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Social interaction in nonhuman primates: an underlying theme for primate research.

Social living is assumed to be a critical feature of nonhuman primate existence inasmuch as most primate species live in social groups in nature. Recent USDA legislation emphasizes the importance of social contact in promoting psychological well-being and recommends that laboratory primates be housed with companions when consistent with research protocols. Our goals were to examine the link between social housing and psychological well-being and to explore the idea that research may be compromised when primates are studied in environments that vary too greatly from their natural ecological setting (individual cage housing versus group housing). Three general points emerge from these examinations. First, providing companionship may be a very potent way in which to promote psychological well-being in nonhuman primates; however, social living is not synonymous with well-being. The extent to which social housing promotes psychological well-being can vary across species and among individual members of the same species (for example, high- and low-ranking monkeys). Secondly, housing conditions can affect research outcomes in that group-housed animals may differ from individually housed animals in response to some manipulation. Social interaction may be a significant variable in regulating the biobehavioral responses of nonhuman primates to experimental manipulations. Finally, a larger number of socially housed subjects than individually housed subjects may be necessary for some biomedical research projects to yield adequate data analysis. Thus, social living has significant benefits and some potential costs not only for the animals themselves, but for the research enterprise.

Animals

Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca.

As the first part of a comparative investigation of primate frontal cortex, we compared the frontal architectonic organization of Galago, a small-brained, strepsirhine (or "prosimian") primate, to that of an anthropoid primate, Macaca, by using myelin- and Nissl-stained material. We were able to distinguish many more areas in both taxa than have been recognized in most previous studies of the primate frontal lobe. In particular, we were able to subdivide many of the areas shown in the commonly cited architectonic map of Walker (J. Comp. Neurol. 73:59-86, 1940). Delineation of areas was greatly facilitated by the use of the Gallyas technique for staining myelin. The areal organization of much of frontal cortex (specifically, the premotor, orbital, and medial regions) appears to be very similar in Galago and Macaca. In these regions, we were able to recognize the same complement of areas in both taxa, with few exceptions. In the granular frontal cortex (GFC), by contrast, we were able to distinguish about twice as many areas in Macaca as in Galago. For most of the GFC areas of Galago, there are architectonically similar areas in Macaca; the areas shared by both taxa correspond mainly to the arcuate and superior areas of Macaca (i.e., the region encompassed by Walker's areas 45, 8A, and 8B). However, there are many additional, more rostral, areas in Macaca for which there are no obvious homologues in Galago. In particular, Galago lacks cortex resembling the distinctive, lightly myelinated cortex of the Macaca principal sulcus (Walker's area 46 and its subdivisions). Our results are difficult to reconcile with the view that frontal lobe organization varies little across taxa. Rather, they suggest that granular frontal cortex underwent considerable change during primate evolution, including the addition of new areas in anthropoids.

Animals

The skin primates. XLIV. Numerical taxonomy of primate skin.

Data on 84 characteristics of the skin of 36 species of primates were extracted from a series of articles describing the histological and histochemical properties of the skin of primates. The data were subjected to a cluster analysis. The results were in reasonably good agreement with orthodox primate taxonomies although some exceptions were apparent. The species clustered into four main groups approximately comparable to Prosimii, Cercopithecoidea, pithecoidea, and Hominoidea are commensurate with standard taxonomic practice. Within the Ceboidea, however, the Atelinae and Alouattinae tend to group with the Hominoidea, Aotus and Saimiri show variable placements, and Callimico groups with the Callithricidae.

Animals

Architectonics of the parietal and temporal association cortex in the strepsirhine primate Galago compared to the anthropoid primate Macaca.

A number of higher order association areas have been described in the parietal and temporal cortex of large-brained anthropoid primates such as Macaca. However, little is known about the evolution of these areas, and the existence of homologous areas has not yet been clearly demonstrated in other mammalian groups. We addressed this issue by comparing the myelo- and cytoarchitecture of posterior association cortex in the anthropoid Macaca to that of the small-brained, strepsirhine ("prosimian") primate Galago. Our results suggest that Galago possesses many, if not most, of the areas present in Macaca. We were able to identify regions in Galago which resemble Macaca posterior parietal area 7, superior temporal polysensory cortex (ST), inferotemporal visual cortex (IT), the temporoparietal auditory area (Tpt), and posterior parahippocampal cortex (areas TH and TF). Area 7, ST, and IT can each be subdivided further in Macaca, and for most of these subdivisions we were able to identify counterparts in Galago. However, we could not distinguish as many divisions of ST cortex in Galago as in Macaca, and it is possible that new areas arose in this region during anthropoid evolution. There also appear to be general differences in architectonic organization between these animals, with Macaca exhibiting greater development of pyramidal layer IIIc and of the internal granular layer (IV) across much of the parieto-temporal cortex. These findings suggest that many, although possibly not all, of the parietal and temporal association areas present in the modern anthropoid Macaca evolved early in primate history, prior to the divergence of the lineages leading to strepsirhines and anthropoids.

