The Functions of the Olfactory Parts of the Cerebral Cortex

Home , Olfactory system, Pallium (neuroanatomy)

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 superficial 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 dominated 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 organization. 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

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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 representation. 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 localization 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 exteroceptive 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 subcortical reflex connections is surprisingly constant from the lowest to the highest vertebrates. But smell is even more important as an exteroceptive 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 activators of complex sensorimotor systems whose pattern of performance is determined primarily by other senses with sharper localization both physiologically 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 excitations and bodily movements as may be in process. The preceding discussion relates to subcortical -activities which are common to fishes and men. It evidently has a bearing on the significance Downloaded by guest on October 1, 2021 VOL. 19, 1933 ANATOMY: C. J. HERRICK 11 of the olfactory cortex if we recall that in phylogeny the-entire cortex was differentiated within and finally emerged from an olfactory field. In the lower Amphibia, where there is no differentiated cortex, the pallial part of the cerebral hemisphere can be readily recognized, and the whole of this field is clearly under strong olfactory dominance. Within this field well differentiated cortex appears in reptiles, and the whole of this cortex is again probably under strong olfactory influence. It is questionable whether anything properly called neopallium is present below the mammals, and, as already pointed out, in the lowest surviving mammals the olfactory cortex is more massive and far more highly specialized than the neopallium. In the Amphibia, where cortex is not differentiated, there is no evidence that the olfactory influence upon one part of the pallial field is physiologically different (except in intensity) from that of any other part. Such incomplete differentiation of pallial fields as is apparent here has taken place under the influence of penetration of various systems of non-olfactory projection fibres into the pallial field, and this is probably true throughout all later phylogenetic stages. In Amphibia we see the beginning of penetration of exteroceptive systems of thalamic projection fibres into the pallial field, and in reptiles this is more extensive; but in neither of these cases is any region of the pallial field set apart as the exclusive receptive center for these fibres, nor within the thalamic radiations are the various sensory systems (touch, vision, etc.) segregated each with its own cortical projection center. This segregation and cortical localization does appear in mammals, and this marks the emergence of neopallium as contrasted with the "general cortex" of the reptilian dorsal pallial area. The most primitive cortex, then, is an olfacto-cortex, that is, cerebral cortex in which olfactory connections and functions are well represented throughout its extent. But no degree of elaboration of olfactory apparatus alone has ever in any known animal given rise to cerebral cortex. Associ- ation is a characteristic cortical function, and this implies diversity in the things associated. Cortex does not appear in the pallial part of the olfactory field of any lower vertebrate unless and until several strong systems of non-olfactory projection fibres penetrate the pallium and have definite and separate localization within it. Association between these physiologically different pallial areas has value for behavior. These areas are different in their non-olfactory connections, even though olfactory connections are common to all of them. What, then, is the significance of these olfactory connections? It seems probable that here, as in the subcortical field, olfactory impulses serve as activators of complex sensorimotor systems whose pattern of performance is largely determined by the non-olfactory members of the complex. This function, of course, is in addition to any specific olfactory Downloaded by guest on October 1, 2021 12 ANA TOMY: C. J. HERRICK PROC. N. A. S. reactions that may be present. In reptiles there are from three to six incompletely separated cortical areas with different subcortical connections, all of which are under some olfactory influence and are structurally similar to the simplest olfactory cortex known in mammals. The supposed primordium of the neopallium at the anterior end of the dorsal area of "general cortex" is reached by thalamic projection fibres, and these so far as now known belong to the somesthetic system. If optic, auditory or other exteroceptive systems are represented, these have no localized cortical area of their own. Such a cortex can have very little efficiency as an analyzer of experience. Probably all parts of it are activated by olfactory impulses, some more, some less. In the three chief projection areas they are combined with different aggregates of non-olfactory excitations, and all of these interact one with another through the associational apparatus. The net result of the total cortical activity would probably be in the main a differential inhibition or reinforcement of subcortical adjustments already in process with a minimum of either analytic or synthetic specificity within the cortex itself. In other words, this primitive type of cortex would tend to act as a whole to influence responses to external stimulation whose specific pattern is determined subcortically. There is doubtless some specificity of cortical reinforcement and inhibition, but so far as can be inferred from structural arrangement this can be only of very general sort. In even the lowest of the mammals there is a tremendous advance. The neopallial field is well defined and within it are clearly localized somesthetic, optic and auditory areas, each with its own system of thalamic projection fibres, and there is a much larger mass of intrinsic associational apparatus. The olfactory cortex shows still greater advance, and indeed it has already reached the culmination of its differentiation. This differentiation shows an elaborate apparatus for summation and intensification of olfactory excitations and little evidence of patterns of cortical