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The Functions of the Olfactory Parts of the Cerebral Cortex

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The Functions of the Olfactory Parts of the Cerebral Cortex VOL. 19, 1933 ANA TOMY: C. J. HERRICK 7 THE FUNCTIONS OF THE OLFACTORY PARTS OF THE CEREBRAL CORTEX By C: JUDSON HERRICK DEPARTMENT OF ANATOMY, UNIVERSITY OF CHICAGO1 Read before the Academy, Tuesday, November 15, 1932 In reptiles and mammals the dorsal wall of the cerebral hemisphere which contains the superficial gray cortex is called pallium or mantle. In all amphibians and some fishes the corresponding part of the hemisphere can be identified as a pallial field or primordial pallium, even though super- ficial gray cortex is lacking or present in very rudimentary form. This identification is made on the basis of the position of this field and the anatomical arrangement of its nervous connections. Below the reptiles (Fig. 1) the entire pallial field is dominated by the olfactory system, for large numbers of fibres spread throughout its mass derived either directly from the olfactory bulb or from an anterior olfactory area closely adjacent to the bulb. In reptiles (Fig. 2) well defined cortex is differentiated throughout the pallial field and this cortex again is domi- nated by the olfactory system, though the dorsal one of the three chief cortical areas receives a much larger proportion of non-olfactory fibres than does the corresponding area of amphibians. This cortex is of very simple patterm, consisting of one thin layer of cells which are arranged in three chief sheets or areas-medially the archipallium (hippocampal cortex), laterally the palaeopallium-(piriform cortex), and between these the dorsal or "general" cortex which occupies the locus of the mammalian neopallium but has not attained the structure and connections characteristic of typical neopallium. Between existing reptiles and mammals is a wide gap in pallial organiza- tion. In all mammals the olfactory part of the pallium is quite sharply separated from the non-olfactory neopallium and the entire pallial field is greatly enlarged and structurally complicated. In the lowest extant mammals (Fig. 3) the olfactory part of the pallium has already attained enormous size and complexity, and from this point onward in phylogeny it is very conservative, with little change in its organization except such as is incidental to the enlargement of the neopallium or the reduction of the peripheral olfactory apparatus in some species. The neopallium, on the other hand, in primitive mammals is relatively small, in many cases being less extensive and less complicated than the olfactory pallium; but the mammalian series shows progressive increase in the size and complexity of the neopallium, which culminates in the human brain (Fig. 4) with upward of a hundred anatomically definable areas and a mass which makes up nearly half the total weight of the brain. Downloaded by guest on October 1, 2021 8 ANA TOMY: C. J. HERRICK PROC. N. A. S. This rapid elaboration of the neopallium within the single Class of Mam- malia is one of the most dramatic cases of evolutionary transformation known to comparative anatomy. Why, within the mammalian class, does the olfactory pallium culminate J orsal arec IxippocompaI dorsal cortex area hippocompol N a . .... area I 2 3 ~ 4 J $ Figures 1 to 4.-Diagrams showing approximately the relative extent of the olfactory and non-olfactory pallial fields as seen in cross-sections of various vertebrate brains. Figure 1, Necturus, with entire pallial field olfactory (X 12); figure 2, the box-tortoise, Cistudo, with differentiated cortex, all of which is under olfactory influence (X 7); figure 3, the opossum, Didelphis, with olfactory cortex (hippocampus and piriform) more extensive than non-olfactory cortex (neopallium) (X 4); figure 4, human, with enlargement of neopallium and reduction of olfactory cortex (X 1/2). in the lowest and earliest members and thereafter remain relatively sta- tionary while the neopallium exhiibits so amazing an enlargement and differentiation? Presumably the answer to this question is to be sought Downloaded by guest on October 1, 2021 VOL. 19, 1933 ANA TOMY: C. J. HERRICK 9 in the significance of the pallium to the mode of life and to changes in the pattern of adjustment. Clearly the relative part played by the sense of smell in adjustments mediated by the cerebral cortex is very different in lower members of the series and in higher. An analysis of cortical representation of the various sensory systems would seem to be an appropriate place to begin such an inquiry. First, it should be noted that the visceral, or interoceptive senses have meager cortical representation throughout the series; these internal adjustments are largely taken care of by subcortical nervous apparatus. The primary significance of the cortex, then, is to be sought in adjustments to external events as reported through the exteroceptive senses. Ancillary to these adjustments are the proprioceptive senses, which also have cortical repre- sentation. The external environment is so much wider than the internal that