Animals

Ipsilateral cortical connections of granular frontal cortex in the strepsirhine primate Galago, with comparative comments on anthropoid primates.

Modern studies of granular frontal cortex (GFC) in large-brained, anthropoid primates, such as Macaca, indicate that this region is comprised of many areal subdivisions. These areas vary in their architectonic appearance and each has a distinctive, diverse set of corticocortical connections. The great extent of the GFC region in anthropoids, and its high degree of areal parcellation, suggest that some GFC areas may be specializations of anthropoids, not found in other mammals. To investigate this possibility, we studied the corticocortical connections of GFC in the relatively small-brained, strepsirhine primate Galago, with a series of eight tracer injections in the frontal cortex, and an additional eight injections of parietal and temporal cortex. Tracers used were wheat-germ agglutinin conjugated to horseradish peroxidase and tritiated amino acids. Our results indicate that Galago GFC has strong, reciprocal connections with the parietal area-7 complex and with higher-order temporal areas; there are additional connections with extrastriate visual cortex, parahippocampal, and cingulate areas, and frontal cortex. Thus GFC has an extremely diverse array of cortical connections in Galago, as in Macaca. However, we also found that the pattern of parietofrontal connections is simpler in Galago than in Macaca. Specifically, parietal areas project to fewer discrete zones within the GFC of Galago, consistent with the view that these animals have fewer GFC areas than Macaca. In addition, Galago GFC possesses connections that specifically resemble those of Macaca arcuate cortex, but lacks connectional patterns that are characteristic of principalis cortex. These results are in accord with our previous architectonic studies, which indicated that Galago does not possess homologues of principalis areas. We conclude that the arcuate areas are common elements of primate GFC organization, while the areas located within and adjacent to the principal sulcus are anthropoid specializations.

Animals

Evaluation of the sub-human primate tube test for pregnancy in primates.

A haemagglutination inhibition test, developed specifically for primates, diagnoses early pregnancy in the chimpanzee, gorilla, orang-utan and baboon. The test was sensitive and reacted positively when the concentration of gonadotrophin in urine was equivalent to 0.03 i.u. human chorionic gonadotrophin per ml. This degree of sensitivity and the certitude that it cross-reacts with primate luteinizing hormone probably accounts for most of the false positive results.

Animals

Studies on the biosynthesis of pulmonary surfactant. The role of the methylation pathway of phosphatidylcholine biosynthesis in primate and non-primate lung.

The relative importance of the choline incorporation and methylation pathways of phosphatidylcholine biosynthesis was studied in the rat, rabbit, rhesus monkey and human lung. In vitro studies showed that phosphatidylethanolamine methyltransferase activity in the lungs of all species was only a fraction of that in rat liver. In vivo experiments were carried out to study the incorporation of an intravenously administered equimolar mixture of L-[methyl-14C]-methionine and [methyl-3H] choline into lipid inthe lung and liver of the rabbit and monkey. Over 90% of the total radioactivity incorporated into lipid was found in phosphatidylcholine. In the liver, methionine incorporation was 40--71% of that of choline in the rabbit and 99--120% in the monkey while in the lungs of both species it was less than 3%. On a weight basis, choline incorporation in the lung was 2--4 times that in the liver. These findings suggest that the methylation pathway is of little quantitative significance in the biosynthesis of phosphatidylcholine in primate and non-primate lung.

Animals

Primate retroviruses: immunological cross-reactivity between major structural proteins of new and old world primate virus isolates.

The major 35,000-molecular-weight internal antigen (p35) of the squirrel monkey retrovirus (SMRV) was isolated and partially characterized. Immunological analysis of SMRV p35 led to the demonstration of antigenic determinants common to SMRV and the Mason-Pfizer monkey virus (MPMV). A broadly reactive competition immunoassay was developed utilizing antiserum to MPMV to precipitate 125I-labeled SMRV p35. Although the major structural proteins of MPMV and SMRV competed with equal efficiency in this assay, type B and type C oncornavirus proteins lacked detectable reactivity. Antibodies reactive with the major structural proteins of both MPMV and SMRV were observed in sera of several normal rhesus monkeys with known prior exposure to MPMV-infected animals. These findings demonstrate the ability of sera from naturally immunized primates to recognize broadly reactive interspecies antigenic determinants shared by the major structural proteins of type D oncornaviruses, and they suggest possible horizontal transmission of MPMV among rhesus monkeys. Although sera from a number of squirrel monkeys contained antibody to SMRV p35, the possibility that this latter reactivity was due to endogenous virus activation rather than horizontal transmission cannot be ruled out.

