume that the layer of cilia is the most significant portion of the cell surface for olfaction, and this view seems strengthened by the fact that modified cilia are the transducing elements in several other sensory systems, including the retina. However, there is an extensive unciliated surface of the receptor also exposed to the stimulating agent, and it may well be that the cilia have only an accessory function. But whatever may be the relative significance of cilia, microvilli, or other specializations of the cell surface, we are, in all cases, far from knowing the detailed molecular arrangement of the membrane. Yet this knowledge must precede a full understanding of the odorant-receptor interaction. We are also ignorant of the detailed events following the initial disturbance of the membrane. Presumably it involves the release of energy which may first have to be amplified before it can migrate across the considerable distance from the ciliated surface of the cell to the region of the cell body. It is generally assumed that the triggering of the all-or-none propagated impulse will occur at, or near this region of the cell. Although slow potentials can be recorded from varying depths in the olfactory mucosa their relation to the intracellular transfer of excitation is not clear.

5 OLFACTION IN MAMMALS 425 THE PRIMARY OLFACTORY NEURONES, THE OLFACTORY BULB, AND THE CENTRAL OLFACTORY CONNECTIONS Among the mammals studied so far (other than the platypus) few major differences have emerged in the arrangement of the afferent fiber projections onto the olfactory bulb. However, in the pig there is a curious segregation of the primary neurones into four groups; each group projects to a different "sector" of the bulb. Each of the four sectors in each bulb shows marked modifications in the arrangement of its cellular elements. Thus, the glomeruli in each sector form two layers, each two or more glomeruli thick, and there is an increase in the density of mitral cells in both the outlying and main mitral cell layers (Crosby and Humphrey, 1939). The salient features of the mammalian olfactory bulb are outlined in Figure 3. The layers are well defined, and in a proportion of cases each mitral cell and tufted cell appears to be associated with only one glomerulus by a single main dendrite. This contrasts with the situation in amphibians, reptiles, and teleosts where such a relation has not been observed; each of these cells has several main dendrites ending in two or more glomeruli. In other words there seems to be an evolutionary increase in the degree of segregation between neighboring pathways. If the situation in the visual system of mammals provides any guide, the transfer of olfactory information from the epithelium to the bulb might be associated with increased functional specialization of single cells. Electrical recordings from single bulbar cells and from the olfactory epithelium have failed so far to provide sufficient evidence to confirm this view. However, so little is known about the relevant parameters and the principles governing the organization of input to the olfactory bulb, that this possibility cannot be eliminated. A further problem concerns the relation of the neural discharge of the olfactory bulb to the behavioral response of the animal to odor stimulation. Fortunately, it Eil. Pkxiform Layer Int. Pleiiform Layer Glomerulus Tufted Cell Mitral Cell -J5.000 Granular Gill Receptors Olfactory Mucosa FIG. 3. Structure of the olfactory bulbs and their relations to the nerves and mucosa (modified from Moulton and Tucker, atter Gastaut and Lammers). A.C., anterior commissure. The figures are estimates made by Allison and Warwick, 1949, of the numbers of each type of cell in the olfactory bulb and in the olfactory mucosa lining one nasal cavity of the rabbit. is now possible to study the nerve impulse activity of the bulb of freely moving animals, including rats and rabbits, by telemetering the output from electrodes chronically implanted with their tips in the region of the mitral cells (Fig. 4). Ever since the studies of Cajal there have been numerous reports that fiber systems originating in the tufted cells of one bulb cross in the anterior commissure and terminate in the opposite bulb (see Moulton and Tucker, 1964, for references). More recently, careful degeneration studies by Lohman and Lammers (1967), as well as by Scalia (1966) and others, have failed to reveal more than a few fibers, at most, interconnecting the bulbs. These discrepancies may arise from the difficulty of making large lesions in the olfactory bulb which do not also involve parts of the an-