effective adjustment to outside events requires a more or less accurate localization of the source of the stimulus. Appropriate response to a tactile contact or cutaneous pain can be made only if the locus of the stimulus is accurately registered in the central adjustor. For the senses of hearing and sight peripheral localization is even more important, for the source of the stimulus may be far removed from the body in any direction. The movable external ears of most mammals assist in this orientation. In primates the eye is the preeminent distance receptor, and here localiza- tion within the peripheral field reaches its ultimate refinement and central localization of the visual nervous apparatus is correspondingly precise. The sense of smell stands in sharp contrast with these localizing extero- ceptive senses. The organ of smell is both an exteroceptor and an intero- ceptor. For the latter function its central con,nections within the brain are intimately bound up with all of the other nervous apparatus of feeding, nutrition and reproduction, and the neurological pattern of these sub- cortical reflex connections is surprisingly constant from the lowest to the highest vertebrates. But smell is even more important as an extero- ceptive sense, giving warning of enemies and other noxious things and guiding the animal to mates, food and other desirables. The curious thing about these exteroceptive olfactory functions is that they are carried on very efficiently despite the total lack of any capacity for localizing the source of the stimulus within the olfactory sense itself. Odors may be discriminated in terms of quality and intensity, but they cannot be localized in space. If the source of an odor is to be determined, we must use some other sense-sight, hearing or direction of wind-or else we must move our own bodies to and fro to judge relative intensities of the odor. Now all of these exteroceptive senses are highly developed in fishes and amphibians which lack well differentiated cerebral cortex; and of these, Downloaded by guest on October 1, 2021 10 ANATOMY: C. J. HERRICK PROC. N. A. S. in many of these animals, smell seems to be the dominant member. There is no evidence that the sense of smell of fishes differs essentially from our own and the close similarity of -the central connections of the olfactory system of fishes with the subcortical olfactory connections of man points in the same direction. In view of the obvious importance of olfaction in feeding, mating and avoiding reactions and in view of its lack of localizing efficiency, it is evident that in these animals the olfactory reactions typi- cally are not simple elementary reflexes but are ordinarily conjoined with other sensorimotor responses. What part do they play here? The central connections of the olfactory nerve in all vertebrates are characteristically diffuse, widely dispersed and interconnected with one another and with other sensory systems in an intricate web of correlation fibres. From this complex the more specific olfactory pathways converge into a few final common paths, chiefly by way of the mammillary bodies and the interpeduncular nucleus. The main motor outflow from these centers is into the apparatus of mass movement (locomotion and the like), and these final common paths are the same as those of the other extero- ceptors. Other olfactory outlets pass into the apparatus of various local reflexes, and here again they merge with the sensory systems which are the specific activators of these particular reflexes. There are some specific olfactory reflexes, like sniffing and nausea, but these are mostly visceral; when the organ of smell functions as a distance receptor the response is effected through final paths which are common to olfactory and other sensory systems and the pattern of response is determined by the conjoint action of all of these. These arrangements suggest that exteroceptive olfactory excitations (leaving out of account here the visceral reactions) serve chiefly as acti- vators of complex sensorimotor systems whose pattern of performance is determined primarily by other senses with sharper localization both physio- logically and anatomically. The histological structure of the olfactory centers favors both irradiation and summation or intensification (avalanche conduction of Cajal) and it provides no recognizable apparatus adapted for the preservation of sharply defined local patterns of excitation such as is so characteristic of optic pathways and centers. Our own experience, too, gives many instances when faint odors call forth various non-olfactory activities, conscious or unconscious, without exhibiting any characteristic behavior patterns of their own. The quality of the stimulus apparently determines whether it is followed by a seeking or an avoiding reaction; but other details of the pattern of performance, particularly the localization of the source of the stimulus, are contributed by such other sensory excita- tions and bodily movements as may be in process. The preceding discussion relates to subcortical -activities which are common to fishes and men.
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