localization. Such histological localization as is apparent is chiefly at the margins of the olfactory field wbere neopallial connections are strongly developed and of different composition depending on the localization patterns of the adjoining neopallium. In sharp contrast with this arrangement, the definite localization pattern of the neopallium indicates that this cortex can now perform the functions of an analyzer in simple situations. It can probably also initiate new patterns of behavior ("insight" of Kohler or "reasoning" of Maier); but this synthetic function is meagerly represented and moreover it is held in abeyance under ordinary conditions by the enormous preponderance of the olfactory type of cortex. These inferences drawn from structural arrangements are supported by what experimental evidence we have of cortical participation in behavior Downloaded by guest on October 1, 2021 VOL. 19, 1933 ANA TOM Y: C. J. HERRICK 13 patterns of lower mammals, such as opossums and rats. Here there is evidence that the cortex exerts some relatively non-specific influence upon learning and remembering; and, in the simpler situations especially, this is in large measure independent of the localization pattern. The whole cortex seems to act as a differential activator or inhibitor. But this is not all of the story, for in certain types of experitrent, and especially in more complicated problem situations, the cortical participation is of different type. The localization pattern enters into some of these situations, indicating that the analysis of peripheral experience by the sense organs is maintained up to the cortical level and here synthetically recombined in new patterns. This gives "insight." It is this synthetic function which is enlarged in higher mammals and this implies cortical representation of peripheral localization, so that the outer world is correctly and adequately mirrored in the inner (cortical) experience. This spatial representation of the outer world requires localization in space of the central apparatus, and this is what we find anatomically in the visual nervous pathways and centers preeminently. The experiments of Lashley and others show that cortical participation in the conditioning of visual habits is more definitely localized than of somesthetic habits like maze-running. It is perhaps significant in this connection that in most of the experiments designed to test the part played by the cortex of lower mammals in learning the ablation operations involve only the neopallium, leaving the olfactory cortex intact or but slightly injured. Under these conditions that part of the cortex which is preeminently non-specific in its normal function is still acting in full efficiency. It is true that the neopallium also contains a large amount of non-specific tissue which is physiologically equipotential, but this tissue, unlike that of the olfactory cortex, is set within a matrix of physiologically specific and localized projection cortex. It will be interesting to find out just what happens to these adjustments to external situations-problem boxes and the like-when the olfactory cortex is wholly removed, and the hippocampal and piriform parts sepa- rately, with the neopallium left so far as possible intact. These are difficult, but probably not impossible surgical operations. We have experimental proof that total destruction of both olfactory nerves impairs cortical efficiency in learning where smell is a factor in the process of conditioning, as, of course, is inevitable. But this operation sheds little light on other intrinsic functions of the olfactory cortex, for the associational connections of this cortex with the neopallium are very extensive and diversified and in an animal deprived of olfactory organs these connections are still intact. The "olfactory" cortex may exert a profound influence upon all neopallial activity even in an animal which is normally totally anosmic, as indicated by the preservation of well differentiated hippocampal cortex in the dolphin which has no olfactory apparatus. Downloaded by guest on October 1, 2021 14 ANA TOMY: C. J. HERRICK PROC. N. A. S. The inferences drawn from these considerations are: 1. In exteroceptive adjustments the olfactory sense, lacking localization of its own, cooperates with other senses in various ways, including a qualitative analysis of odors and the discrimination between desirable and noxious stimuli, activation or sensitizing of the nervous system as a whole and of certain appropriately attuned sensorimotor systems in particular, with resulting lowered threshold of excitation for all stimuli and differential reinforcement or inhibition of specific types of response. 2. Tissue differentiation within the pallial field began in phylogeny with the penetration into this part of the primitive olfactory area of various systems of non-olfactory projection fibres, resulting in more efficient adjustments (both interoceptive and exteroceptive) to all situations containing olfactory excitation. 3. In the course of differentiation of the cerebral cortex the olfactory system plays the dominant r6le in primitive types, to be reduced to a subordinate position in primates as the neopallium is expanded and differentiated. 4. At all stages of cortical elaboration an important function of the olfactory cortex, in addition to participation in its own specific way in cortical associations, is to serve as a non-specific activator for all cortical activities. This is a generalized activity of primitive type acting on the neopallial cortex as a whole, lowering its threshold or increasing its sensi- tivity, or, in the case of noxious stimuli, exerting inhibitory influence. This type of non-specific activity is one of the major functions of the olfactory cortex, though all parts of the neopallium also exhibit it to some degree. It comes to expression in overt behavior, learning capacity, memory, etc., as a differential influence upon other cortical and subcortical functions of those exteroceptive sensoriplotor mechanisms whose specific patterns of response show well defined anatomical and physiological localization. Having no localization pattern of its own, it may act in two ways: first upon other exteroceptive systems whose localized mechanisms are adapted to execute adjustments where external orientation is de manded, and, second, upon the internal apparatus of general bodily atti- tude, disposition and affective tone, the "intimate senses" of Starbuck. I This research was aided by a grant to the University of Chicago by the Rocke- feller Foundation. Downloaded by guest on October 1, 2021