6 426 DAVID G. MOULTON FIG. 4. Telemetry of nerve impulse discharges from the olfactory bulb of the rat: (A) The transmitter is plugged into sockets attached to the rat's skull. Those, in turn, are soldered to wire electrodes chronically implanted in the olfactory bulb. Since the device weighs less than 2 g it does not disturb the behavior of the rat, which can move freely. The activity is relayed to an F.M. receiver. (B) Traffic of nerve impulses telemetered from the olfactory bulb of a rat sniffing food pellets. The level of resting discharge is shown at the extreme left. Short bursts (seen clearly near the center of the trace) may occur with each inspiration. However, when the rat sniffs rapidly, individual bursts are not always evident. This is seen in the right-hand section of the trace. The trace covers a 5-sec period and the highest spikes shown arc in the order of 100 fiv. (For further details, see Moulton, 1967b, and Skutt, et al., 1967). terior olfactory nucleus. If there were such involvement, centrifugal fibers originating in non-bulbar areas, but crossing in the anterior commissure, might show degeneration and be mistaken for bulbar associational fibers. THE VOMERONASAL (jacobson's) ORGAN Although this organ has been the subject of a remarkable number of studies, and of much speculation, its function remains obscure. In mammals it is an elongated blindending tube lying ventral to the nasal fossae and opening either anteriorly into the nasal cavity, or opening into the buccal cavity by way of the nasopalatine canal. It has a sensory epithelium similar to that of the olfactory organ and is connected to the accessory olfactory bulb by the vomeronasal nerve. In a dog of average size the length of the organ is 3 cm (Klein, 1882). Unlike birds, most mammals retain a well-developed vomeronasal organ. However, the degree of development never reaches the peak seen in some reptiles where the vomeronasal fibers may exceed in bulk those of the olfactory nerve. In the rabbit, for example, Allison (1953) estimates that the number of receptors is about one-thirtieth the number in the olfactory epithelium. In this species the organ opens into a cleft immediately below the nostrils. Nevertheless, the number of mammals having a well-developed organ is much larger than commonly stated and includes bats, insectivores, and prosimians. Welldeveloped accessory bulbs or organs are also found in the platypus, opossum, cat, fox, dog, rabbit, and guinea pig. On the other hand, while accessory bulbs are found in new-world monkeys (platyrrhini) they are absent or rudimentary in old world monkeys (catarrhini), as in most aquatic mammals. The main bulb and accessory bulb are independent of one another in size (Stephan, 1965; Mann, 1961). Mammals may also extract additional information about the properties of odorous molecules from the free nerve endings oi the trigeminal nerve in the nasal mucosa. Electrophysiological recordings have shown that in the rabbit the sensitivity to odorants of both vomeronasal and nasal trigeminal receptors may approach, and in. some instances exceed, that of the olfactory organ (Tucker, 1963a). The interrelations of these systems are discussed more fully by Moulton (1967a). OLFACTION IN EXTREME ENVIRONMENTS Different vertebrate groups sharing the same environment must often extract from it quite different sets of information. Thus, in contrast to fish, aquatic mammals show severe reduction in the olfactory organ; there is a similar divergence between most birds and bats.

