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Squirrel Monkeys and Space Motion Sickness

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Squirrel Monkeys and Space Motion Sickness Japanese Journal of Physiology, 52, 1–20, 2002 REVIEW Squirrel Monkeys and Space Motion Sickness Kenichi MATSUNAMI Science and Technology Promotion Center, Kakamigahara, 509–0108 Japan Abstract: Studies of the vestibular system in system is crucially important in the genesis of squirrel monkeys in consideration of space mo- SMS (SAS). In this connection, the ablation stud- tion sickness (SMS) or space adaptation syn- ies of labyrinth, semicircular canals, and other drome (SAS) were reviewed. First, the phyloge- SAS-related areas were referred to, and consid- netic position of the squirrel monkey was consid- eration was made for experiments about caloric ered. Then the anatomico-physiological studies irrigation of the ear. A hypothetic model was then of both the peripheral and the central vestibular proposed for the genesis of SAS. [Japanese systems were described, because the vestibular Journal of Physiology, 52, 1–20, 2002] Key words: squirrel monkey, vestibular system, cerebral cortex, space motion sickness (SMS), space adaptation syndromes (SAS). The construction of the new space station will be contamination of fatal B virus for human subjects; (4) completed soon, and many experiments will be under- They are relatively free from dysentery or tuberculo- taken. Many Japanese scientists will join in these new sis; (5) They are less dangerous because of their small experiments. Animal experiments are expected to size. On the other hand, (1) They are small and weak, solve problems in space physiology. Several kinds of thus vulnerable to bleeding during surgery; (2) The nonhuman primates such as the chimpanzee (Pan bone of the skull is thin, and it is difficult to perma- troglodytes), common squirrel monkey (Saimiri sci- nently anchor a cylinder to the skull for a continuous urea), rhesus monkey (Macaca mulatta), and stump- recording of neuronal activity; (3) They are expensive, tailed monkey (Macaca speciosa) have already been particularly in Japan, because of their high mortality used. The rhesus monkey is the commonest and best- rate during importation from South America. known nonhuman primate used in the research of Several reviews and monographs relating to the space physiology as well as in medicine. squirrel monkey and space medicine follow. Although In this article, however, we will report on experi- it is old, “The Squirrel Monkey” [1] is a book worth ments conducted with squirrel monkeys in relation to consulting before undertaking experiments with this space motion sickness (SMS) (or space adaptation monkey. The 12th chapter of the monograph is de- syndrome (SAS)—hereafter, SAS will be used in the voted to space medicine. As for other species of mon- same sense), since they are among the most appropri- keys, refer to the work of Simonds and Bourne [2]. ate animals for experiments on earth and in the space Several works are also related to space medicine station for the following reasons: (1) They are com- [3–11]. monly used in the research of SAS; (2) They serve as appropriate experimental animals because of their Evolution and Phylogeny small size and light weight; (3) They are safe from the The squirrel monkey belongs to the New World mon- Received on September 25, 2001; accepted on December 21, 2001 Correspondence should be addressed to: Kenichi Matsunami, Science and Technology Promotion Center, Kakamigahara, 509–0108 Japan. Tel: 181–583–79–2221, Fax: 181–583–79–2258, E-mail: [email protected] Abbreviations: aVOR, angular vestibulo-ocular reflex; ChAT, choline-acetyl transferase; CV, covariance; FPN, floccular projection neurons; FTN, floccular target neurons; Ig, granular insular cortex; IVN, inferior vestibular nucleus; LVN, lateral vestibular nucleus; MLF, medial longi- tudinal fascicules; MVN, medial vestibular nucleus; OKAN, optokinetic after nystagmus; OKN, optokinetic nystagmus; PIVC, parieto-insular vestibular cortex; PPH, nucleus prepositus hypoglossi; Ri, retroinsular cortex; SAS, space adaptation syndromes; SI, SII, somatosensory area I and II; SMS, space motion sickness; SVN, superior vestibular nucleus; VCR, vestibulo-collic reflex; VOC, vestibulo-oculo-collic; VOR, vestibulo-ocular reflex; WBR, whole body rotation; YPN, y-group projection neurons; 2V, vestibular area of area 2; 3aV, vestibular area of area 3a. Japanese Journal of Physiology Vol. 52, No. 1, 2002 1 K. MATSUNAMI keys (the Platyrrhini), more specifically to Cebidae/ cord and cerebellum, the indices are capuchin monkey Cebidae/Cebina/Saimiri (cf. Napier and Napier [12]). (347), squirrel monkey (545), rhesus monkey (321), The common squirrel monkey (Saimiri sciureus) is chimpanzee (135), gorilla (150), and man (210). It can the one we usually see in zoos and remember as the be seen that the squirrel monkey has the largest pro- first monkey to travel into space in an American satel- gression index, except for the superior vestibular nu- lite (1958). The genus of Saimiri comprises three cleus. It must be also pointed out that the talapoin of species: S. sciureus, S. boliviensis, and S. oerstedi. In the Cercopithecus family (Cercopithecus talapoin), its customary classification, it is also known as Boli- also an arboreal habitant, is the only monkey that vian, Peruvian, or Colombian, depending on its native shows a progression index superior to the squirrel habitat. The Bolivian is considered the most sensitive monkey. to motion sickness. Here we briefly discuss the growth of the squirrel When considered from an evolutionary viewpoint, monkey, since we have no other appropriate place for the squirrel monkey shows some unique features, for it in this article. The squirrel monkey becomes adult example, the evolution of the primate brain according at 3 years old (body weights are 0.6–1.1 kg [male] and to Stephan [13]. The ratios of brain weight to body 0.4–0.8 kg [female]), and the average life span is 15 weight (brain [g]/body [g] are: howler monkey years for the Bolivian squirrel monkey [15]. It was fed (Alouatta, 51/6,40050.0080), capuchin monkey (Cebus, by standard commercial food pellets in a warm room 80/3,00050.0226), squirrel monkey (Saimiri, 22/6805 (recommended room temperature 26°C). In addition, 0.0324), rhesus monkey (M. mulatta, 93/6,0005 mill worms were supplied for enough protein (1 mill 0.0155), chimpanzee (P. troglodytes, 420/46,0005 worm/d). 0.0091), gorilla (Gorilla gorilla, 465/124,00050.0037), and man (Homo sapiens, 1,330/65,00050.0205). It is Anatomy of Vestibular System curious that the squirrel monkey is superior even to Two main hypotheses have been proposed for the eti- human beings in its brain weight in relation to body ology of space adaptation syndromes (SAS); i.e., the weight. However, it is only true for the progression sensory conflict theory and the fluid shift theory. Fur- index proposed by Stephan, which defines it as the thermore, the asymmetry of the left and the right ratio of the volume (which is almost equal to the otolith and the production of chemical substances in weight) of the part of the brain of the respective pri- the central spinal fluid have also been proposed. Nev- mate species to the volume of that of the most primi- ertheless, the vestibular system plays a pivotal role in tive and “imaginary” insectivora. Therefore a more the genesis of SAS; thus the anatomy of the vestibular appropriate index must be developed to distinguish system has been widely reported [16–21]. Further, an the memory and learning capability among primates. atlas of the brain of the squirrel monkey is indispens- Since the focus of the present article is on space able to research of the central nervous system [22]. physiology, especially SAS, we will consider the pro- Measurements of the vestibular organ have been gression index of the vestibular nuclear complex. The obtained in the cat, squirrel monkey, and man. The di- progression index of some representative primates ameter of the monkey’s ampulla is 1.28 mm. The [14] is capuchin monkey (Cebus albifrons; 361), squir- height of the crista is 0.23 mm, and the thickness is rel monkey (419), rhesus monkey (329), chimpanzee 0.23 mm. Other figures were obtained [23–25]. The (205), gorilla (154), and man (262). It is clear from size of the human maculae was twofold to fourfold these indices that arboreal primates have a higher pro- greater [26]. The surface area of the sacculus is gression index. Concerning the superior vestibular nu- 0.73 mm2. These values are 60–70% of those of man cleus, which mainly projects to the oculomotor nuclei and are relatively larger when the size of the skull is and is important to the vestibulo-ocular reflex, the compared to that of man [23, 26]. The plane of the progression index is capuchin monkey (542), squirrel horizontal semicircular canal tilts upward by monkey (531), rhesus monkey (471), chimpanzee 18–22 deg from the stereotaxic horizontal plane for (292), gorilla (152), and man (247), reflecting the vi- both the squirrel and rhesus monkeys. Taking these sual and vestibular dominance of the arboreal pri- values into account, a nose-down tilt of 15 deg is rec- mates. Concerning the medial vestibular nucleus, ommended for the most effective horizontal canal which is important to the vestibulo-collic reflex, the stimulation [27]. Morphological measurements of progression indices are capuchin monkey (348), squir- each angle were similarly made among the anterior, rel monkey (369), rhesus monkey (262), chimpanzee posterior, and horizontal semicircular canals. Two (224), gorilla (152), and man (247). Concerning the types of sensory hair cells exist in the sacculus and lateral vestibular nucleus, which projects to the spinal the utriculus. Type I hair cells are covered by the calyx 2 Japanese Journal of Physiology Vol. 52, No. 1, 2002 Squirrel Monkey in Space Physiology and situated more in the central part of the crista. Type Ultracytochemically ouabain-sensitive, K1-depen- II hair cells lack the calyx.
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