Animals

Vitamin C deficiency in captive nonhuman primates fed commercial primate diet.

Scurvy was diagnosed in 19 rhesus monkeys (Macaca mulatta) and four squirrel monkeys (Saimiri sciureus) from a colony of nonhuman primates maintained on a commercial diet. Signs of weakness, reluctance to move, gingival hemorrhage, bruising, proximal and distal metaphyseal fractures, weight loss and anemia appeared in juvenile and young adult rhesus monkeys over a 2 week period. Clinical signs subsided after 5 days of vitamin C therapy. At the same time, cephalohematomas and weakness developed in squirrel monkeys, which failed to respond to treatment. These cases were associated with manufacturer's admitted error in preparation of the commercially prepared monkey diet.

Anemia

[Comparative anatomy of the tongue of Pan troglodytes (Blumenbach, 1799) and other primates. II. Findings in other primates].

This 2nd part of our studies shows that the papilla foliata is fully developed in Pan, Cebus, and Macaca; in Prosimians the papilla foliata is well developed in Lemur and Chirogaleus. In Galago crassicaudatus, this papilla is missing. Among 3 individuals of Microcebus, the papilla foliata was differently developed: in 2 cases, the tongue exhibited only 2 on both sides and a very low folia. Taste buds were found in the epithelium of only one side of each folium. In the 3rd case, the folia of the papilla were developed only on one side of the tongue, whereas, on the other side, a typical papilla was missing. Instead of the papilla, the tongue of the same animal exhibited a hillock-like structure; it is a gustatory hillock which exhibited many taste buds. There were 3 gustatory hillocks in all of the specimens of Tupaia glis; they are situated on both sides of the tongue.

Animals

Thermal inactivation study of glutathione peroxidase and glutathione reductase activities in lenses of primates and non-primates.

Heat lability studies of glutathione peroxidase and glutathione reductase activities were conducted on rabbit, sheep, rat, human, galago, cat and rhesus monkey lens supernatants. These species represent five mammalian orders. Incubation periods were 10.0 minutes in duration, with temperatures ranging from 25-100 degrees C (depending on which enzyme was being investigated). Results obtained for glutathione peroxidase activity demonstrated nearly identical heat lability profiles for human and rhesus monkey lenses. Both species were extremely labile to heat, losing activity at 30 degrees C and becoming totally inactive at temperatures of 50 degrees C (rhesus monkey) and 55 degrees C (human). Their profiles were very dissimilar to those of the other five species investigated, providing evidence for the existence of an evolutionary break. Glutathione reductase activity was extremely stable under conditions of highly elevated temperature for all seven species investigated. The human lens enzyme, the most stable of the species, maintained nearly 100% of its original activity up to 65 degrees C. Lenticular glutathione reductase activity did not reach zero levels in any of the seven species until a temperature of at least 80 degrees C was attained.

Animals

The neuroanatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in Old World and New World primates.

Pathways between the dorsal lateral geniculate nucleus (dLGN) and visual cortex in Old World (Macaca, Papio, Erythrocebus, Cercopithecus) and New World (Saimiri, Cebus) primates were studied after injections of horseradish peroxidase and H3 or S35 amino acids into the dLGN or visual cortex. Trans-synaptic autoradiography was also used to study these pathways after an injection of H3 proline-fucose into one eye. The subsequent autoradiographs of visual cortex showed that Old World primates have separate eye inputs (ocular dominance columns) in the striate cortex, whereas New World monkeys have overlapping or non-separated eye inputs. In both primate groups the geniculocortical input to layer IVA formed a pattern which resembled a honeycomb in tangential sections, unlike the solidly labeled layer IVC. Also common to the two primate groups was a projection from dLGN to layer VI. There was no dLGN projection to any prestriate area in any of the primates. However, after an injection limited to the prestriate cortex of Macaca, light autoradiographic labeling was seen in the interlaminar zones and the magnocellular and S laminae, demonstrating a prestriate-dLGN pathway. Our results indicate that the primate visual system differs significantly from the cat in having no dLGN projection to area 18. There are also signficant differences between primates in the level at which the possibility of binocularity (of an excitatory nature) first occurs in the striate cortex because in the species studied thus far with neuroanatomical methods, Old World primates have ocular dominance columns in layer IV but most New World monkeys lack them.

Animals