7 OLFACTION IN MAMMALS 427 Aquatic mammals The regression of olfactory function is particularly severe in porpoises, dolphins, and odontocete whales, while in seals and walruses the ethmoidal turbinals are not only reduced in area but are almost entirely surrounded by bony walls (Breathnach, 1960; Negus, 1958). This failure to exploit odors might, at first, seem curious, and the suggestion that organs adapted for life in air cannot function effectively in an aqueous medium is not acceptable. Electrical recordings from the primary olfactory neurones of the air-breathing gopher tortoise show that responses to odorants presented in an aqueous phase are closely similar to those delivered in a gaseous phase (Tucker, 19636). More probably we are dealing with an evolutionary failure to segregate olfactory and respiratory functions: in aquatic mammals water drawn in across the olfactory organ will also reach the lungs. There appears to be no evidence concerning the possible chemosensory role of free nerve endings in aquatic mammals, although in mysticete whales the trigeminal nerve is the largest of all the cranial nerves. Bats The importance of olfaction to most bats is implied not only by the well-developed olfactory system, but also by the widespread distribution of scent glands. These occur in various locations, including the upper lip, the base of the tail, the throat, the center of the forehead, and the wing membranes (Allen, 1940). The odors of these glands may serve important social functions. For example, Nelson (1965) reports that flying foxes (Pteropus poliocephalus) use their scapular glands to mark territory. He also claims that females identify their young, and members of other social groups recognize each other, by smell. The vomeronasal organ of certain phyllostomatoid bats, although not prominent, is apparently well-developed, and according to Mann (1961) there is no direct relation between the volumes of the main olfactory and accessory bulbs in four species. In Phyllostomns hastatus, a large omnivorous neotropical bat, the entrance to the vomeronasal organ is by way of a long, very narrow duct. If odorants are to reach the organ, strong vasoconstriction of the erectile tissue lining the duct may be required. In addition, however, opening of the duct may be assisted by movement of the anterior cartilaginous prongs of the vomeronasal organ. These are, in turn, controlled by the musculus levator labi which also retracts the upper lip. Sexually motivated individuals of four genera have been seen violently retracting the upper lip in a "characteristic fashion", and Mann has argued that the vomeronasal organ in bats is specifically involved in the release of sexual activities. Moles Although the mole (Talpa europaea) is not blind, vision is poorly developed and a large proportion of the total sensory inflow seems to be channeled through the snout and ears. Direct evidence of the importance of olfaction is lacking but it is said that the mole can detect earthworm mucous smeared on a glass plate up to 30 cm away (Quillian, 1966). Furthermore, the olfactory organs and bulb are well developed; in fact, the olfactory epithelium covers a wider area than in the cat (Graziadei, 1966). In Scalopus aquaticus marchinus the arrangement of the cellular elements of the bulb is similar to that of the shrew (Blarina brevicauda) and the free-tailed bat (Tadarina mexicana) (Crosby and Humphrey, 1939). The bulb has prominent hypothalamic and epithalamic connections suggesting important olfactosomatic and olfactovisceral relations (Johnson, 1957). THE NOSE AS A CHEMOTACTILE ORGAN Both moles and pigs are oustanding examples of species in which the olfactory and tactile functions of the snout are highly developed. In the rooting pig the cortical area for the snout is proportionally larger

8 428 DAVID G. MOULTON' than in any other ungulate, and exceeds that for the rest of the body combined. Thus, in terms of tactile function, the pig's snout is perhaps analogous to the human hand. But, in a rooting animal, the snout must often extract tactile and olfactory information stimultaneously, and the two inputs are doubtless closely integrated. We may be justified, therefore, in speaking ol a chemotactile sense. Prominent olfactory and trigeminal supplies to the snout are also found in the opossum and a number of soricid shrews. In the platypus, Smith (1910) describes the trigeminal nerve as enormous, and claims that the snout is one of the most sensitive tactile organs found in any vertebrate. Similarly Echidna, with well-developed olfactory bulbs, has an extensive beak representation in the sensory cortex. REFERENCES Allen, G. M. A Bats. Harvard Univ. Press, Cambridge, Mass. Allison, A. C The morphology oc the olfactory system in the vertebrates. JJiol. Rev. 28: Allison, A. C, and R. T. T. Warwick Quantitative observations on the olfactory system of the rabbit. Brain 72: Bekesy, G. von Olfactory analogue to directional hearing. J. Appl. l'hysiol. 19: Breathnach, A. S The cetacean central nervous system. Biol. Rev. 35: Craig, A. B., M. Dvorak, and F. J. Mcllreath Resistance to airflow through the nose. Ann. Otol. Rhinol. Laryngol. 74: Crosby, E. C, and T. Humphrey Studies of the vertebrate telencephalon. 1. The nuclear configuration of the olfactory and accessory olfactory formations and of the nucleus olfactorius anterior o certain reptiles, birds and mammals. J. Comp. Neurol. 71: Dieulafe, L Morphology and embryology of the nasal fossae of vertebrates. Ann. Otol. Rhinol. Laryngol. 15: Graziadei, P Electron microscope observations of the olfactory mucosa of the mole. J. Zool. (London). 149: Johnson, T. N The olfactory centers and connections in the cerebral hemisphere of the mole. (Scalopus aquatictis machrimis). J. Coinp. Neurol. 107: (ones. F. R. H Reactions of fish to stimuli. Proc. Indo-Pacif. Fish. Conn. 8: Klein, E The organ of Jacobson in the dog. Quart. J. Microscop. Sci. 22: Lauruschkus, G Ober Riechfeldgrosse und RiechfcldkoeHi/.ient bci einigen Hunderassen mid dev Kat/e. Arch. Tierhcilk. 77: Lohinan. A. H. M.. and Laminers. H On tlie structure and fibre connections of Ihe olfactory centres in mammals, p In V. Zotternian, fed.], Sensory mechanisms, Progr. in Brain Research, vol. 23. Elsevier Publishing Company, Amsterdam. Mann, G Bulbus olfactorius accessorius in Chiroptera. J. Comp. Neurol. 116: Moulton, 1). G., and D. Tucker Electrophysiology of the olfactory system. Ann. N. Y. Acad. Sci. 116: Moulton, D. G., and L. M. Beidler Structure and function in the peripheral olfactory system. Physiol. Rev. 47:1-52. Moulton, X). G. 1967a. The interrelations of the chemical senses, p In M. R. Kare and O. Mailer, [ed.]. The chemical senses and nutrition. Johns Hopkins Press, Baltimore. Moulton. D. G. 1967/?. The measurement of spike activity telemetered from the olfactory bulb, and behavioral response to odorants in rats and rabbits. In. N. Tanyolac, fed.], Odor theories and odor measurement. Proc. NATO Advanced Study Inst. Symp., Istanbul, (In press). Negus, V Comparative anatomy and physiology of the nose and paranasal sinuses. E. & S. Livingstone, Ltd., Edinburgh. 402 pp. Negus, V Further observations on the air conditioning mechanism of the nose. Ann. Roy. Coll. Surg. Eng. 27: Nelson, J. E Behaviour of Australian Pteropodidae (Megachiroptera). Animal Behav. 13: Quilliam, T. A The mole's sensory apparatus. J. Zool. (London) 194: Scalia, F Some olfactory pathways in the rabbit brain. J. Comp. Neurol. 126: Skutt, H. R., R. G. Beschle, D. G. Moulton, and W. P. Koella New subminiature amplifier transmitters for telemetering biopotentials. Electroenceph. Clin. Neurophysiol. 22: Smith, G. E Jacobson's organ and- the olfactory bulb in Ornithorhynchus. Anat. An/.. 11: Smith, G. E Some problems relating to the evolution of the brain. The Lancet 1: Stephan, H. von Der Bulbus olfactorius accessorius bei Insektivoren und Primaten. Acta Anat. 62: Stephan, H., and O. J. Andy Quantitative comparisons of brain structures from insectivores to primates. Am. Zoologist 4: Tucker, D. 1963a. Olfactory vomeronasal and trigeminal receptor responses to odorants, p In Y. Zotterman, fed.], Olfaction and taste. Perganion Press, Oxford, England. Tucker, D. 1963b. Physical variables in the olfactory stimulation process. J. Gen. Physiol. 46:

9 OLFACTION IN MAMMALS 429 Whittcn. \V. K. 1966a. I'heromones and mammalian Whitten, W. K. 1966ft. l'ersonal communication, reproduction, p In Anne McLaren, [ed.], Wieland, C Inaug.-Dissertation., Berlin. Advances in reproductive phjsiology, vol. 1. (Cited by Laiiiuschkus, 1942). Academic Press, New York.

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